Download A new flatworm (Platyhelminthes: Polycladida) which mimics a

<oological Journal of the Linnean Society (1994), 110: 19-25. With 2 figures
A new flatworm (Platyhelminthes:Polycladida)
which mimics a Phyllidiid Nudibranch
(Mollusca, Nudibranchia)
L. J. NEWMAN, L. R. G. CANNON
Worms, Queensland Museum, P . O . Box 3300, South Brisbane, Eld. Australia 4101
AND
D. J. BRUNCKHORST
Australian National Parks €5' Wildlfe Service, P . O . Box 636, Canberra, A C T .
Australia 2601
Received December 1992, acceptedfor publication April 1993
A new species of polyclad flatworm, Pseudoceros imitatrrs sp. nov. (Polycladida,
Pseudocerotidae), is described from Papua New Guinea and recorded from the Great Barrier Reef,
Australia. This polyclad resembles the phyllidiid nudibranch Phyllidiella pustulosa (Cuvier)
(Nudibranchia, Phyllidiiae) in size and colour pattern. I t is proposed that P. imitatus is a mimic of
the aposematic nudibranch in order to avoid predation by reef fish. Mimicry between polyclad
flatworms and opisthobranch molluscs is reviewed.
ADDITIONAL KEY WORDS:-Pseudocerotidae
aposematic - mimicry.
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Pseudoceros
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nudibranch - Phyllidiidae
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CONTENTS
Introduction . . .
Methods . . . .
Systematics . . .
Material examined
Description . .
Taxonomic remarks
Discussion
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Acknowledgements
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References
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INTRODUCTION
Coral reef inhabitants are characterized by their conspicuous colours and
patterns. These are believed to provide camouflage, to function as sexual flags, to
serve as warning colours or for the purpose of mimicry. Typically, phyllidiid
nudibranchs are brightly coloured and possess particularly repugnant, noxious,
002+4082/94/001019
+ 07 S08.00/0
19
0 1994 The Linnean
Society of London
20
L. J. NEWMAN E T AL.
bioactive compounds for chemical defence which they sequester from their
sponge food (Faulkner & Ghiselin, 1983; Brunckhorst, 1991). These animals are
usually seen exposed during the day advertising their presence to predators, i.e.
they are aposematic (Brunckhorst, 1991). Brunckhorst (1988, 1989) was the first
to report mimics of these nudibranchs, one of which was a n unidentified polyclad
flatworm. Subsequently, Glosliner and Behrens ( 1990) reported mimicry between
a dorid nudibranch and a flatworm.
Polyclad flatworms, generally dull in temperate waters, are often brilliantly
coloured and conspicuous in tropical waters. Hyman (1951) believed the bright
and constrasting hues served as warning colouration. T h e observation of Johnson
( 1983) of the brilliantly coloured Persian carpet worm, Pseudobiceros bedfordi
(Laidlaw) and Pseudoceros zebra (Leuckart) crawling about in the open during the
day would support this. Hyman (195 1) also suggested that flatworms are seldom
eaten by predators as their surface secretions appear distasteful, if not toxic.
Certainly, polyclads are often seen damaged (Johnson, 1983; Newman, pers.
obs.).
The most commonly recognized tropical polyclads are members of the genus
Pseudoceros. Over 130 species have been recognized, primarily on the basis of their
colour patterns (Hyman, 1951; Prudhoe, 1985). Sixteen species are recorded
from tropical Australian waters (Hyman, 1954, 1959; Prudhoe, 1977), while
only two species have been described from Papua New Guinea (Palombi, 1931;
Faubel, 1984). The biologrcal significance of colour patterns in these flatworms
has not been investigated. T h e polyclad mimic of the phyllidiid nudibranch
reported by Brunckhorst (1988, 1989) proves to be a new species of Pseudoceros,
which is described here.
METHODS
Worms were hand collected by Scuba and fixed in 10% formalin buffered
with seawater or Bouin’s fluid. Colour photographs were taken in situ. Whole
mounts were prepared by first staining with Mayer’s Haemalum, then
dehydrating in graded alcohols and mounting in Canada balsam. Longitudinal
serial sections of the reproductive regions were prepared by embedding tissue in
56°C Paraplast, cutting at 6-8 pm, and staining with haematoxylin and eosin.
Drawings and measurements were made with the aid of a camera lucida. All
material is lodged at the Queensland Museum: wholemounts are designated
(WM) and serial sections (LS).
SYSTEMAlICS
Order Polycladida Lanig, 1884
Suborder Cotylea Lang, 1884
Family Pseudocerotidae Lang, 1884
Genus Pseudoceros Lang, 1884
Pseudoceros imitatus sp. nov.
(Figs. IA-C, 2A)
POLYCLAD M I M I C O F NUDIBRANCH
21
C
pr
I
's
Pe
Figure 1. Pseudoceros imitatus sp. nov. A, Dorsal surface colour pattern; B, Holotype,
morphology of the ventral surface; C , Diagrammatic reconstruction of the reproductive system
(c = cement glands, e = ejaculatory duct, i = intestine, p = pharynx, pe = penis papillae, pr =
prostatic vesicle, s = stylet, se = seminal vesicle, v = vas deferens). Scale bars = 2 mm.
Material examined
Holotype. 1 8 m depth, patch reef 1 km south of Lion Island, off Motupore
Island, southwest Papua New Guinea, 17 June 1988, D. J. Brunckhorst, Q M
G210006 (WM), plus LS of reproductive region. Colour transparencies of the
L. J. NEWMAN E l A L .
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Figure 2. Comparison of the colour pattern of (A) the Hatworm Pseudoceros imifrtussip. nov.
and (B) the nudibranch Phyllidklla pustulosu, in situ, from southwest Papua New Guinea (photos by
D. J. Brunckhorst) (scale bar=5 mm).
holotype are also lodged, Q M Photographic Index # 138 & 139. Paratype:
same data as holotype, QNI 210007 (LS). Other material: 15 m depth, outer reef
off Wongad Island, Madlang, northeast Papua New Guinea, 27.10.92, R.
Hanley, Q M 2 10008 (WM ) . Record: 20 m depth, Wheeler Reef off Townsville,
northeast Australia, 24 November 1974, I. Loch, colour transparencies Q M
Photographic Index # 134-137.
Descr$tion
Colour and pattern. Dorsal surface black with large irregularly shaped creamyellow spots, each raised medially, some fused to form pustules of varying shapes
and sizes (Figs. lA, 2A). Margin composed of smaller spots which merge
together. Tips of the anterior marginal tentacles are black. Colour pattern of the
Australian specimen varies slightly; spots are more numerous and fused to form
elongate longitudinal groups of pustules, and black pigmentation is reduced
forming irregular lines between the pustules. Preserved colour of the holotype is
black, the chromatophores embedded in the parenchyma, and irregular beige
spots. Ventral surface grey-black fading to cream centrally, with cream margin
(Fig. 1B).
Morphology. Body elongate and oval, soft, relatively small (holotype 13 mm
long x 7 mm wide preserved, paratype 8 mm long x 5 mm wide preserved,
Madang specimen 18 mm long x 10 mm wide preserved) (Fig. 1A). Margin with
few shallow ruffles, anteriorly forming two pointed folded pseudotentacles.
Cerebral eyespot composed of about 60 eyes (in largest specimen) in horseshoe
shaped cluster. Marginal eyes obscured due to the black pigment, few eyes
laterally on the pseudotentacles. Pharynx anterior, highly ruffled with numerous
bifurcating folds and mouth central (Fig. 1B). Male pore mid-body, near and
posterior to the pharynx, female pore directly posterior to male pore. Sucker
mid-body, 2.4 mm posterior to female pore.
Reproductive system. Only the male reproductive system is mature in the
holotype: paratype is immature and Madang specimen mature, but damaged
medially .
\
Y
POLYCLAD MIMIC OF NUDIBRANCH
23
Male. Testes ventrally scattered throughout the body, vasa deferentia with
ducts arising posteriorly and laterally on each side a t the level of the sucker, they
enter ventrally into the seminal vesicle (Fig. 1C). Seminal vesicle relatively long,
1.0 mm total length, U-shaped with thick walls. Ejaculatory duct leaves the
anterior end of the seminal vesicle and coils dorsally then ventrally to join the
prostatic duct in the middle of the penis. Prostatic duct short, leading from a
small (0.3 mm length) oval, thin walled prostatic vesicle. Single male pore, male
antrum shallow, penis armed with a short sclerotic stylet.
Female. Female pore 1.3 mm behind the male pore, with prominent cement
glands developing. Ovaries scattered dorsally throughout the body. Oviducts
and vagina not developed.
Diagnosis. Pseudocerotidae with ruffled pharynx, male copulatory system
directly behind or beneath the pharynx, prostatic vesicle free without folds, and
female apparatus single. Pseudoceros, sensu strictu according to Faubel (1984) (i.e.
with tentacular and cerebral eyes present, male copulatory apparatus single with
seminal vesicle, prostatic vesicle antero-dorsal to male complex, and armed penis
papilla) with a U-shaped muscular seminal vesicle. Dorsal surface with raised
cream-coloured spots, forming soft irregularly shaped pustules.
Etymology. The specific name imitatus (from imitator L. masc. = mimic) was
chosen as this species imitates a phyllidiid nudibranch.
Taxonomic remarks
Pseudoceros imitatus does not resemble any other described species of Pseudoceros:
its colour and pattern of irregular pustules are unique. The soft raised pustules
are not similar to the large acute papillae found in Acanthozoon which, in this
genus, also contain branches of the gut diverticula. Details of the reproductive
system of only some 20 species of Pseudoceros are known. Only one other species
possesses a long curved seminal vesicle and small penis stylet, viz. P. pardalis
Verrill from Bermuda. Pseudocerospardalis can be distinguished from P. imitatus by
its curved prostatic vesicle and pattern of regular rounded bright yellow spots on
the flat smooth dorsal surface.
DISCUSSION
In contrast to terrestrial organisms, such as butterflies, the role and
importance of warning colouration and mimicry in marine organisms is virtually
unknown. Whilst further intensive field studies are required, some evidence for
aposematism, mimicry and related behavioural mechanisms in marine
invertebrates, particularly opisthobranch molluscs, has been reported
Edmunds, 1974; Ros, 1977; Brunckhorst, 1989, 1991; Gosliner & Behrens, 1990;
Rudman, 1991). Intra-phyletic Batesian or Mullerian mimicry are rarely
reported as it is difficult to establish mimetic roles through field observations.
Such species should be studied in the context of their visual perceptions
(Edmunds, 1987; Brunckhorst, 1991).
Pseudoceros imitatus bears a striking resemblance to the common reef
nudibranch Phyllidiella pustulosa (Cuvier) (Fig. 2B). This nudibranch has
irregular groups of hard pustules on the dorsal surface which are surrounded by
24
L J NEWMAN E T A L
a reticulum of narrow black lines. Furthermore, the rhinophores (resembling the
pseudotentacles in Pseudoceros) are black in colour. Gills in phyllidiid
nudibranchs are found ventro-laterally and hence the only obvious
distinguishing characteristic between this nudibranch and this flatworm, in situ,
are the retractable rhinophores of the nudibranch. The pustules in P. pustulosa
are generally pale pink but can range to grey-green. Both the nudibranch and
the flatworm have a pale dorsal margin. Therefore, these two species are
extremely similar in their dorsal morphology, colour and pattern.
The biology and ecology of tropical pseudocerotids are largely unknown and
these polyclads can be considered rare, as most species are known only from
single records. On the other hand, the nudibranch P.pustulosa is known to be one
of the most common tropical nudibranchs, and its aposematic coiouration and
flamboyant behaviour are well documented (Johnson, 1989; Brunckhorst, 1989,
1991). It is therefore assumed that P. imitatus mimics the more common
phyllidiid in order to avoid predation by reef fish, which learn to associate these
colour patterns with something inedible.
Arndt (1943) demonstrated with crude extracts injected intracardially and
intraperitoneally that some mediterranean polyclads are toxic to vertebrates
(frogs and guinea pigs). Three acotylean species have been reported to contain
toxins such as tetrodotoxin (Halstead, 1978; Miyazawa et al., 1986), but detailed
studies have not been undertaken ofcotyleans. Randall & Emery (1971) found a
juvenile reef fish that mimics a pseudocerotid in colour pattern and behaviour
(undulations of the margin). It seems possible that this juvenile fish might be
mimicking a toxic flatworm.
The question remains as to whether pseudocerotid flatworms are unpalatable
and displaying aposematic colouration, or whether they are simply mimicking
distasteful nudibranchs. Edmunds (1974) stated that unless an animal is
exceptionally noxious and resilient to sampling by a predator, it is difficult to see
the selective advantage for a rare species in being conspicuous instead of noxious.
O n the other hand, Rudman (1991) suggested that relatively rare species with
bright obvious unique colour patterns are ignored by predators because of their
novelty. Further research into flatworm taxonomy, biology and biochemistry is
needed in order to determine the significance of the colour patterns in
conspicuously patterned polyclads.
ACKNOWLEDGEMENTS
The authors are indebted to: M r Ian Loch, Australian Museum; Dr Russell
Hanley, Northern Territory Museum; Dr Matthew Jebb, Christensen Research
Institute (CRI contribution 91); staff of the University of Papua New Guinea,
Motupore Island Research Station; and Mrs Christine Lee, Queensland
Museum. Funding for this research was supported by the Australian Research
Council (LRGC) and Hawaiian Malacological Society (DJB).
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POLYCLAD MIMIC OF NUDIBRANCH
25
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