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Morphological clarifications of Australian hylid and limnodynastid tadpoles

Article  in  Zootaxa · June 2016

DOI: 10.11646/zootaxa.4126.1.10

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 Zootaxa 4126 (1): 146–150 ISSN 1175-5326 (print edition)
http://www.mapress.com/j/zt/
Copyright © 2016 Magnolia Press
Correspondence ZOOTAXA
ISSN 1175-5334 (online edition)
http://doi.org/10.11646/zootaxa.4126.1.10
http://zoobank.org/urn:lsid:zoobank.org:pub:731F6B55-FB9A-47AB-90D7-A70E44304C06

Morphological clarifications of Australian hylid and limnodynastid tadpoles

MARION ANSTIS1,5, JODI J. L. ROWLEY2,3 & RONALD ALTIG4

1
School of Environmental and Life Sciences, University of Newcastle, University Drive, Callaghan NSW 2308, Australia.
E-mail: frogpole@tpg.com.au
2
Australian Museum Research Institute, Australian Museum, 1 William St, Sydney, NSW, 2010, Australia.
E-mail: jodi.rowley@austmus.gov.au
3
Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney NSW
2052, Australia.
4
Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39762 U.S.A.
E-mail: raltig@biology.msstate.edu
5
Corresponding author. E-mail: frogpole@tpg.com.au

Tadpole morphology usually is consistent within taxa and ecologies (Altig & Johnston 1989), but the occurrences of
unique morphologies offer informative perspectives on the potential diversity of these structures. Anstis (2013)
characterized most of the tadpoles of Australia, but a thorough understanding of certain morphological features requires
closer examinations. Until we understand the morphological features of anuran larvae, and preferably their ontogeny, we
cannot productively discuss their evolution or ecological significance.
Our targeted species include Litoria dahlii, L. dayi, L. subglandulosa and Limnodynastes lignarius. Adults of L.
dahlii are almost entirely aquatic in permanent ponds and lagoons, and the skin of the tadpoles has a uniform field of
small depressions. The majority of hylid tadpoles of the Australopapuan Region have keratinized jaw sheaths, a LTRF of
2/3, and a dorsal gap in the marginal papillae. A few stream dwellers with complete marginal papillae have modified oral
structures. The oral disc of L. dayi has an uncommonly large expanse beyond the third lower tooth row. Various features
of the jaw sheaths, labial teeth, and what are presumed to be modified submarginal papillae need verification. The
essentially identical mouthparts of the sister taxa L. subglandulosa and L. daviesae are profoundly different from all
other Australopapuan hylids. The mouthparts lack typical tooth ridges and keratinized structures, and the tadpoles feed
from deposits of flocculent silt in slow-flowing streams (Anstis & Littlejohn 1996; Tyler & Anstis 1975). We verified the
structure of small, weakly keratinized projections associated with a paddle-shaped structure in the medial part of the
upper labium of L. subglandulosa. The unusual marginal papillae on the lower labium of the tadpoles of Li. lignarius
were examined. All of these structures were examined with dissecting and scanning microscopy for verification of the
various structures.
One specimen of each species that had been identified in preparation for the publication of Anstis (2013) was
examined; this book includes line drawings of the tadpoles and their mouthparts. Each sample was stained with Crystal
Violet and observed and photographed with a dissecting microscope before being prepared for scanning microscopy (i.e.,
critical-point dried, attached to aluminum stubs with conductive tape, sputter-coated with gold, and viewed and
photographed with a Zeiss EVO LS 15): a piece of belly skin of the Litoria dahlii (stage 36 of Gosner, 1960, 64.3 mm
total length (TL), Fogg Dam, Northern Territory; not catalogued), the entire oral apparatuses of tadpoles of L. dayi (stage
26, 27.6 mm TL, Tully, Queensland, not catalogued) and L. subglandulosa (stage 32, 21.7 mm TL, Point Lookout, New
South Wales; AMS R119022), and the ornate marginal papillae on the lower labium of Limnodynastes lignarius (stage
34, 56.2 mm TL, Nuwarlandja Rock, Kakadu National Park, Northern Territory, not catalogued). In addition, a drawing
from Anstis (2013) made with the aid of a drawing tube attached to a stereoscopic microscope of one specimen of L.
lignarius (stage 36, Mitchell Plateau, Western Australia; AMS R182662), was included to assist understanding of this
oral disc as a whole.
The skin of the tadpole of Litoria dahlii has an evenly distributed field of circular pits (0.06–0.20 mm in diameter;
about 12–18/mm2). As observed with a dissecting microscope, the pits appear to have distinct edges and smooth bottoms
(Fig. 1A). As viewed with a scanning microscope (Fig. 1B), the bottoms of the pits are smooth, the edges of the pits are
less distinct, and secretory pores were not seen.
The oral apparatus of Litoria dayi (Fig. 1C) presents several notable morphological traits. Near the distal extent of

146 Accepted by M. Candioti: 13 May 2016; published: 16 Jun. 2016

the unusually large area of the lower labium beyond the third lower tooth row, there are three rows of large, pillow-
shaped pads (Fig. 1D) that we interpret as modified submarginal papillae. Views of an intact specimen with a dissecting
microscope showed a lightly keratinized area on the buccal (rear) face of the robust jaw sheaths. After staining, views of
that area showed a uniformly granulate surface, and the scanning images verified this structure (Fig. 1E). The lower jaw
sheath had a cancellous surface and the serrations were severely worn. The small, densely arranged labial teeth have
numerous, long cusps, and most of the teeth were either extremely worn or broken (Fig 1F).

FIGURE 1. Photographs and scanning micrographs: Litoria dahlii: (A) the small pits in intact, nonstained belly skin and (B), a
comparable scanning image (scale bar = 100 µm). Litoria dayi: scanning images of (C) the oral apparatus (scale bar = 1 mm; x =
approximate area shown in D), (D) the large, mound-like submarginal papillae (scale bar = 100 µm) on the distal area of the lower
labium, (E) the granulate, lightly keratinized area (scale bar = 20 µm) on the buccal face of the lower jaw sheath, and (F) the labial
teeth in LTR A-1 (scale bar = 10 µm).

The face of the oral disc (Fig. 2A) of the tadpole of Litoria subglandulosa has a dense field of conical papillae of
various sizes and arrangements. A transverse row of particularly large, conical papillae resides where one would expect
the first anterior row of labial teeth would be on a more typical tadpole. A slight yellowish tinge and the presence of
exfoliating epidermal cells indicate minor keratinization of the epidermis of the large papillae. A single, medial, paddle-
shaped projection lies in line with these large papillae and dorsal to the upper jaw. The paddle, usually present as a single

MORPHOLOGICAL CLARIFICATIONS OF AUSTRALIAN TADPOLES Zootaxa 4126 (1) © 2016 Magnolia Press · 147
projection, is sometimes divided into two smaller projections with a less precisely formed paddle at the end. The curved
distal edge of the paddle supports 5–9 filiform projections (Fig. 2A–D) that vary from translucent to darkly keratinized,
and no subdivisions could be seen with a dissecting microscope. When the paddle was stained, the mitotic anlagen for the
projections could be seen (Fig. 2B), and in some cases, more than one projection emerged at a given site on the rim of the
paddle. These projections are formed by a series of somewhat cylindrical or conical structures arranged in the same way
as typical labial teeth in a tooth series, but they extend beyond the tissue of the paddle. In an individual at stage 26, the
paddle had eight finger-shaped, nonkeratinized projections lying almost parallel to each other.

FIGURE 2. Photographs and scanning micrographs: Litoria subglandulosa: (A) the oral apparatus (scale bar = 200 µm), (B) the
medial paddle stained with Crystal Violet and viewed with a dissecting microscope that shows (arrow) the pale mitotic areas in the
base of the paddle that form the tooth-like elements, and (C) the medial paddle and tooth strands at lower (scale bar = 100 µm), and
(D) higher (scale bar = 20 µm) magnifications. Limnodynastes lignarius: (E) the ornate, midventral, marginal papillae (scale bar = 100
µm) and (F) labial teeth with prominent struts on the face of each cusped tooth (scale bar = 10 µm).

148 · Zootaxa 4126 (1) © 2016 Magnolia Press ANSTIS ET AL.

FIGURE 3. Oral disc of tadpole of Limnodynastes lignarius at stage 36 (Gosner 1960), from Mitchell Plateau, Western Australia.
Scale bar = 1 mm.

Tadpoles of Limnodynastes lignarius have a LTRF of 5–7(3–7)/3 and a dorsal gap in the uniserial marginal papillae
(Fig. 3). The unusually complex structure of the midventral marginal papillae (Fig. 2E) has rather widely spaced basal
projections that support 2–4 smaller papillae that branch from the tips. Some of the submarginal papillae directly behind
the marginal papillae are exceptionally large. The closely-spaced labial teeth have a prominent medial strut on the front
surface (Fig. 2F), and the cusps of the first replacement tooth can be seen through the wall of the sheath of the presently
erupted tooth.
A function of the pits on the skin of the tadpoles of Litoria dahlii could not be suggested, but they are not micropores
as suggested as a possibility by Anstis (2013). A study of their early ontogeny may be informative. The unusually large
expanse of lower labium beyond the third lower tooth row of the tadpole of L. dayi provides an increase in the contact
area with a substrate. This area surely increases the ability to maintain position in fast-flowing water, and the rows of
large, pillow-shaped submarginal papillae surely provide flexible contact surfaces that can conform to irregularities in
the substrate. Young teeth have a number of long cusps, but the large number of labial teeth in the middle of the tooth
head had a consistent pattern of breakages. The cancellous surface on the lower jaw sheath, the severely worn jaw
serrations, and the worn and broken labial teeth may be indicators of chytrid fungus infections.
Thibaudeau and Altig (1988) suggested that tooth ridges, marginal papillae and submarginal oral papillae are
homologs and that the face of the oral disc is totipotent for tooth formation. As a new tooth is formed at the base of a
tooth series (Altig 2007), the presently erupted tooth falls off. There are no developmental data for the rate of tooth
production or if and how labial teeth are attached to each other during development. We do not know why the teeth in
either of the following two cases are retained in strands beyond the tooth ridge. The keratinized projections from the
medial paddle of the tadpole of Litoria subglandulosa do not have the total structure of labial teeth, but they are formed
from a series of almost cylindrical or spike-shaped cones that interdigitate in the same way as teeth in a tooth series.
Tyler and Anstis (1975) suggested that these structures may serve a sensory or filtration purpose given the fine,
flocculent silt covering the substrate on which the tadpoles feed in streams, and this silt was found in the gut of tadpoles
preserved after capture (M. Anstis, pers. obs.). However, the small size and flexibility of the paddle and its projecting
strands makes potential scraping function against the substrate or effective filtration unlikely. An abnormal specimen of
the suctorial tadpole of Heleophryne (Heleophrynidae; R. Altig, pers. obs.) is another case of labial teeth remaining
attached in strands after they are pushed out of the tissue of the tooth ridge. Long, flexible strands of up to 40 teeth
projected from some tooth sites.

MORPHOLOGICAL CLARIFICATIONS OF AUSTRALIAN TADPOLES Zootaxa 4126 (1) © 2016 Magnolia Press · 149
 This oral morphology of L. subglandulosa reflects an obvious change in feeding mode from most of its congeners
and shows the wide latitude of oral morphologies. The mantellid tadpole of Boophis picturatus has a similar morphology
but with fewer and shorter papillae, and this tadpole swallows sand particles to harvest the attached organisms (Altig &
McDiarmid 2006).
Other than a rather few exceptional cases, marginal papillae are typically described only by arrangement (e.g.,
uniserial/biserial) and distribution (e.g., complete, with a dorsal gap or with dorsal and ventral gaps). The addition of
more accurate and specific notations of size and shape would often add considerably to the use of these features as
morphological descriptors. The unusual configurations of the ventral marginal papillae of Limnodynastes lignarius may
be an alternative morphology to increase the contact points of the marginal papillae and presents several questions about
the formation and function of marginal papillae.
Anstis acknowledges the assistance of Michael Crossland, Ian Morris, Keith McDonald, and Mike Tyler during her
fieldwork. Altig was supported by a Geddes Visiting Research Fellowship from the Australian Museum. Ross Sadlier’s
permission to destructively process the tadpole of Litoria subglandulosa in the herpetological collection and Sue
Lindsay’s patient operation of the scanning microscope at the Australian Museum in Sydney are gratefully appreciated.

References
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