Phascogale tapoatafa tapoatafa ( Meyer, 1793 )

Have, Ten, 2015, Taxonomic revision of Phascogale tapoatafa (Meyer, 1793) (Dasyuridae; Marsupialia), including descriptions of two new subspecies and confirmation of P. pirata Thomas, 1904 as a ‘ Top End’ endemic, Zootaxa 4055 (1), pp. 1-73 : 23-35

Phascogale tapoatafa tapoatafa ( Meyer, 1793)

Holotype: As explained by Mahoney & Ride (1988: 25), “the holotype is the specimen described and figured under the name Tapoa Tafa by Anon. [Hunter, J.] in White, J. (1790). Journal of a Voyage to New South Wales with sixty-five plates of non descript animals, birds, lizards, serpents, curious cones of trees and other natural productions. London: J. Debrett xvii 335 pp. (281–284 pl 58); preparation 3758 of Owen, R. (1841). Descriptive and Illustrated Catalogue of the Physiological Series of Comparative Anatomy Contained in the Museum of the Royal College of Surgeons in London. Products of generation. London: R. & J.E. Taylor Vol. 5 iv + xxxvii 284 pp. (209) is part of the holotype specimen)”. Although Troughton (e.g. 1967: 31) notes that “the specimen figured was preserved in the Museum of the Royal College of Surgeons”, neither Thomas (1888) nor Mahoney & Ride were able to locate an appropriate candidate, either in this collection or in the Natural History Museum, London. However, the original plate in White (1790) is unambiguously diagnostic (provided locality data are also taken into account) and neotype designation is unwarranted.

Geographic Region HV (mm) TV (mm) Wgt (g) Geographic Region HV (mm) TV (mm) Wgt (g) Southwest Western Australia Mean 179.95 199 190

s.d. 19.61 16.16

n 11 11 1 Max 210 230

Min 153 182

Victoria Mean 193.25 206.25 155.75 s.d. 20.30 12.34 41.44 n 4 4 4 Max 213 222 187 Min 165 195 96 New South Wales/Southern Queensland Mean 186 189.5 183

s.d. 15.56 23.33

n 2 2 1 Max 197 206

Min 175 173

'Top End', Northern Territory Mean 174.5 185.5 125.75 s.d. 11.90 5.20 17.67 n 4 4 4 Max 188 192 150 Min 160 180 108

Kimberley, Western Australia Mean 145 144

s.d.

n 1 1

Max

Min

Revised description. This account is primarily based on specimens from the central to north coastal region of New South Wales, including one topotypical specimen ( AM 932) collected in 1894 at Kingswood near Sydney. An adult male specimen from Coraki in northern New South Wales ( CM 20990) is illustrated in Fig. 4 . Regional variation is noted after the main account.

External measurements taken from museum specimen records are summarised in Table 4 . Adults in a Victorian population attained body weights of 311g for males and 212g for females ( Soderquist 1995c).

The dorsal fur is relatively dense and lush, the contour hairs measuring 12–13 mm in the centre of the back. The overall colour of the back and flanks is grey with a silvery frosting, this effect imparted by narrow white tipping on grey-based contour hairs. Abundant black-tipped guard hairs are distributed evenly over the body and project as much as 9 mm through the fur. The mid-dorsal zone is distinctly darker than the flanks owing to a more intense basal pigmentation.

Ventral fur colouration varies from grey with an extensive cream wash to predominantly cream (e.g., CM 3740). In most specimens, the central strip at least consists of pure cream fur, merging laterally into grey-based fur with a progressively shorter cream tipping. In all specimens, the pale ventral colouration extends anteriorly to the chin, posteriorly to surround the cloaca, and laterally to clothe the inner surface of the fore- and hind-limbs. The scrotum is heavily pigmented and densely clothed in cream fur. A pigmented gular gland is evident on some adult specimens of both sexes but the location of this gland is not marked by any obvious external discolouration of the fur. In some specimens the fur in this region has a slight russet tinge basally. The ventral fur in juveniles tends to be duskier, with a diffuse pale cream wash.

Table 5 a: Males

Geographic Region SL ZB OBW BS FMW C1-M4 M1-4

SouthwestW.A. Mean 46.34 27.49 18.61 5.67 6.80 17.60 10.28 s.d. 1.10 1.01 0.43 0.42 0.18 0.51 0.42 n 10 10 10 10 9 10 10 Range 44.57–47.79 26.17–28.81 17.97–19.09 4.94–6.32 6.40–7.02 16.89–18.69 9.70–11.23

SouthAustralia Mean 50.47 29.98 18.92 6.13 6.85 18.83 10.94 s.d. 0.86 0.66 0.58 0.87 0.31 0.67 0.54 n 3 3 3 3 3 3 3 Range 49.56–51.28 29.42–30.70 18.25–19.30 5.42–7.10 6.50–7.05 18.23–19.55 10.54–11.56

Victoria Mean 47.29 27.75 18.76 6.01 6.86 18.33 10.71 s.d. 2.09 2.12 0.46 0.63 0.53 0.55 0.25 n 8 7.00 7 7 7 8 8 Range 45.24–51.39 24.73–30.61 18.20–19.45 5.22–7.00 6.43–7.98 17.77–19.49 10.29–11.17

.S.W./ Mean 47.55 28.45 18.95 5.76 6.41 17.78 10.34

Queensland

s.d. 2.15 1.65 0.86 0.39 0.20 0.44 0.23 n 15 17 18 18 17 17 18 Range 42.60–51.73 24.02–30.00 17.31–19.95 4.95–6.35 6.04–6.74 16.78–18.59 9.91–10.70

NorthQueensland Mean 47.50 29.33 18.61 6.51 6.39 17.25 9.82 s.d.

n 1 1 1 1 1 1 1 Range

TopEnd',N.T. Mean 46.55 27.37 17.21 5.31 5.84 17.13 9.46 s.d. 0.98 1.84 0.25 0.38 0.04 0.31 0.31 n 3 4 4 4 3 4 5 Range 45.91–47.67 25.58–29.94 16.97–17.50 5.02–5.87 5.81–5.89 16.83–17.55 9.07–9.92

Kimberley,W.A. Mean 44.16 25.28 17.75 5.01 6.01 16.79 9.91 s.d. 0.85 1.35 1.09 0.33 0.24 0.15 0.26 n 2 2 2 2 2 2 3 Range 43.56–44.76 24.32–26.23 16.98–18.52 4.77–5.24 5.84–6.18 16.68–16.89 9.74–10.21

TOTAL 42 44 45 45 42 45 48

……continued on the next page TABLE 5 a. (Continued) TABLE 5 b. Females Range 42.99–46.84 24.98–28.17 18.23–18.78 4.92–5.83 6.57–6.92 16.86–17.79 9.99–10.72

SouthAustralia Mean 47.33 26.96 19.00 5.37 6.95 18.66 11.01 s.d. 1.14 1.22 0.76 0.22 0.08 N 1 2 2 2 1 2 2 Range 26.15–27.76 18.14–19.86 4.83–5.90 18.5–18.81 10.95–11.07

Victoria Mean 46.64 27.20 18.42 5.70 6.65 18.10 10.69 s.d. 1.16 1.19 0.74 0.48 0.39 0.34 0.35 N 6 6 6 6 6 6 7 Range 45.06–47.75 25.14–18.11 17.51–19.42 5.22–6.37 6.06–7.23 17.61–18.52 10.19–11.07

.S.W./Sth Mean 44.29 26.24 18.52 5.35 6.51 16.75 10.24

Queensland

s.d. 1.07 0.45 0.32 0.44 0.22 1.41 0.30 N 8 9 9 9 9 9 9 Range 42.05–45.5 25.63–27.10 18.0–18.97 4.90–6.32 6.10–6.80 16.39–18.20 9.79–10.70

TopEnd',N.T. Mean 41.29 23.80 16.14 4.80 5.98 16.08 9.28 s.d. 1.10 0.85 0.71 0.40 0.26 0.34 0.17 n 6 6 6 6 6 6 6 Range 40.09–42.66 22.43–24.67 15.05–16.98 4.28–5.24 5.68–6.46 15.49–16.38 9.04–9.50

Kimberley,W.A. Mean 41.51 16.66 5.42 6.70 16.58 10.19 s.d.

n 1 1 1 1 1 1 Range

TOTAL 31 32 33 33 31 33 35

…….continued on the next page TABLE 5 b. (Continued) Range 13.78–15.46 7.69–8.90 16.12–18.81 7.94–8.94 4.75–6.03 2.80–3.10 1.76–2.02

SouthAustralia Mean 15.39 8.39 17.85 8.32 5.25

s.d. 0.40 0.09 0.19 0.55

N 1 2 2 2 2

Range 8.11–8.67 17.70–17.91 8.18–8.45 4.86–5.64

Victoria Mean 15.16 8.81 18.00 8.61 5.41 2.72 1.84 s.d. 0.66 0.55 0.62 0.17 0.11 0.11 0.03 N 6 6 6 6 7 2 2 Range 14.30–15.81 7.79–9.30 16.82–18.63 8.44–8.80 4.93–5.84 2.62–2.80 1.82–1.86

S.W./Sth Mean 14.53 8.34 16.91 8.07 5.37 2.64 1.92

Queensland

s.d. 0.28 0.18 0.36 0.44 0.37 0.13 0.05 N 9 9 9 9 6 9 9 Range 13.95––14.91 8.03–8.54 16.31–17.50 7.42–9.00 4.81–5.78 2.50–2.86 1.82–2.00

TopEnd',N.T. Mean 12.64 7.38 14.57 6.82 5.18 2.23 1.54 s.d. 0.43 0.54 0.50 0.17 0.32 0.12 0.05 n 6 6 6 6 6 4 4 Range 11.82–12.97 6.71–8.08 16.31–17.50 6.61–7.05 4.68–5.60 2.12–2.40 1.50–1.58

Kimberley,W.A. Mean 13.10 7.60 7.08 6.06 2.40 1.60

s.d.

n 1 1 1 1 1 1 Range

TOTAL 32 33 32 33 32 21 21 Geographic region SL ZW OBW BS FMW C1-M4 M1-4

Southwest W.A. F2 8.42 5.24 NS NS NS NS NS

d.f. 1 1

P 0.010 0.035

South Australia / Victoria F2 NS NS NS NS NS NS NS

d.f.

P

.S.W./Southeast Queensland F2 15.99 15.23 NS 6.13 NS 7.93 NS

d.f. 1 1 1 1 P 0.001 0.001 0.020 0.010

Top End', Northern Territory F2 48.79 NS 8.08 NS NS 24.17 NS

d.f. 1 1 1 P 0.000 0.022 0.001

Continued.

Geographic region PALW ARW PRW IOW RD LCL LCW

Southwest W.A. F2 NS NS 6.36 NS 7.78 NS NS

d.f. 1 1

P 0.022 0.012

South Australia / Victoria F2 NS NS NS NS NS 12.01 10.73 d.f. 1 1.00 P 0.041 0.047

.S.W./Southeast Queensland F2 17.25 7.34 12.09 NS NS 68.43 33.19 d.f. 1 1 1 1 1 P 0.000 0.013 0.002 0.000 0.000

Top End', Northern Territory F2 NS 15.74 10.69 NS NS 25.49 31.11 d.f. 1 1 1 1 P 0.004 0.011 0.004 0.003 The fur on the head is pale grey on the sides of the face and dark grey with diffuse frosting on the crown. Additional facial patterning includes a well-developed, dark russet mid-rostral stripe, a broad and indistinct, dark grey loreal stripe and small, black postorbital spot, distinct off-white infra- and supra-orbital crescents, and a variably expressed cream-tipped preauricular tuft. Preauricular patches are indistinct in around 30 % of specimens and seem to be less conspicuous in juveniles than in adults. In most specimens, the cream fur of the chin and throat extends around the corner of the mouth and merges into a supralabial bar, while the cheek patch is cream peppered with black. The rostral vibrissal pads are densely clothed in short grey fur and the basal papillae are unpigmented and not visible. All facial vibrissae are thick and black, sometimes with gingery tipping. The pinnae are moderately elongate and broad, weakly to moderately pigmented and sparsely furred. The anterior border of each pinna supports a narrow band of short black hairs.

The basal portion of the tail is thickly furred above and on the sides, and supports numerous projecting guard hairs, continuing the colour and texture of the rump ( Figs 4 and 6 ). The tail narrows rapidly to form a distinct ‘stem’, which is clothed above and below by long, adpressed hairs. Dorsally and around the sides of the tail, these hairs are white with short black tips, while those on the ventral surface are black with short cream tips grading to dark russet at the base of the brush. The tail ‘brush’ is lush and measures up to 165 mm; it consists of jet black hairs except for a short section of dark russet hairs ventrally, at the base of the brush. The basal portion of the tail, from cloaca to base of brush, measures to 90 mm.

The upper surface of the pes supports a mixture of white, dark grey and russet hairs, giving it an overall grizzled appearance. This merges into white fur on the sides of the foot and around the heel. The digits are densely clothed in white hairs. The plantar surface of the pes is granular and supports a total of five conspicuously striated pads. The inner metatarsal and first interdigital pads are fused, usually with no obvious line of demarcation; their combined length is 13.1 mm. The outer metatarsal pad is moderately long; on AM932 it measures 7.4 mm and is separated by a gap of 3.9 mm from the fourth interdigital pad. The second to fourth interdigital pads are elongate and of subequal length. Both feet on one specimen ( CM 1316) show a clear line of demarcation between the conjoined inner metatarsal and first interdigital pads.

Females in all populations usually have eight teats in the pouch (e.g. Cuttle 1982; Soderquist 1993a); occasional individuals have seven teats.

Cranial and mandibular anatomy of a fully adult male ( CM 24425) and subadult male ( CM 1316) are illustrated in Figure 16 . Cranio-mandibular and dental measurements for each sex are provided in Table 5.

The New South Wales to southeast Queensland populations of P. t. tapoatafa show clear male-biased sexual dimorphism in cranio-dental measurements ( Table 6 & Fig. 9 ). For all dimensions bar one ( FMW), mean values are higher in males than females and for nine dimensions the contrast is statistically significant. This latter subset includes measures of overall cranial size ( SL, ZW, PALW, PRW) and of the lower canine ( C 1 L; C 1 W), as well as measures that are sensitive to canine enlargement ( C 1- M 4 L, ARW). The combined South Australian and Victorian sample shows a less pronounced male-biased dimorphism in which statistical significance is attained only for measures of the lower canine. In this population, the contrast in PRW also approaches significance. These observations on the Victorian population are consistent with Soderquist’s (1995c) finding that the marked sexual dimorphism in body weight among Victorian P. tapoatafa is due primarily to somatic energy stores that are laid down in preparation for the short breeding season when foraging effort is curtailed. In the Victorian population studied by Soderquist the ratio of average adult male to female body weights is 1.62 (Soderquist unpublished data, reported by Rhind & Bradley 2002).

Geographic variation. Possible clinal variation within P. t. tapoatafa is observed in various cranial and dental dimensions but with somewhat different expression in each sex. Among males there is a very slight and gradual decrease in cranial length ( Fig. 17 a) from South Australia to Queensland, coupled with a more pronounced shortening of the upper molar row that also shows a more abrupt break between southern and northeastern populations ( Fig. 17 b). Females show a more pronounced decrease in both cranial and dental dimensions ( Figs 17 d–e). Both sexes show an abrupt and significant contrast between southern and northeastern populations in the breadth of the foramen magnum ( Fig 17 c,f); this variable is little affected by overall growth of the cranium.

The different pattern of geographic variation between the sexes of P. t. tapoatafa is largely a product of the variable expression of sexual dimorphism between the southern and southeastern Australian populations. Essentially, males of P. t. tapoatafa vary only slightly in cranial size throughout their range, while the more pronounced clinal variation in female cranial size, from large in the south to smaller in the north, creates a widening contrast between the two sexes. Overlaid on this pattern is a more pronounced geographic variation in molar size, with southern animals of both sexes having larger teeth on average than those from New South Wales and Queensland. On present evidence, this variation appears to be manifested in different ways between the sexes—step-like in males vs clinal in females—but larger samples from critical areas are needed to be certain of this.

Distribution and conservation status. The historical distribution of P. t tapoatafa corresponded to the more or less continuous tract of forested country that extended from the southeastern corner of South Australia, extending across most of Victoria (probably excluding only the northwestern mallee region and country above the treeline) and then running north along the coastal strip and mountainous hinterland of New South Wales and Queensland, north at least to Mackay ( Fig. 18 ). A recently collected sub-fossil specimen from Ukerbarley station, 7 km NW of Coonabarabran ( Fig. 18 & Table 9 ), indicates that populations of this taxon once occurred on the western slopes of the Great Dividing Range in New South Wales. Whether any of these survived into historical times is not known.

At the western end of its range, a population of P. t. tapoatafa was recorded historically in the Mt Lofty Ranges of South Australia ( Fig. 18 ). Although Wood Jones (1923) understood the range of this species (as P. penicillata ) to extend to the Murray River, sub-fossil collections from several archaeological sites in this area have failed to confirm its former presence ( Wakefield 1964). Morphologically, the few available specimens from the Mt Lofty population appear to be indistinguishable from Victorian specimens. However, in the absence of genetic data, it is not possible to decide whether the Mt Lofty population was genuinely isolated or not. Caution in this regard is further indicated by a subfossil record of P. tapoatafa from a cave deposit of mid-Holocene age on Kangaroo Island ( Fig. 18 & Table 9 ), indicating a wider distributional and habitat range than might be inferred from the few historical records alone.

As reported in a later section, populations of Phascogale tapoatafa are also present in northern Queensland. These resemble the nominate race in most morphological features but show a moderate level of genetic differentiation (albeit based on a single individual from the northern population). Today these populations appear to be separated from those in the south by a gap of more than 400 km of significantly drier habitat. However, a subfossil record of P. tapoatafa from Christmas Creek, inland of Townsville ( Table 9 ) signals the possibility of recent continuity between these populations. The northern Queensland population is herein left unallocated at subspecific level.

Although Victoria, New South Wales and Queensland still host populations of P. t. tapoatafa , its geographic range is now extremely fragmented and many regional populations are in decline. Indeed, the only region in which the taxon might be said to be secure is southeastern Queensland. Phascogale tapoatafa is probably extinct in South Australia, with the last vouchered record dating to 1969. Wood Jones (1923: 101–102) remarked on the former abundance of the species in South Australia and noted that it was known to “the South Australian Murray River natives’ as “ pundi ”. He also speculated on the possible existence of populations of this taxon “over a wide area in the Centre”. It is possible that these reports referred instead to P. calura , which Wood Jones tentatively included in the South Australian fauna on the basis of an early record from ‘Adelaide’ but otherwise knew little about. In fact, Spencer and Gillen had obtained several specimens of P. c a l u r a from Central Australia prior to 1901 ( Baynes & Johnson 1996), although no further specimens were obtained from this area.

Phascogale t. tapoatafa has been the focus of several field studies in Victoria ( Cuttle 1978, 1982; Soderquist 1993a, 1993b, 1994a, 1994b, 1995a; Soderquist & Ealey 1994; Soderquist & Lill 1995) but little is known of the species’ ecology in New South Wales or Queensland. The difference between these populations in the degree of sexual dimorphism suggests caution in assuming a uniformity of all aspects of ecology among populations of this widespread subspecies. Dixon & Huxley (1989) reported extracts concerning Victorian P. tapoatafa from the natural history notes of Donald F. Thomson, drawn primarily from sources on the Bellarine Peninsula where the species was so common in the 1940s–1960s that it invaded local residences and was regarded as a nuisance. There are no modern records of the species in this area.

Figures

FIGURE 4. Representative ‘ puppet’ skins of nominotypical Phascogale tapoatafa (CM 20990, an adult male from Coraki, New South Wales, in a) dorsal view and b) ventral view and P. t. pirata (CM 7225, an adult male from Nourlangie Rock, Arnhem Land, Northern Territory, in c) dorsal view and d) ventral view), illustrating the extremes of variation in body proportions and colouration among the Brush-tailed Phascogales.

FIGURE 6. Ventral surface of the tail in representatives of four populations of the Phascogale tapoatafa group; a) nominotypical P. tapoatafa (CM 20990); b) P. t. pirata (CM 7225); c) P. taoatafa southwestern W. A. (WAM 5006, from Balingup Brook); d) P. tapoatafa Kimblerley, W. A. (WAM 16028, from Pago Mission).

FIGURE 9. Bivariate scatter plots of cranio-dental dimensions, illustrating varying degrees of inter-populational variability separately for male and female samples. Variables: a) SL vs ZW; b) SL vs C 1 - M 4; c) SL vs OBW; d) SL vs M 1 - 4; e) SL vs FMW; f) SL vs IOW; g) SL vs PRW. Population codes: 1: southwest Western Australia; 2: South Australia; 3: Victoria; 4: New South Wales and southeast Queensland; 5: northeast Queensland; 6: ‘ Top End’ of the Northern Territory; 7: Kimberley region of Western Australia. Left hand series are females; right hand series are males.

FIGURE 16. Crania and dentaries of P. tapoatafa tapoatafa. a) CM 24425, an adult male from Coraki, New South Wales, and b) CM 1316, a subadult male from Wallaby Creek, near Urbanville, New South Wales. Each series consists of (left to right) dorsal view of cranium, ventral view of cranium, and lateral view of right dentary.

FIGURE 17. Graphical representation of geographic variation within P. t. tapoatafa in selected craniodental dimensions (SL; M 1 - 4; FMW). Values for individual specimens are plotted in geographic sequence (Geo Seq) from west to east for South Australia and Victoria, and then from south to north for New South Wales and southeast Queensland. Population codes: 2: South Australia; 3: Victoria; 4: New South Wales and southeast Queensland. Plotted variables are a) Skull Length; b) M 1 - 4; c) Foramen Magnum Width. Left hand series are females; right hand series are males.

FIGURE 18. Map of eastern Australia, showing the contemporary (dark grey) and historic (light grey) distribution of P. tapoatafa tapoatafa, based on museum specimens and reliable sightings. Star symbols are sub-fossil records judged to be of late Holocene age. Square symbols represent the location of two sight records that might pertain to either P. pi r at a or P. tapoatafa.

Tables

TABLE 4 a. Summary external measures of male Phascogale tapoatafa group specimens used in this study (HV headvent, TV tail-vent, Wgt weight). Obvious subadults excluded.

Southwest Western Australia Mean s.d. n	200.5 17.95 10	208.5 10.63 10	170 1
Max Min South Australia Mean	228 175 230	226 193 225
s.d. n	1	1
Max
Min Victoria Mean s.d.	202.2 13.99	203.2 16.18	185.33 15.95
n Max Min	5 220 182	5 230 188	3 196 167
New South Wales/Southern Mean Queensland s.d. n	196.4 26.17 5	202.4 24.13 5	212.5 84.15 2
Max Min Northern Queensland Mean	230 170 201.5	238 178 202.5	272 153 185
s.d. n Max	12.02 2 210	3.54 2 205	1
Min 'Top End', Northern Territory Mean s.d.	193 209.5 0.71	200 204 5.66	234
n Max Min	2 210 209	2 208 200	2 234 234
Kimberley, Western Australia Mean s.d. n	163 6.56 3	159 20.07 3
Max Min	170 157	180 140