Heleioporus australiacus australiacus ( Shaw & Nodder, 1795 )

Mahony, Michael J., Penman, Trent, Bertozzi, Terry, Lemckert, Frank, Bilney, Rohan & Donnellan, Stephen C., 2021, Taxonomic revision of south-eastern Australian giant burrowing frogs (Anura: Limnodynastidae: Heleioporus Gray), Zootaxa 5016 (4), pp. 451-489 : 476-478

Heleioporus australiacus australiacus ( Shaw & Nodder, 1795)

The Giant Burrowing Frog, Eastern Owl Frog

Figs 6 , 7 , 8 , 13 .

Synonymy from Cogger et al. (1983).

Rana australiaca Shaw & Nodder, 1795

Philocryphus flavoguttatus Fletcher, 1894

Heleioporus flavoguttatus Fletcher, 1898

Holotype. The original description by Shaw & Nodder (1795) was based on a plate of the species and drawings of the feet, hands and mouth ( Fig. 6A ) sent from New Holland (= Australia) ( Lee 1967). Moore (1961) noted that he had never found a reference to the existence of the type of Rana australiaca .

An important issue to address is whether the specimen from which the plate was drawn came from within the range of H. a. australiacus in the Sydney Basin bioregion or whether it could have possibly come from the range of H. a. flavopunctatus subsp. nov. in the south-eastern corner bioregion. There is no doubt that the drawing is of H. australiacus as several features such as the body form and proportions of the limbs, colouration and pattern, and the occurrence of the nuptial spines on the fingers are diagnostic. The drawing shows distinct nuptial spines on three fingers, and it is reasonable to consider that the subject was a male. The most distinctive feature between specimens of the two subspecies is the size of the yellow spots on the flanks. The plate shows these spots to be moderate in size and well-spaced, and there is no indication of larger spots or fusion of spots. This would indicate that the subject specimen was most likely from the Sydney region. We consider this assessment tentative since the plate is not a technical scientific drawing and does not show some features such as the glandular ridge at the posterior margin of the jaw, which is present in the majority of specimens we have examined. At the time the plate was drawn and presented to Shaw & Nodder (1795), Sydney was well established, but the southern coastline and hinterland was not so developed. On balance and given the level of exploration of southern Australia at the time the plate was drawn it seems unlikely that the location where the type was collected will ever be known.

In the absence of a type specimen and with the subdivision of H. australiacus we take the step to nominate a neotype for H. australiacus sensu stricto. We have chosen a specimen that is well preserved from within the known range within the Sydney Basin bioregion.

Designation of Neotype. AMS R104952 Adult male collected by G. Webb on 5 th October 1979 in Maroota State Forest , NSW, -33.5287°, 150.9865°.

Specimens examined. See Table 1 and Supplementary Table S1 for details of specimens examined.

Measurements of neotype (in mm), SVL 74.5, HW 30.9, HL 21.4, ED 8.3, EN 7.6, IND 7.93, TL 24.6, FL 30.6, IMT 4.6.

Description of neotype. The neotype (AMS R104952) is a large (SVL 74.5 mm) adult male ( Fig. 13A ). The body is rounded and robust, head wide (HW/HL 1.44), with short and robust limbs (TL/SVL 0.33). Arms and legs are thick and muscular with the maximum girth of the arms exceeding that of the legs. The head is rounded when viewed from above and deep when viewed laterally. The eyes are large and prominent (ED/EN 1.09). The pupil is vertical. Tympanum large, circular, slightly smaller than diameter of the eye and covered by skin with small tubercles. Sternum divided posteriorly.

Dorsal surfaces, including limbs and head, granular with many small tubercles. Upper flanks with larger tubercles ( Fig. 13B ). A glandular ridge, comprising a series of tubercles with a larger tubercle at the axil, extends from the side of the face below the midline of the eye to the axil. Scattered tubercles also occur on the chin, chest and posterior and inner surfaces of the limbs. Most small tubercles are dark with lightly pigmented tip. Ventral surfaces smooth, although there is wrinkling that has occurred in preservation. The cloaca has larger, elongated, contrastingly coloured tubercles and skin folds on both lateral sides inclined at an outward angle and extending up to the dorsal surface of the thigh ( Fig. 13C ). Numerous, smaller, rounded, non-contrasting coloured tubercles occupy remaining surfaces around the cloaca.

Hands are wide with short, rounded fingers and without webbing. The fingertips are rounded and ventrally resemble a tubercle but are not disc shaped, and two larger tubercles occur at the base of each finger. Palmar surface with a prominent inner-metacarpal tubercle at the base of finger one, with large tubercles at the base of each finger and smaller tubercles on the palm and finger joints ( Fig. 13D ). Slight lateral fringe on fingers two, three and four. Proximal half of finger one is almost twice as thick as the other fingers. Fingers sequence in length 3> 1> 2> 4.

Distinct, large, dark brown to black keratinized, conical, nuptial spines on the upper surface of the first three fingers. On the first finger a large spine occurs at the junction of the first phalange, and three smaller spines occur along the second phalange. On the second and third fingers there are 6 and 5 smaller spines, respectively.

The foot is broad, and the plantar surface is smooth. Upper surface slightly lighter tone than dorsum, without tubercles or spines. Toes short and robust, with rounded tips, and in size 4> 3> 5> 2> 1. No webbing between the toes. Large non-keratinized inner metatarsal tubercle much longer than the fifth toe, rounded on the apex, contrasting in colour to the plantar surface of foot ( Fig. 13E ). Large and forward inclined pointed tubercles at the base and joints on each toe. Tubercles between the junctions of all toes except 4 and 5.

Preorbital papillae comprises a large dark lobe with several small papillae along the base ( Fig. 8A ). Upper eyelid is darker than the background colouration. Nictitating membrane is milky (presumably transparent prior to preservation), with the upper margin darkly coloured. The vomerine teeth in two prominent transverse series extending from the midline to the posterior median border of the choanae.

Variation. A large (SVL, females mean = 70.4 mm, range = 60.5–77.6; males mean = 74.9 mm, range = 58.6– 90.8), rotund frog with stout body. The legs are stout and muscular (TL/SVL 0.28–0.39 in females and 0.27–0.42 in males). Males have thicker arms and musculature on the sternum. Head broad and short (HW/HL 1.31–1.59 in females and 1.1–1.6 in males). Viewed from the side the head is deep and blunt, the eyes prominent (ED/EN 1.09– 2.81). The snout is short with the nostrils closer to eyes than tip of snout. Males do not have a vocal sac.

The dorsal surfaces of the body and limbs are moderately granular with many small, rounded tubercles. The ventral surface is smooth with scattered tubercles on the chest and chin.

Both adult male and female individuals vary in the extent of the occurrence of black keratinised spines on tubercules from no spines through to prominent spines on varying combinations of body surfaces including the flanks, face, throat, chest, forelimbs and around the cloaca, and more rarely on the lateral aspects of the dorsum.

The iris is silvery, with irregular black lines extending throughout. Preorbital papillae in anterior corner of eye vary among individuals from a single flattened lobe to several globular lobes ( Figs. 8A–D ).

Males and females are significantly different in body size (SVL) ( Tables 5 & 6), and can be distinguished by some external morphological traits, especially during the breeding season. Girth of forelimbs exceeds girth of legs in mature males, less than girth of legs in females. Adult males have large, cone-shaped, black keratinized nuptial spines on fingers one to three with one or two large spines on the first finger, largest spine with bony core on metacarpophalangeal knuckle of first finger; black caps of spines may disappear out of breeding season. Small spines occur in the middle of the tubercles that cover the dorsal surfaces of the body and limbs, flanks, posterior of thigh especially around the cloaca, on the glandular ridge below the eye and tympanum and on the scapular and beneath the chin. These nuptial spines are absent in females although smaller spines on the dorsal surface occur in females.

Colour and pattern. Colouration and texture of the skin does not differ between the sexes. Dorsal surfaces of the body, head, limbs and hidden surfaces of the thigh and groin are brown to bluish black without larger blotches or patches. The dorsal surfaces of the hands and feet are a lighter shade of the dorsal colour with lighter white mottling, with a yellow spot on top of hand in some specimens ( Fig. 6A–H ). There are often poorly defined yellow or cream patches on the upper surfaces of the femur and humerus. There are many small raised rounded tubercles that are slightly darker in tone on the dorsum and overall provide a slightly shagreened appearance.

The dorsal colouration extends to mid-way down the flanks where it gradually transitions to the cream colour of the ventral surfaces. Above the insertion of the arm is also cream coloured. On the lateral surfaces the tubercles are larger than on the dorsum and most are capped with light-coloured spots, in some individuals they are yellow, others white and in others a mixture of white and yellow. The number of spots vary considerably (mean = 17 in females, 27 in males) however, in most cases they cover one tubercle and do not join adjacent spots to form larger spots. The mean size of coloured spots on the flanks is 1.1 mm in females and 1.3 mm in males. The spots are larger towards the groin. At the transition with the venter the larger tubercles are cream coloured.

In most specimens, a prominent yellow or cream coloured glandular ridge of larger interconnected tubercles extends posteriorly along the upper maxilla from below the eye to beneath the tympanum and terminating above the axil. The upper margin of the mandible has many fine tubercles and is yellow or white.

Ventral surfaces, including limbs, white to bluish white, tending towards transparent on the chest. The throat is washed with darker brownish colouration in males, immaculate in females. Ventral areas are smooth, except for the throat and anterior chest regions, which are sprinkled with whitish tubercles, which are tipped with tiny black spines.

Soles and palms lightly to darkly pigmented with the same colour as dorsum. The metatarsal tubercle is cream to brown, with other tubercles cream coloured.

The tubercles surrounding the cloaca with yellow or white spots that rarely coalesce to form a ring with a small gap at the top and bottom in most specimens ( Fig. 7A–H ).

The iris is finely reticulated silver grey. The nictitating membrane is transparent with a sharp black line on the upper margin.

Male call. The call is a low-pitched owl like “wup..wup..wup” sound (FrogID application) that is repeated in long sequences. The call comprises a single note made up of distinctive pulses and meets the description of pulse repetition in the sound categories of Beeman (1998). Call duration is less than half a second (mean 0.35 s, range 0.29– 0.42 s), and is composed of 4 to 5 pulses per call (mean 4.6, range 3.6–5.0). Inter-call duration varied considerably (28.0–37.6 calls per minute), and along with call duration and pulse repetition rate is dependent on temperature ( Table 8). The call is broadband, and the dominant frequency can vary considerably among populations (Supplementary Table S4). This species also produces the male aggressive call and defensive call like that described in H. a. flavopunctatus subsp. nov. ( Table 9, Fig. 12 ). We have not analysed a defensive call for this species.

Most locations had similar DF, however three locations in the mid-north of the range of H. a. australiacus in NSW (Ku-ring-gai Chase National Park, Wedderburn and Brisbane Waters National Park) showed markedly higher DF values (Supplementary Fig. S4 ; Supplementary Table S4; Supplementary Information 1). These higher DF values were accompanied by correspondingly higher means for the low (5%) and high (95%) frequency levels. The higher DF values observed at Ku-ring-gai Chase National Park are greater than can be explained by the variation possible in the fast-Fourier transformation (FFT) (RavenPro 1.6). For calls recorded at 4800 Hz, the FFT transformation at a sampling rate of 512 points with 50% overlap, has a resolution of 86.1 Hz, and at sampling rate of 1024 with 50% overlap the resolution is 43.05 Hz. Therefore, the observed differences (Ku-ring-gai 609.6 compared to 347.5 at Brisbane Waters National Park) are not explained by the level of resolution (43.05 Hz).

Breeding Biology. Anstis (2017) has described the breeding biology.

Distribution. There is a portion of the range for which we can be certain based on the genetic analyses; from Corrabare State Forest in the Watagan Mountains in the north (-32.93°, 151.20°) to Dharawal National Park on the Woronora Plateau in the south (-34.239°, 150.918°) ( Fig. 1 ). We are less certain of the southern boundary of the distribution of H. a. australiacus . Between Dharawal National Park and the northern most genotyped location for H. a. flavopunctatus (Parma Creek Nature Reserve), there is a gap of about 90 km within which there is only one genotyped sample, an F 2 hybrid. Although DFA classifications for ungenotyped vouchers (Hyams Beach and near Robertson) from within the gap provided high posterior assignments to H. a. australiacus (Supplementary Table S2), we cannot be certain of their identity in the absence of vouchers for hybrids to determine hybrid DFA posterior distributions. To ascertain the southern limit of the distribution of H. a. australiacus , and to further investigate the nature of the interaction with H. a. flavopunctatus, further genetic sampling will be required.

The distribution of H. a. australiacus is largely within the Sydney Basin bioregion. Extensive areas of the basin consist of uplifted sedimentary plateaus that are extensively eroded to form steep escarpments with small streams on the plateau, and larger streams in the valleys. Much of this rugged landscape is reserved for conservation or in water catchments. Large areas of its habitat in the central eastern portion of the basin, known as the Cumberland Plain, have been cleared for urban and agricultural development, although it appears from the distribution of historic collections that the frog was not found widely in this area which now is covered by the urban metropolis of Sydney.

Conservation status. Following the taxonomic subdivision of H. australiacus it is necessary to assess conservation status based on the revised distribution of this taxon. Based on the IUCN Red List criteria ( IUCN 2016, Mace & Lande 1991), we assess H. a. australiacu s to be Endangered, since the Area of Occupancy (AOO) is less than 2000 km 2, and there is evidence of population reduction from mapping of records over three generations ( Table 11. Fig. 15 ) [criteria, A2(c)B2(a)(b)]. Although H. a. australiacus is known over a relatively large range (EOO 8502 km 2) the number of location records and the reports of population sizes are low. The Atlas of Living Australia has 190 records in the decade 2010–2020 compared with 436 in the previous decade.

Figures

FIGURE 1. Map of south-eastern Australia showing the collection locations for Heleioporus. A) samples genetically examined (bold site numbers), locations for call recordings (italicised site numbers), and B) specimens examined morphologically (larger black squares) and records in the ALA, accessed November 2020 (smaller black squares). Red filled squares—H. a. australiacus, blue filled circles—H. a. flavopunctatus subsp. nov., grey filled triangle—hybrids. Site numbers in A) refer to localities detailed in Table 1.

FIGURE 4. Phylogenetic analyses of Heleioporus concatenated SNP data based on A) maximum likelihood and B) SVDQuartets analyses. Terminal taxa of eastern Heleioporus are numbered with locality codes in Table 1. Numbers at nodes in the ML tree are bootstrap proportions, all nodes in the SVDQuartets tree had 100% bootstrap proportions.

FIGURE 6. Colour pattern profiles for adult individuals of A) plate from Shaw & Nodder (1795); B–H) Heleioporus a. australiacus, and I–P) H. a. flavopunctatus subsp. nov.

FIGURE 7. Examples of the colour patterning around the cloaca in eastern Australian Heleioporus. A–H) Heleioporus a. australiacus; A) AMS R27631 Darkes Forest NSW, B) SAMA R45377, C) Ourimbah NSW, D) AMS R78853 Pittwater NSW, E) SAMA R12064 Gosford, F) ANWC A0357 Wadbilliga, G) AMS R95406 Darkes Forest, H) AMS R104952 (neotype) Maroota; and I–P) H. a. flavopunctatus subsp. nov., I) Yambulla NSW, J) Yambulla NSW, K) Narooma NSW, L) NMV D50515 (type) Yalmy Road, Vic., M) NMV D33671 6 km S Ben Cruachan, Vic., N) NMV D33672 6 km S Ben Cruachan, Vic., O) no voucher state forest near Eden, NSW, P) AMS R136722 Coolangubra State Forest, NSW.

FIGURE 8. Variation in the pre-orbital papillae in anterior corner of eye of eastern Australian Heleioporus. Heleioporus a. australiacus—A) AMS R104952 (neotype) Maroota State Forest, B) AMS R5958 North Sydney, C) AMS R9470 Wollemi National Park, D) AMS R78853 Commodore Heights. H. a. flavopunctatus subsp. nov.—E) AMS R136719 Coolangubra State Forest, F) ANWC A0357 Wadbilliga, G) AMS R136730 Coolangubra State Forest, H) ANWC A1504 Bondi State Forest.

FIGURE 12. Aggressive calls in eastern Australian Heleioporus. A) H. a. australiacus, Ourimbah State Forest, NSW. B) Enlargement of one call showing dense pulses, and C) enlargement of a call from H. a. flavopunctatus subsp. nov. from Morton National Park, NSW.

FIGURE 13. Images of eastern Australian Heleioporus types. A–E) Neotype of Heleioporus a. australiacus. AMS R104952 from Maroota State Forest, NSW. F–J) Heleioporus a. flavopunctatus subsp. nov. NMV D56515 from Yalmy Road, 1 km E.N.E. of Waratah Road junction, Gippsland, Victoria. Photograph in life P. Robertson.

FIGURE 15. Historic distribution of eastern Australian Heleioporus by decadal sampling periods from the ALA (accessed May 2020). Circles show where records have declined in the far south east of the distribution of H. a. flavopunctatus subsp. nov. and in the Greater Blue Mountains area in the north west of the distribution of H. a. australiacus.