In celebration of Dr. John J. Engel: A tribute to 40 years in bryology
Botany
NEW SERIES, NO. 47
Part Eight: Hornworts
Chapter Twenty: Taxonomic Studies of the Australian Anthocerotophyta II: The Genus
Phaeoceros
D. Christine Cargill1 and Bruce A. Fuhrer2
1
Centre for Plant Biodiversity Research, Australian National Herbarium, GPO Box 1600, Canberra,
ACT 2601, Australia
2
25 Sunhill Avenue, Ringwood, Victoria, Australia
Accepted May 20, 2008
Published November 24, 2008
Publication 1550
Abstract
Four species within the hornwort genus Phaeoceros are recognized and described for
Australia: the cosmopolitan P. carolinianus (Michx.) Prosk.; two new combinations of taxa
endemic to Australia—P. evanidus (Steph.) Cargill & Fuhrer comb. nov., P. inflatus (Steph.)
Cargill & Fuhrer comb. nov.; and a species new to science, P. engelii Cargill & Fuhrer sp. nov.
A key to all four species is also given.
Introduction
The hornworts have become a pivotal group in
understanding the transition from nonvascular
land plants to vascular land plants (Qiu et al.
2006). A seemingly homogeneous group, recent
molecular and ultrastructural studies have
revealed a surprisingly diverse group of plants.
Traditional relationships have been discarded,
such as that between Anthoceros L. emend. Prosk.
and Phaeoceros Prosk., others have been confirmed, such as between Megaceros Campb. and
Dendroceros Nees., and new and novel ones have
been revealed, such as the position of the unique
FIELDIANA: BOTANY, N.S., NO. 47, NOVEMBER 24, 2008, PP. 239–253
239
Leiosporoceros Hässel (Duff et al., 2004, 2007;
Cargill et al., 2005). These studies have concentrated on relationships at the level of genera and
higher yet species boundaries within the group
still remain confused. This paper is the second in
a series revising the hornwort species of Australia
and is a foundation paper for the genus Phaeoceros
in this region.
Crand.-Stotl. (category 2) (family Phymatocerotaceae Duff et al.); Paraphymatoceros Hässel
(category 3); and Phaeomegaceros Duff et al.
(category 4) (subfamily Phaeomegacerotoideae
Duff et al.). Hässel’s study highlighted the broad
diversity of spore patterning within this group,
and recent molecular results have confirmed
the importance of spore characters as well as
highlighting the importance of others such as
chloroplast, pyrenoid, or tuber morphology.
Historical Review
After a comprehensive study of the hornworts,
Proskauer (1951) circumscribed the genus
Phaeoceros from the broadly defined Anthoceros
on the basis mainly of the absence of internal
schizogenous cavities in the thallus typically
found in Anthoceros. However, characters considered of secondary importance included irregularly
arranged antheridial jacket cells and yellow
spores. Acceptance of the new genus was not
universal and controversy surrounded its nomenclature until recently. The name Anthoceros has
now been conserved for those elements that
possess dark-colored spores and a cavernous
thallus (Stotler & Crandall-Stotler, 2003).
After Proskauer’s revisions for the genus
Phaeoceros, a number of studies ensued. These
included the studies of Hässel de Menéndez (1989)
who recognized 23 species for North and South
America. On the basis primarily of the patterns of
the distal and proximal faces of the spores
observed through scanning electron microscopy
(SEM), she emphasized the importance of spore
differences in the separation of species. She
grouped the American species into four distinct
categories on the basis of the patterns of the spore
distal face: 1) spores with spines or baculae, for
example, P. carolinianus (Michx.) Prosk. (Fig. 3.);
2) spores with large projecting verrucae, for example the spores of P. tenuis (Spruce) Hässel or P.
pearsonii (M.A. Howe) Prosk. (Hässel de
Menéndez, 1989); 3) spores with fine, low ornamentation, for example the spores of Phymatoceros
bulbiculosus (Brot.) Stotler et al. (Crandall-Stotler
et al., 2006); and 4) spores with depressions, for
example the spores of Phaeomegaceros fimbriatus
(Gottsche) Duff et al., (Hässel de Menéndez,
1989 as Phaeoceros fimbriatus Gottsche). These
groupings were not given any taxonomic status
by Hässel, but recent molecular studies have
partially supported these categories, giving rise
to three new genera, a new family, and a new
subfamily: Phymatoceros Stotler, W.T. Doyle &
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History of Australian Taxa
The earliest record of an Australian hornwort
was made by Lehmann and Lindenberg in 1832
describing Anthoceros adscendens and A. glandulosus (Lehmann 1832). Over the next 80 years,
only 11 more taxa were added to the Australian
records until the comprehensive publications of
Stephani in 1917. He attributed 19 anthocerotes
to Australia, of which eight were new to science
and two species were new records for Australia.
Of the 29 taxa recorded for Australia (many of
which are yellow spored), only two species have
been recognized for the genus Phaeoceros: P.
laevis and P. carolinianus (McCarthy 2006). Scott
and Bradshaw’s important foundational checklist
of Australian liverworts (Scott & Bradshaw 1985)
did not accept the generic rank of Phaeoceros.
Instead they preferred to follow Jones’ (1958) and
Schuster’s (1963) placement as a subgenus of
Anthoceros. Molecular studies have subsequently
supported Proskauer’s original split of Anthoceros
into two distinct genera (Duff et al., 2004, 2007;
Frey & Stech, 2005), and the genus Phaeoceros is
universally accepted.
A number of regional revisions of Phaeoceros
have been published over the last two decades,
including Japan, South East Asia, and islands of
the Pacific (Hasegawa, 1984a, b, 1986a, b, 1991,
1993, 2002), New Zealand (Campbell, 1981a, b,
1982, 1993), North and South America (Hässel de
Menéndez. 1989; Schuster 1992), and India
(Asthana & Srivastava, 1990). However, since the
prodigious publication of Stephani (1900–1924),
no comprehensive revision of the hornworts for
Australia has been undertaken. The aim of this
paper is to determine the status of the yellowspored taxa previously published for Australia.
Also included is the description of a new species,
P. engelii named in celebration of John Engel’s 40
years of publications in the field of bryological
studies.
FIELDIANA: BOTANY
Materials and Methods
The type specimens of all yellow-spored taxa
originally described for Australia were examined,
including collections of Phaeoceros from all major
Australian herbaria. Field collections were also
made over a wide geographical range within
Australia. Where mature sporophytes were
present, spores were sampled for viewing with
SEM. Air-dried spores were removed from
capsules and mounted on double-sided sticky
tape attached to aluminum stubs. Stubs were gold
coated and viewed with either a Hitachi S-570 or
a Jeol JSM 6400 SEM. Spores and pseudoelaters
were also mounted in water for measurement and
color information with subsequent permanent
mounting in either Hoyer’s or Johnson Brite®.
Both rehydrated herbarium specimens and live
field collections were examined, sectioned,
measured and drawn for gametophytic and
sporophytic characters with the use of both compound and dissecting microscopes with attached
drawing tubes. Habit and light microscope images
of Phaeoceros were taken with a Nikon Coolpix
5000 digital camera.
Colors of gametophytes were determined by
the use of the Royal Horticultural Society Colour
Chart (1995).
Results
Type specimens of all species were available
and examined. Of the seven yellow-spored taxa
originally described for Australia, six fell into one
of either three distinct groupings corresponding
to the three species: Phaeoceros carolinianus, P.
evanidus, and P. inflatus. Unfortunately, of the
remaining taxon, neither the lectotype nor the
isolectotype of Phaeoceros tuberosus (Taylor)
Prosk. that we have seen to date had mature sporophytes, though morphologically the gametophyte clearly falls at the very least within the
order Notothyladales Hyvönen & Piippo. Speculation as to which genus it might fall under and
the need to examine fertile type material has
required us to leave P. tuberosus out of this paper
at present. Tubers described for all four taxa
in this paper are typical of those found in P.
pearsonii (M. Howe) Prosk., which are ventral,
subterminal, and without stalks.
Descriptions are given of all three species, as
well as of a new species, P. engelii. A list of distinguishing features is given in Table 1.
Phaeoceros Prosk., Bull. Torrey Bot. Club 78(4):
346 (1951)
ETYMOLOGY—From the Greek phaeo- (dark)
and ceros (a horn), in reference to the dark
coloring and shape of the mature sporophyte.
TYPE—Phaeoceros laevis (L.) Prosk.
A widely occurring genus in both the Northern
and Southern hemispheres Phaeoceros consists of
ca. 40 taxa, of which Phaeoceros carolinianus
(Michx.) Prosk. and P. laevis are the most widespread species worldwide (Hässel de Menéndez,
1987; Schuster 1992). Distinguishing characters
for the genus in Australia include smooth solid
thallus, yellow spores, irregularly arranged jacket
cells of the antheridia, and possession of tubers in
some species.
Phaeoceros carolinianus (Michx.) Prosk. Bull.
Torrey Bot. Club. 78: 347. 1951
Basionym—Anthoceros carolinianus Michx.
Flora Boreali-Americana 2: 280. 1803. Type: USA.
Carolina inferiori, herb. Camus, herb. Richard
(holotype in PC).
Synonyms—Anthoceros australiae Beauv. ex
Steph. Spec. Hepat. 6: 571 (1924) syn. nov. Type:
Australia, New South Wales, F. v. Mueller (as A.
crispus) (lectotype G!).
Anthoceros brotheri Steph. Hedwigia 32: 141
(1893) syn. nov. Type: Australia, Queensland,
Brotherus 859 (lectotype in G!).
Anthoceros communis Steph. Bull. Herb. Boissier
5: 86 (1897). Type: Japan, Akita, Faurie 1484
(lectotype in G!) NSW 261411.
Anthoceros multicapsulus Steph., Spec. Hepat. 5:
991 (1916) syn. nov. Type: Lord Howe Island.
(lectotype in G!).
Thallus transparent, yellow-green to dark green
(RHS Colour chart 135D; 137B,C, and D; 144B)
growing on soil or rock. Plants small to medium
in size, up to 20 mm in length and 15 mm in width,
forming fans, rosettes, patches or mats, adhering
to bare soil or rock. Furcate to irregularly
branched, frequently with ventral unstalked
tubers becoming broad and flat, full of starch
granules. Thallus solid, 8–12 cells thick in transverse section, varying from biconvex to planoconcave to concave-convex. Dorsal epidermal
cells quadrate to hexagonal, 17–83 × 17–48 µm.
Internal cells 26–82 × 26–70 µm. Ventral clefts
observable sometimes and flanked by two cells.
Nostoc colonies scattered through ventral half of
thallus, appearing as dark dots. Rhizoids ventral,
hyaline, or pale brown.
CARGILL AND FUHRER: PHAEOCEROS TAXONOMIC STUDIES
241
Monoicous, androecium with 2–5 antheridia
per cavity, jacket cells irregularly arranged, 256 ×
133 µm, stalk up to 38.4 µm long. Involucre erect,
conical-cylindrical, up to 6 mm long, contracted
at the mouth, 5–7 cells thick in transverse section.
Sporophyte capsule up to 80 mm long, exserted,
opening by two valves becoming twisted with
drying, with well-developed columella, becoming
yellow and then dark brown with age from
the apex down. Assimilative layer 4–5 cells thick
and sporogenous layer of two rows of spores.
Epidermal cells of capsule elongated rectangular,
99–227 × 16–22.5 µm, walls becoming thickened
with maturity, stomata present in the capsule
wall. Spores bright yellow, rounded-tetrahedral
equatorial diameter 36–43 µm. Distal face covered with numerous spines, proximal face finely
rugose with button-shaped verrucae confined to
the center of each triradiate face. Proximal face
with a distinct triradiate mark, covered in a
sculpturing of small bacillar and button-like
papillae along its length. Pseudoelaters thin
walled, up to 5 cells in length, frequently branched,
43–199 µm long and 9.5–22 µm wide, pale
brown.
ETYMOLOGY—The species epithet “carolinianus” refers to the location of the type collection,
which was originally collected in North (or
?South) Carolina, USA.
DISTRIBUTION AND ECOLOGY—A ubiquitous
species across Australia, it is typically found
growing on bare soil, on and beside bush tracks,
roadside banks and banks of waterways (Fig.
1a).
AFFINITIES AND DIFFERENTIATION—Phaeoceros
carolinianus (Fig. 2) is closely related to P. laevis,
with many Australian collections identified as P.
laevis; however, sexual condition and spore
proximal patterns distinguish these two species.
Phaeoceros carolinianus is monoicous and
FIG. 1. Gametophyte and sporophytes of the four Australian species of Phaeoceros. (a) Phaeoceros carolinianus
(Cargill & Fuhrer 841. Queensland); (b) Phaeoceros evanidus (Cargill & Fuhrer 875. Queensland. Millstream Falls
NP); (c) Phaeoceros inflatus (Cargill & Fuhrer 475. Victoria. Warrandyte SP); (d) Phaeoceros engelii (Cargill & Fuhrer
1017. Victoria. Lower Glenelg NP, Moleside Crk.) Scale = 10 mm.
242
FIELDIANA: BOTANY
FIG. 2. Phaeoceros carolinianus. (a) Gametophytes
with sporophytes. Scale = 4 mm. (b) Antheridia
illustrating the irregular arrangement of jacket cells
typical of the genus. Scale = 100 µm. (c) Dorsal epidermal cells of thallus. Scale = 100 µm. (d) Transverse
section (TS) of thallus. Scale = 100 µm. (e) Cells of
thallus through TS section. Scale = 100 µm. (f) TS
through basal section of sporophyte and involucre.
Scale = 100 µm. (g) Internal cells of sporophyte; inv =
involucre; sp = sporophyte. Scale = 100 µm.
proximal verrucae numbers are low and confined
to the central section of each triradiate face
(Fig. 3). The type spores of P. laevis have verrucae
covering each of the triradiate faces and it is
dioicous (Proskauer, 1951; Hässel de Menéndez,
1987). Phaeoceros laevis has not been confirmed
to occur in Australia, and is probably confined to
the northern hemisphere.
SPECIMENS EXAMINED—Australian Capital Territory:
Head of Murray’s Gap, Bimberi Ra., Cotter River
District, mud banks in swampy herb field, Schodde (AD
26972); Gladfield, Darling Downs, Gwyther 331871
(BRI); Bendoura Dam Rd., Brindabella Ra., 28 km SW
of Canberra, Streimann (CBG 7804945); Little Collins
Crk., Brindabella Ra., head of small shaded gully.
Streimann 5281 (CBG 7804939); Botanic Gardens,
Canberra, common on moist, shaded stream banks,
Streimann (CBG 066486); Murray’s Beach, Jervis Bay,
wet shaded cliff face above beach, Streimann 5032
(CBG 7892211); Bull’s Head, Brindabella Ra., on moist
earth, on rock outcrop in Eucalyptus forest, Scott s.n.
(2) (MUCV129). Lord Howe Island: Lord Howe Is.
(MEL 1039116, 1039117, 1039126 & 1039127); 1 km E
of King’s Beach at foot of Mt. Lidgbird, on bank of
creek, Corrick 11049 (MEL 11049). New South Wales:
Minyon Falls, 25 km NNE of Lismore, moist exposed
rocks below falls, Streimann 6844 (CBG 7905590);
Wilson’s Crk., 8 km W of Mullumbimby, on rocks
beside stream, Bender 14 (CBG 7708512); Flat Rock
Crk., North Shore, Sydney, wet banks, Whitelegge
s.n. (MEL 1039092); Mossmans Bay, near Sydney,
waterfalls, Watts 199 (as Anthoceros communis NSW
261411); Centennial Park, Sydney, Cheel 803 (as
Anthoceros brotheri NSW 261409); between Mt. Kiera &
Wollongong, moist soil, on the roadside, Coveny s.n.
(NSW 261536); Gosford Rd. near Woy Woy, rocks
by waterfall, Bessie 1/59 (SYD); Huntley Point, Barnard
s.n. (SYD BARN 4.11.25); Somersby Falls, Na-Thalang
s.n. (SYD O.N.T. 2.7.66(1)); Nadgee Fauna Reserve,
between W Newtons Beach and Little River, on soil
on bank of gully, Hewson s.n. (SYD HJH 18.4.65 (1)).
Norfolk Island: Broken Bridge Crk., on continuously
wet overhanging rock, Hoogland 6632 (CANB 77819).
Queensland: Mooloolah River, 2 km SW of Mooloolah,
Moreton District, on peaty detritus among rocks in
bed of running stream, Windolf 124 (BRI 331874);
Warrumbah Crk., Carnavon Nat. Park, narrow shaded
gorge with scattered shrubs and trees, on semi-exposed
rocks in creek, among Lunularia, Steimann 52188 (CBG
9312854); Murphey’s Crk., 16 km NE of Toowoomba,
side of creek on rocks, dry sclerophyll forest, Streimann
370 (CBG 051234); Kin Kin Crk., 19 km NNW of
Tewantin, creek bank, sandy loam, Telford 4341 (CBG
7902323); Johnstone River track near Sutties Crk.,
Tully, on roadside bank, tropical rainforest, Scott s.n.
(MELU 6743); Blencoe Crk., Kiirama State Forest,
Cardwell, riverbank, cleared tropical rainforest, Scott
s.n. (MUCV 6924) Millstream Falls, Ravenshoe, on bare
soil at side of track, Cargill & Fuhrer (MUCV 7991);
Wright’s Crk. Rd., Lake Eacham Nat. Park, on
roadside bank, Cargill 55103 & 55104 (MUCV 7980 &
MUCV 7981); Greene’s Falls, S of Mt. Glorious, in rainforest, on wet rocks at top of waterfall, Smith & Tindale
H62 (NSW 261553); Millstream Falls, Ravenshoe, Watts
s.n. (NSW 261550). South Australia: Back Valley, off
Inman Valley, Southern Lofty Region, Cleland 51 (AD
5889); Back Valley Southern Lofty Region, Cleland s.n.
(AD 6000); Ashbourne Area, Southern Lofty Region,
CARGILL AND FUHRER: PHAEOCEROS TAXONOMIC STUDIES
243
FIG. 3. SEM micrographs of spores of Phaeoceros carolinianus. (a, c) Distal face; (b) proximal face; (d, f) detail
of proximal micro-ornamentation; (e) close-up of micro-ornamentation of distal face. Scales: (a–c) 10 µm; (d–f)
1 µm. [a–f from Cargill & Fuhrer 490, Australia. Victoria. S E Gippsland, Costicks Weir, Mundic Crk.]
growing on spongy ground near Juncus sp. and Callitrix
stagnalis, soakage start of creek, Murfet 668 (AD 27625);
Square Waterhole near Mt. Compass, in a swamp,
Symon s.n. (AD 6923). Tasmania: Norfolk Island,
244
Robinson (MEL 1039122). Victoria: Black Spur, Bastow
s.n. (MEL 1039095); Buffalo Ra. F. von Mueller s.n. (MEL
1028292); Spring Gully at Maliuns, 52 km N of Orbost
on the Bogong Hwy. Thiele 709 (MELU 2452). Western
FIELDIANA: BOTANY
Australia: Worriga Gorge, Drysdale River Nat. Park,
on wet sandstone rocks in shaded part below waterfall,
George 14100 (MEL 1023878); Sandy Crk., King Leopold
Ranges, Kimberleys, in peaty creek bed, Scott
s.n. (MELU 789); Galvans Gorge, West Kimberleys,
damp earth among ferns, under fall of water, Willis
s.n. (MELU 547).
Phaeoceros evanidus (Steph.) Cargill & Fuhrer
comb. nov.
Basionym—Anthoceros evanidus Steph., Spec.
Hepat. 5: 990 (1916). Type: Australia, Port
Denison, W.W. Birch (lectotype in G!).
Thallus pale transparent yellow-green to green
(RHS Colour Chart 143C, 145B), delicate,
growing in rosettes on bare moist soil patches.
Plants small up to 15 mm long and 2.4–15 mm
wide, from single lingulate thallus to ± fan-shaped
branched thallus with overlapping lobes originating from a persistent, narrow strap posteriorly,
furcately branched. Margins irregularly crenulate
to ± entire, sometimes lateral margins curving
upward becoming canaliculate. Thallus solid,
but some plants occasionally with large inflated
epidermal cells giving the plant a “quilted”
appearance typically seen in members of the
Anthocerotaceae s. str. Thallus concave-convex
to plano-convex in transverse section, 7–11
cells thick. Dorsal epidermal cells quadrate to
hexagonal, 28–92 × 19–53.3 µm. Cells with single
chloroplast and pyrenoid. Some populations with
dorsal stalked obpyriform to obovoid-shaped
propagules (583–1,000 × 473–500 µm). Surface
of propagules crenulate because of bulging
epidermal cells. Stalk up to 1000 µm long and
500 µm wide, composed of rectangular cells with
single orange chromoplast. Plants sometimes with
ventral unstalked tubers. Ventral clefts flanked
by two cells at apical notch. Nostoc colonies
scattered through thallus, appearing as dark dots.
Rhizoids hyaline along ventral surface.
Monoicous, androecia scattered over dorsal
surface, 1–4 antheridia per cavity, spherical
yellow-orange, on short stalks, 115–132.5 × 82.5–
100 µm, jacket cells irregularly arranged. Involucre
erect and cylindrical, contracted at the mouth,
1.2–2.8 mm long, 4–10 cells thick. Capsules erect,
5–12 mm long, exserted, splitting by two valves,
assimilative layer 4–7 cells thick in transverse
section, sporogenous layer 2 cells thick, with welldeveloped columella. Epidermal cells of capsule
elongate rectangular (66–143 × 8.5–19.2 µm)
punctuated with stomata (33 × 21 µm). Spores
bright yellow, rounded-tetrahedral, with smooth
border, equatorial diameter from 32–49 µm.
Distal surface with numerous coarse, wart-like
protuberances, frequently coalescing in the center
of the face, with smaller scattered verrucae in
between larger protuberances, equatorial girdle
smooth. Proximal surface with distinct triradiate
mark covered in small spherical to baculate papillae on either side of a narrow, smooth dehiscence
line. The three triradiate faces of the proximal
surface covered with distinct button-like verrucae. A distinct shallowly papillate margo encircles
the entire proximal face. Pseudoelaters 1–3 cells,
36–164 × 9.5–33 µm, pale brown, thin-walled,
occasionally branched.
ETYMOLOGY—The species epithet “evanidus”
in Latin means vanishing. Stephani was probably
referring to the ephemeral nature of this species.
DISTRIBUTION AND ECOLOGY—This species is
confined to the tropical northeastern region of
Australia from the Atherton Tablelands of Far
North Queensland to northern New South
Wales.
AFFINITIES AND DIFFERENTIATION—Possibly
overlooked because of small size of plants (Fig.
1b), it is distinguished from both P. carolinianus
and P. inflatus by its distinct spore patterning
(Fig. 5). The spore distal face of the former
species is covered in spine-like protuberances,
whereas that of the latter species displays fewer,
less coarse protuberances. Both species also lack
the number of distinct button-like verrucae covering each of the triradiate faces. The proximal
micro-ornamentation between verrucae is lacking
in P. evanidus, whereas it is composed of interweaved vermiculae for both P. carolinianus and P.
inflatus. It is also distinguished from P. inflatus by
its monoicous sexual condition (Fig. 4).
SPECIMENS EXAMINED—New South Wales: Duck
Creek Rd., 22 km WNW of Bulahdelah, disturbed
clearing beside road at edge of forest dominated by
Eucalyptus. Curnow 3304 (CBG 9313538); New South
Wales. Leichardt s.n. (MEL 1039120). Queensland: Port
Denison [Qld]. W.W. Birch s.n. (lectotype G 2107/5);
Charleys Creek, 18 km NNE of Proserpine, poor,
scrubby forest on rocky hillside, on soil. Curnow 1160
(CANB 753174); Millstream Falls NP, on bare soil on
side of walking track down to lookout Cargill & Fuhrer
875, 876 (CANB 753175, CANB 753176); Queensland.
Bowmann (MEL1039123) Millstream Falls, Ravenshoe,
on bare soil on side of walking track. Cargill 55100 +
CARGILL AND FUHRER: PHAEOCEROS TAXONOMIC STUDIES
245
FIG. 4. Phaeoceros evanidus. (a–b) Gametophytes
with sporophytes. (a) Scale = 4 mm; (b) two plants,
scale = 3 mm; (c) gametophytes with sporophytes and
propagules, scale = 5 mm; (d) propagules (pr), scale =
100 µm, and epidermal cells of propagules; (e) transverse section through thallus displaying a concaveconvex shape, scale = 100 µm, and internal cells of
thallus; (f) TS through sporophyte (as = assimilative
layer, col = columella, te = tetrads); (g) dorsal
epidermal cells of gametophyte thallus. All cell
illustration scales = 100 µm.
dupl. (MUCV 7986 & MUCV 7987); Broadwater Forest
Park, W. of Ingham, Stone s.n. (MELU 1084)
Phaeoceros inflatus (Steph.) Cargill & Fuhrer
comb. nov.
Basionym—Anthoceros inflatus Steph., Spec.
Hepat. 5: 990. 1916. Type: Australia, New South
Wales, Uralba, W.W.Watts 391 (lectotype in G!,
isolectotype in NSW!).
Thallus bright green to yellow-green to olive
green (RHS Colour Chart: males 144A, B; females
143B), becoming brown when dried, growing on
soil or rocks in mats or rosettes. Female plants
246
small to medium in size, up to 20 mm in length
and 5 mm in width, irregularly branched, apices
of branches spathulate. Thallus solid, 8–9 cells
thick, usually concave-convex, fleshy. Margins of
plants entire, undulate or irregularly crenulate.
Dorsal epidermal cells rectangular to hexagonal,
28–79 × 20–56 µm. Plants frequently with ventral
unstalked tubers. Ventral clefts not observed.
Nostoc colonies scattered through the ventral
portion of thallus as dark dots. Rhizoids ventral
and hyaline or pale brown.
Dioicous, male plants smaller, up to 10 mm
long and 2 mm wide. Androecium with (1–)2–3
antheridia per cavity, ovoid to spherical, white to
bright yellow, sunken into thallus, 163–250 ×
133–150 µm on short stalks, cells of jacket irregularly arranged. Involucres erect cylindrical, up to
4 mm long. Capsules up to 40 mm long, one per
involucre, splitting on either one or two sides by
way of two valves, frequently remaining attached
at apex, stomata scattered throughout epidermal
layer, 61–77 × 41–51 µm, assimilative layer 5–7
cells thick in transverse section, sporogenous layer
1–2 tetrad layers thick, with well-developed columella. Epidermal cells of capsule rectangular to
hexagonal and elongate 59–187.5 × 15–30 µm.
Spores yellow to yellow-grey, 37.5–56.5 µm in
diameter, rounded-tetrahedral. Distal surface
with irregularly scattered, coarse protuberances,
variable in shape crowned with one to several
blunt triangular-shaped, wart-like or tuberculate
papillae, never spine-like, intervening surface
wrinkled, finely papillate or nearly smooth.
Proximal surface with distinct, broad triradiate
mark, entire face surrounded by a distinct
cingulum. Triangular faces, flat or concave, with
fine interwoven vermiculate-like patterning on
surface, verrucae confined to central section of
each face and can be distinct or indistinct.
Pseudoelaters pale brown to dark brown at
maturity, transparent, thin-walled and 1–4 celled,
(41–)46–297 µm in length and 7.5–28(–38.4) µm in
width, linear or branched.
ETYMOLOGY—The species epithet “inflatus”
arises from Stephani’s observation of an inflated
assimilative layer within the capsule resulting
in a bulging involucre (see Stephani’s Icones
Hepaticarum).
DISTRIBUTION AND ECOLOGY—A relatively
common species among the Australian
anthocerotes, extending down the eastern area
of Australia from Queensland down to Victoria.
FIELDIANA: BOTANY
FIG. 5. SEM micrographs of spores of Phaeoceros evanidus. (a) Distal face; (b) one of the triradiate sections of
proximal face; (c) proximal face and equatorial view of spores; (d) group of spores and pseudoelaters. All scales =
20 µm, except (b) = 10 µm. [a–d from type of Anthoceros evanidus (G)]
Typically found growing on moist soil of banks
and pathways, often in shaded habitats.
AFFINITIES AND DIFFERENTIATION—Stephani
described this species from a specimen sent to him
by Rev. W. W. Watts from the Richmond River
at Uralba, NSW (Stephani, 1916). His description
of this taxon is somewhat confusing, in that he
has described the thallus “cavernosa” which is
typical of Anthoceros s. str.; yet, he is clear that
the spores are pale yellow and minutely papillate.
Examination of the type specimen confirms its
placement within the genus Phaeoceros with
possession typically of a solid thallus, irregularly
arranged jacket cells of the antheridia and yellow
spores. It differs from both P. carolinianus and
P. evanidus in its dioicous sexual condition and
irregular coarse protuberances topped by smaller,
irregular-shaped papillae observed on the distal
face of the spores (Figs. 1c, 6, 7).
SPECIMENS EXAMINED—Australian Capital Territory:
Head of Murray’s Gap, Bimberi Range, on mud banks
in swampy herb. field, Schodde 1302 (NSW 261525 &
CANB 108656). New South Wales: Richmond River,
Uralba, on ground, hill top. 23 September 1901. W. W.
Watts n. 371 (lectotype G! ; isotype NSW 261462!);
Hurstville, near Sydney, on earth, Whitelegge (NSW
259158); North Shore, Sydney, Whitelegge (NSW
259155); NSW 261701; Hurstville near Sydney,
Whitelegge (MEL 1039090); North Shore, Sydney.
Whitelegge s.n. (MEL 1039191). Queensland: Flinders
River (MEL 1039114). Victoria: Near Dimboola. Willis
s.n. (MEL 1039091); end of forest road to Hogan’s
Flat, above Lerderderg River Gorge (and opposite Mt.
CARGILL AND FUHRER: PHAEOCEROS TAXONOMIC STUDIES
247
Blackwood), Blackwood Ranges. Willis s.n. (MEL
1030295); Anderson Inlet, (MEL 1039119); Heathermere
Siding Rd., Heathermere, Cargill & Fuhrer 17733 (MELU
6368); Yeodene, SE of Colac, Beauglehole 1965 (MEL
1043437); Belgrave Sth camping ground, on moist clay
bank beside lake, Scott s.n. (MUCV 367); Whitehills
Dam, Rushworth, Scott s.n. (MUCV 4787); Yarra GlenYea Rd. (west side), on damp clay bank, under trees,
Scott s.n. (MUCV 4328); Main Ridge, Mornington
Peninsula, on clay soil in Eucalyptus obliqua forest,
Scott s.n. (MUCV 2561); Scott’s [farm] block, Frazer
River, King Island, Scott s.n. (MUCV 4022); Jumping
Creek, Warrandyte SP, carpark, on bare soil at side of
road, Cargill & Fuhrer 55014, 55015, 55030 (MELU 7917,
7922, 7916); Silverband Falls, Grampians Nat. Park, at
base of walking track on earth bank, Cargill & Fuhrer
55022, 55025, 55027, 55028, 55029.(MUCV 7906, 7911,
7913, 7914, 7915); Mt. Victory Rd. near Hall’s Gap,
Grampians Nat. Park, rocky alcove on side of road in
deep shade, Cargill & Fuhrer 55020 (MUCV 7903).
Phaeoceros engelii Cargill & Fuhrer sp. nov.
FIG. 6. Phaeoceros inflatus. (a–c) Female gametophytes (No = Nostoc colonies), scale = 3 mm; (b) scale =
4 mm; (c) scale = 5 mm (vt = ventral tuber); (d) dorsal
epidermal cells, scale = 100 µm; (e) TS through thallus,
scale = 100 µm; (f) internal cells of thallus, scale = 100
µm; (g) TS through sporophyte (ep = epidermal cells, as
= assimilative layer, sp = spores; el = pseudoelaters); (h)
mature spore and pseudoelaters, scale = 100 µm.
Type—Australia. Victoria. Lower Glenelg
National Park. Kentbruck Rd. bridge over
Moleside Crk. 11 October 2006. Cargill & Fuhrer
1016 (Holotype CANB).
Ab omnibus aliis speciebus Phaeoceratis propagulis
numerosis habens praeter margines thalli, coloniis nostocinis ventralibus tumescentibus, et propriis eminentia
trabeculatis in pagina distali sporarum, differt.
FIG. 7. SEM micrographs of spores of Phaeoceros inflatus. (G): (a) Distal face; (b) proximal face. Scale = 20 µm.
[a, b from type of Anthoceros inflatus (G)]
248
FIELDIANA: BOTANY
Thallus yellow-green (RHS Colour Chart
146A), but appearing dark green at habitat
because of deep shade and becoming black-green
when dried, growing on soil or rocks in mats close
to edge of creek or on rocks in creek or on banks
of creek. Female plants up to 60 mm long and up
to 11 mm wide, irregularly furcate branching,
frequently with young lateral branches forming
on mature thallus, lobes lingulate at apices.
Thallus solid, 8–13 cells thick, plano-convex to
concave-convex in transverse section, fleshy.
Margins of thallus irregularly crenulate, with
some populations possessing margins fringed
with deciduous propagules. Dorsal epidermal
cells quadrate to hexagonal, 25–57.5 × 22.5–37.5
µm. Thickening of ventral apices observed in
plants not unlike the ventral unstalked tubers
typically seen in this genus. No ventral clefts
observed. Nostoc colonies scattered through
thallus becoming spherical and bulging significantly from ventral surface with maturity.
Rhizoids ventral and pale brown.
Subsequent maturation of the sporophytes and
examination of the spores placed it squarely in
the genus Phaeoceros.
AFFINITIES
AND
DIFFERENTIATION—
Collections made in later years revealed plants
with numerous deciduous propagules growing
almost like a fringe around the margins of the
thallus (Figs. 1d, 8a). They are also found growing in patches on the dorsal and ventral surfaces
of the thallus. Not infrequently, it would appear
that some propagules remained attached to the
parent thallus and grow to produce secondary
branches. Similar structures were also observed
and described by Howe for the species Anthoceros
vegetans M. Howe (Howe, 1934) and by Stephani
for the Chilean species P. propaguliferus (Steph.)
Prosk. (Stephani, 1917). Also peculiar to this
species is the morphology of the mature Nostoc
colonies, which bulge out as a relatively large
hemispherical growth from the ventral surface of
the thallus (Fig. 8c), unlike the typical colonies,
Dioicous, male plants smaller, up to 21 mm
long and 4 mm wide. Androecium with 2
antheridia per cavity, ovoid, pale yellow, sunken
into thallus, 175–325 × 150–240 µm, on short
stalks, jacket cells irregularly arranged. Involucres
erect, cylindrical, flaring at base up to 5 mm long,
5–8 cells wide in transverse section. Capsules up
to 30 mm long, one per involucre, exserted,
becoming blackish brown at tips with maturation
of spores, opening by two valves, 6–8 cells thick in
transverse section, stomata scattered throughout
epidermal layer, 72.5–90 × 42.5–60 µm. Epidermal
cells of capsule rectangular to hexagonal and
elongate 82.5–170 × 12.5–27.5 µm. Spores yellow,
38–56.3 µm in diameter, rounded-tetrahedral.
Distal surface covered in short irregular
trabeculate protuberances frequently coalescing
to form irregular lamellae. Proximal surface
covered in numerous irregular-shaped verrucae.
Pseudoelaters pale brown at maturity, transparent, thin-walled and 1–4-celled, linear or branched,
67–223 µm in length and 15–23 µm in width.
ETYMOLOGY—Named for Dr. John Engel to
commemorate his 40 years in hepaticology.
DISTRIBUTION AND ECOLOGY—This species
is known only from one location beside and
within a creek in the Lower Glenelg National
Park. Its habitat preference is very similar to that
of most Megaceros populations in relatively
shady conditions near running water. In fact,
when first collecting this hornwort, we had
thought that it was indeed a Megaceros.
FIG. 8. Phaeoceros engelii. (a) Female gametophytes with marginal propagules, scale = 10 mm; (b)
male gametophytes, scale = 10 mm; (c) TS through thallus illustrating Nostoc colony bulging from ventral surface, scale = 3 mm; (d) internal cells of thallus, scale =
100 µm; (e–f) TS through sporophyte and involucre, (e)
scale = 3 mm, (f) scale = 100 µm (inv = involucre, sp =
sporophyte, te = tetrad, col = columella; (g) spore and
pseudoelaters, scale = 25 µm.
CARGILL AND FUHRER: PHAEOCEROS TAXONOMIC STUDIES
249
which remain small and well embedded in the
ventral portion of the thallus (Fig. 6e). This phenomenon has not typically been observed in other
Australian species of Phaeoceros. The sexual condition and spore distal pattern (Fig. 9) distinguish
this species from both P. carolinianus and P.
evanidus, both of which are monoicous, whereas
P. engelii is dioicous. Also, the more robust habit
of the populations of P. engelii (Figs. 1d, 8) separates it immediately from the more diminutive
P. evanidus.
It differs from P. inflatus in its possession of
numerous propagules, but where these are not
apparent, it differs significantly in the spore
distal patterns. The spores of P. inflatus, while
displaying protuberances from the distal face,
differ in their micro-morphology. Phaeoceros
engelii displays trabeculate protuberances
(Fig. 9), whereas P. inflatus displays typically
fewer, coarser protuberances that are often
crowned by another layer of spine-like or
wart-like papillae (Fig. 7).
SPECIMENS EXAMINED—Victoria: Kentbruck Rd.
bridge over Moleside Crk., Lower Glenelg NP. Cargill
& Fuhrer 1016 (Holotype CANB); Cargill & Fuhrer
363 (CANB 654152); Cargill & Fuhrer 1015, (CANB);
Cargill & Fuhrer 1017 (CANB).
Key to the Species
1.
1.
2.
2.
3.
3.
Plants monoicous …...........................………..……..........................………….............…………...2
Plants dioicous ….............................……………..........................………….................…………...3
Plants robust, up to 20 mm long, without propagules, widespread distribution, spores with spinelike protuberances over distal face ..…..........................................…..…….Phaeoceros carolinianus
Plants delicate, up to 15 mm long, sometimes with dorsal propagules, restricted in distribution to
tropical and subtropical areas, spores with large, wart-like, coalescing protuberances, proximal
surface with distinct button-like verrucae covering each triangular face...........Phaeoceros evanidus
Plants dark green, often with propagules along margins of thallus and with bulging ventral Nostoc
colonies, restricted distribution, spore distal face covered in short trabeculate protuberances
frequently coalescing to form short lamellae .......................................................Phaeoceros engelii
Plants bright green, without propagules, Nostoc colonies not bulging, widespread, spore distal
face with scattered irregular protuberances .................................…...………… Phaeoceros inflatus
TABLE 1.
Phaeoceros
species
Size of
plants
P.
Up to
carolinianus
20 ×
15 mm
P. evanidus Up to 15
× 2–
15 mm
P.
inflatus
P. engelii
250
Females;
up to 20
× 5 mm
males up
to 10
× 2 mm
Females
up to 60
× 11 mm;
males up
to 21
× 4 mm
List of distinguishing characters of four Australian species of Phaeoceros.
Color
Yellowgreen to
dark
green
Pale
yellowgreen to
green
Bright
green to
yellowgreen to
olive
green
Yellowgreen
to
green
Tuber
type
Propagules
Nostoc
colonies
No. of
Sexual antheridia
condition per cavity
Unstalked, Absent
ventral
marginal
Embedded
Monoicous
in thallus,
not bulging
2–5
Unstalked, Dorsal
ventral
marginal
Embedded
Monoicous
in thallus,
not bulging
1–4
Unstalked, Absent
ventral
marginal
Embedded
in thallus,
not
bulging
Dioicous
(1–)
2–3
Unstalked, Marginal,
ventral
ventral
marginal
and
dark
dorsal
Ventral and
bulging
Dioicous
2
Spores
Yellow,
distal
face
spiney
Yellow,
distal
face
wart-like
Yellow,
distal
face
coarsely
papillate
Yellow,
distal face
trabeculate
forming
lamellae
FIELDIANA: BOTANY
FIG. 9. SEM micrographs of spores of Phaeoceros engelii (a, c) distal face; (b, d) proximal face; (e) detail of
micro-ornamentation of distal face; (f) detail of micro-ornamentation of proximal face. Scales (a–d) 10 µm, (e–f) 1
µm. [a–f Cargill & Fuhrer 363. Victoria. Lower Glenelg NP. Moleside Crk.]
Acknowledgments
The initial research on the hornworts was
supported by an Australian Biological Resource
Study (ABRS) grant to the senior author and Dr.
Neil Hallam in 1992. We also thank the directors
and curators of the following herbaria:
Conservatoire et jardin botaniques, Genève (G)
for access to type specimens from F. Stephani’s
herbarium collection; AD, BRI, CANB, MEL, MELU,
CARGILL AND FUHRER: PHAEOCEROS TAXONOMIC STUDIES
251
NSW and SYD for the loan of their Australian
hornwort collections. Much appreciation to
Mr. Laurie Adams, who kindly composed the
Latin diagnosis. Also, both authors are much
obliged to the two reviewers, Juan Carlos
Villarreal and Matt von Konrat for their
insightful comments resulting in a much improved
paper.
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