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Food of giants - field observations on the diet of Syrinx aruanus (Linnaeus, 1758) (Turbinellidae) the largest living gastropod

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Abstract

Field observations and analysis of faeces from Syrinx aruanus, the largest living gastropod, show that it feeds on large polychaete worms including species of Polyodontes (Acoetidae), Loimia (Terebellidae) and Diopatra (Onuphidae). This is consistent with the known food of other species of Turbinellidae which regularly include polychaetes in their diet.
Food of giants – field observations on the diet of
Syrinx aruanus (Linnaeus, 1758) (Turbinellidae)
the largest living gastropod
John D. Taylor and Emily A. Glover
Department of Zoology, The Natural History Museum, London SW7 5BD, United Kingdom.
Email: j.taylor@nhm.ac.uk
Abstract – Field observations and analysis of faeces from Syrinx aruanus, the largest living
gastropod, show that it feeds on large polychaete worms including species of Polyodontes
(Acoetidae), Loimia (Terebellidae) and Diopatra (Onuphidae). This is consistent with the known
food of other species of Turbinellidae which regularly include polychaetes in their diet.
INTRODUCTION
Syrinx aruanus (Linnaeus, 1758) which inhabits the coasts of western and northern Australia
to Irian Jaya (Wells, 2002) is recognised as the largest living gastropod with shells reaching up
to 91cm in length (Hawaiian Shell News, 1982). Despite its familiarity in books, shell
collections and as ornaments little is known of the biology of this species including the question
of what it eats. Large Syrinx are a popular target of shell collecting activities and populations in
easily accessible habitats are certainly diminished. Conservation of the species is desirable but
there is little biological information on which to base any measures. The only information
concerning the diet of Syrinx is a brief sentence by Wilson (1994) who notes p. 59: “The author
has observed this animal feeding on large, tubiculous polychaete worms on a Western Australian
sand flat.” The discovery of a small population of Syrinx in intertidal habitats around the Burrup
Peninsula, Dampier (Figure 1) enabled us to make some observations on the diet of these large
gastropods which are reported here.
The complex nomenclatural history of the Syrinx aruanus was documented by Harasewych &
Petit (1989). They also showed, using details from the anatomical study by Kesteven (1904),
that from characters of radula, proboscis, protoconch, operculum and egg case, Syrinx should
be included in the subfamily Turbinellinae of the Turbinellidae rather than the Melongenidae
where it had been traditionally placed. The only available illustrations of the radula of S.
aruanus are the drawings in Kesteven (1904 pl. 42, fig. 3) so, additionally, we provide SEM
images of the radula teeth taken from a small specimen from Dampier.
METHODS
Between 25 July – 8 August 2000 a few individuals of Syrinx were observed inhabiting the
low intertidal, muddy sand flats of Withnell Bay on the Burrup Peninsula near Dampier, north
F. E. Wells, D. I. Walker and D. S. Jones (eds.) 2003. The Marine Flora and Fauna of Dampier, Western Australia.
Western Australian Museum, Perth.
218 J.D. TAYLOR, E.A. GLOVER
Western Australia. By easing the animals gently away from the sediment it was seen that some
individuals had proboscides inserted into large polychaete tubes, other individuals were located
above large empty polychaete tubes and in other cases the Syrinx were resting in depressions in
the sediment. Syrinx were measured in the field with a tape measure and the polychaete tubes
dug from the sediment. Because of the nature of the sediment below the surface, which
comprised coarse shell debris, it was not possible to remove complete polychaete tubes. A tube
length of 57 cm was the maximum we were able to extract.
Four individual Syrinx were removed from the shore and kept in containers of seawater
(changed twice daily) to collect faecal samples for analysis. Three of the four captive gastropods
produced faecal strings. Samples from the faecal strings were mounted on glass slides in
Aquamount and examined microscopically for remains of prey. The gastropods were
subsequently returned to their original shore positions.
RESULTS
Faecal samples
Faecal samples were obtained from three Syrinx specimens. From an animal 370mm long the
faeces consisted of a mass of fine golden fibres with setae. The long fibres and the morphology
of the setae indicate that the remains derived from a species of the polychaete family Acoetidae.
The setae are most similar to Polyodontes australiensis (McIntosh, 1885) illustrated in
Pettibone (1989, figs 73–74). This species is reported from Queensland, New South Wales and
Victoria, however, the Acoetidae of Australia are rather poorly collected and studied and there
are likely more species present.
Included amongst the Acoetidae are some of the largest polychaetes known, some reaching
lengths of over one metre. The tubes are substantial with thick walls made up of a dense matt of
fine silken fibres produced by the spinning glands of the parapodia.
Figure 1 a & b. Emersed Syrinx aruanus on intertidal sand at low water spring tide, Withnell Bay, Burrup
Peninsula, Dampier. Scale bar in Figure b = 10cm
DIET OF SYRINX ARUANUS 219
The two other faecal samples from animals of 340mm and 128mm shell lengths yielded
abundant setae and uncini from a species of the polychaete family Terebellidae. The shapes of
the uncini are similar to the two species, Loimia ingens (Grube, 1878) see Hutchings & Glasby
(1988 fig. 11) and L. ochracea (Grube, 1878), illustrated in Hutchings (1997 fig. 6).
Identification on setal characters alone is difficult but the uncini in our samples lack a projection
below the teeth suggesting the latter species as the most likely prey.
Additionally, faecal remains dissected from the rectum of a small subtidal specimen of Syrinx
76mm height, dredged off Dampier in 1999, contained setae similar to Loimia ingens.
Tubes being attacked by or situated under Syrinx
In addition to the faecal samples Syrinx were observed with proboscides extended into
polychaete tubes or the gastropods were lying above tubes. Eight such tubes were collected.
Five of the tubes (15–30mm diameter) were identified from the matt of silken fibres as being
constructed by a Polyodontes species; two of these had apertural diameters of 27 and 30mm
indicating large worms. Three other tubes (diameters 8–12.5mm) had the characteristic form
with a parchment inner layer and an outer layer of attached shells indicating construction by a
Diopatra species.
Radula
In a specimen of shell height 127mm the radula was around 950 µm in width.
Each radular row (Figure 2) consists of a central rachidian tooth flanked by lateral teeth to
each side. The central tooth is broad (550µm) but relatively narrow (150µm), tapering laterally,
with curved anterior and posterior margins. The posterior edges are raised and sharp. Each tooth
possesses a large pointed central cusp with a broad base flanked by two smaller pointed cusps
that are separated from the central cusp by deep grooves. The lateral teeth have broad bases
with a single, awl-shaped, strongly curved cusp located on the inner edge of the tooth. The
radula is very similar in morphology to that of Turbinella pyrum (slide preparation in NHM
London, and Harasewych, 1987 fig. 21).
DISCUSSION
The limited results from the faecal and field observations show that Syrinx aruanus is a
predator of large tubiculous polychaetes, including species of Polyodontes, Loimia and
Diopatra confirming Wilson’s (1994) anecdotal observation. Although polychaete feeding is a
common behaviour amongst smaller neogastropod species (Kohn, 1983: Taylor, 1984a) it seems
to be an unusual specialization amongst larger predatory gastropods. However, large
polychaetes are abundant within shallow water and intertidal muddy sand substrates of northern
Australia and provide a potential food resource for large gastropods. The possession of a long
extensible proboscis is essential to exploit these large worms which can retreat a long way back
into the tubes. Some of the Syrinx observed in the field had narrow proboscides extended for at
least 250mm into the worm tubes.
Comparison with diets of other Turbinellidae
The Turbinellidae comprises five Recent subfamilies (Harasewych, 1998) and little is known
about the feeding biology of most species. Most details of diet are available for the Vasinae,
Taylor (1984b) reporting details of the gut contents of 280 specimens of Vasum turbinellus
220 J.D. TAYLOR, E.A. GLOVER
(Linnaeus, 1758) from various localities in the Indo-Pacific. The diet comprised around 50%
polychaetes and 50% sipunculans, with chaetopterid polychaetes forming about 20% of food
items at most locations but species of Eunicidae and Terebellidae were also common prey.
Vasum rhinoceros (Gmelin, 1791) also ate polychaetes and sipunculans and Vasum ceramicum
(Linnaeus, 1758) consumed eunicid polychaetes. Another vasine for which the diet is known is
Tudivasum armigera (Adams, 1855) from Queensland (unpublished information by P.W. Arnold
reported in Taylor 1984b) where gut contents from 29 individuals contained setae from the
polychaete families Pectinariidae, Flabelligeridae and Chaetopteridae.
For the Turbinellinae, the Indian chank, Turbinella pyrum (Linnaeus,1758) is known to feed
upon terebellid and eunicid polychaetes (Hornell, 1915, Moses, 1923). Additionally, two out of
sixteen specimens of the Caribbean chank Xancus angulatus (Lightfoot, 1786) were observed
regurgitating the sipunculan Siphonosoma (Edwards, 1970, also see Kohn 1975).
The only information available for species of the deep water Ptychatractinae is a record that
the stomach contents of Benthovoluta claydoni Harasewych, 1987 included an amphipod
Figure 2 a–d. Radular teeth of Syrinx aruanus, Withnell Bay, Dampier, shell height 127 mm. a, central and lateral
teeth; b, central and lateral teeth at bending plane; c, detail of lateral teeth; d, detail of cusps on central
teeth. Scale bars: Figures a & b = 200mm, Figures c & d = 100mm
DIET OF SYRINX ARUANUS 221
(Harasewych 1987). Finally, for the Columbariinae, Harasewych (1983) reports the rectal
contents of Fulgurofusus brayi (Clench, 1959) from the Caribbean as containing large numbers
of setae from the polychaete families Serpulidae and Chaetopteridae.
In summary, for the relatively few species for which details of diet are available polychaetes
and sipunculans are important components in the diet of Turbinellidae. The diet of large
polychaetes recorded here for Syrinx aruanus is consistent with this pattern
Comparison with diets of other large gastropods
Species from several other predatory caenogastropod families (Cassidae, Ranellidae,
Fasciolariidae, Melongenidae and Volutidae) reach comparable sizes to Syrinx aruanus and it is
of interest to compare their diets.
Some of the largest living gastropods are found within the superfamily Tonnoidea namely
species of Charonia (Ranellidae) up to 330 mm and Cassis (Cassidae) 350mm Species of
Charonia are specialist feeders upon holothurians, asteroids and echinoids (Laxton, 1971,
Percharde 1972; Nurgranad et al. 2000) whilst Cassis species are specialist on echinoids
(Hughes & Hughes, 1981). Both genera utilise acidic salivary secretions (Andrews, Page &
Taylor 1999) to gain access to the prey.
Amongst the Neogastropoda, several large gastropod species are found within the family
Fasciolariidae. Pleuroploca gigantea from the Caribbean attains shell heights of 600mm and
Paine (1963a) showed that they feed upon other large gastropods such as smaller conspecifics,
but also Busycon, Fasciolaria and Murex species. In the Galapagos, Pleuroploca princeps
(Sowerby, 1825) also feeds largely on other gastropods (Stupakoff, 1986)
A number of other large gastropods are members of the family Melongenidae. In Hong Kong
Hemifusus ternatanus (Gmelin, 1791) (to around 330mm height) ate the bivalve Pinna
pectinata (Morton 1986 a). Many other melongenids have a similar diet of bivalves, including
Hemifusus tuba (Gmelin, 1791) (Morton, 1985), Busycon spp. (some species over 500mm)
(Paine, 1963b; Kent, 1983) and Melongena corona (Gmelin, 1791) (Bowling, 1994) although
Pugilina cochlidium (Linnaeus, 1758) feeds upon barnacles (Tan & Phuah, 1999)
The family Volutidae contains several large gastropod species that all seem to feed upon other
molluscs. The feeding behaviour of Melo melo (Lightfoot, 1786) was studied by Morton (1986)
who showed that it consumed other gastropods particularly Hemifusus tuba and Babylonia
lutosa. Melo amphora (Lightfoot, 1786) co-occurs with Syrinx on the lower shore at Withnell
Bay. A large specimen (ca 40 cm shell length) was seen feeding on a smaller conspecific (ca 20
cm) and totally enveloped in the foot. Similarly, Wilson & Gillett (1971, pl. 78) illustrate Melo
amphora feeding on another volute Zebramoria zebra. From West Africa, Cymbium glans
(Gmelin 1791), with a shell height up to 360mm also feeds on other gastropods including other
species of Cymbium (Marche-Marchad, 1977)
In summary, most other larger predatory gastropods feed upon other molluscs including other
large gastropods. The exceptions are the tonnoidians Cassis and Charonia which are specialist
predators upon echinoderms. Also, large gastropod species in general tend to have similar diets
to those of smaller species in their respective families, as is true for Syrinx compared with other
species within the Turbinellidae.
ACKNOWLEDGEMENTS
We are grateful to Pat Hutchings for advice on polychaetes, Brian Morton for collecting
222 J.D. TAYLOR, E.A. GLOVER
additional worm tubes and to Fred Wells, Diana Walker and Diana Jones for organising the
Marine Biological Workshop at Dampier.
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The copulation, spawning and hatching of gastropod Hemifusus ternatanus under laboratory conditions were described. After copulation, the female whelks laid trapezoidal egg capsules on the hard surface of the aquarium at about 40 min per capsule. The number of eggs (280–300 μm in size) in the capsules ranged from 1500 to 3000, positively correlated with the size of capsule. The hatchlings crawled out of the capsules over a 58-day incubation period at 21–23 °C. The hatchlings were 3.00–6.04 mm in total shell length and 4.15–21.4 mg in wet body weight, and could hang upside down the water by their feet. In an artificial culture, cutting the capsules as soon as cleft is found at the apical area may help prevent mortality. Six diets were provided over a ten-week period to compare their effects on post-hatching growth and survival. At the end of the experiment, the hatchlings fed with live clam Meretrix meretrix had the highest growth and survival rates, followed by those fed with frozen oyster Crassostrea rivularis, and was significantly higher than those fed with frozen mackerel Pneumatophorus japonicas, frozen shrimp Penaeus vannamei, eel feed, and microalgae Chlorella pyrenoidsa (P < 0.01). Although mackerels have higher protein and amino acid content than clams and oysters, the growth and survival rates of mackerel-fed hatchlings were significantly lower (P < 0.01), suggesting that other hatchling-preferred substances besides umami amino acids may be present in bivalves. In a subsequent 140-day rearing, clam-fed whelks showed a nearly linear growth (about 12 mm per month), indicating the potential of H. ternatanus for aquaculture.
... The macrofauna included the abundant asteroid Astropecten sumbawanus, an actively foraging predator of bivalves (Wells & Lalli, 2003). Six large Syrinx aruanus, a gastropod predator of large polychaetes were permanently present during the study period (Taylor and Glover 2003, this volume). Rock and cobble areas were densely covered by Saccostrea cucullata. ...
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Describes a diet consisting of c50% polychaete annelids and 50% sipunculans. Chaetopterid polychaetes form c20% of the diet at most places but species of Eunicidae and Terebellidae are also common prey items. Vasum rhinoceros, an East African species, also eats polychaetes and sipunculans, and 2 individuals of the large Vasum ceramicum had been feeding upon eunicid polychaetes. Amongst those gastropods with which it coexists Vasum turbinellus overlaps in diet with species of Mitridae and Drupa lobata and D. grossularia, which are sipunculan specialists, and to a lesser extent with species of Conus and D. morum which feed upon polychaetes, particularly from the Eunicidae and Nereididae.-from Author
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The anatomy of Latiromitra Locard, 1897, is very similar to that of other representatives of the Ptychatractinae, notably in the short or very short proboscis, the presence of an accessory salivary gland, the ventral odontophoral retractor passing through the nerve ring, and the position of the buccal mass at the proboscis base in contracted position. Latiromitra differs from Ceratoxancus by its fused salivary glands (clearly separate in Ceratoxancus). Based on anatomical and conchological characters, Cyomesus Quinn, 1981, and Okinawavoluta Noda, 1980, are confirmed and/ or placed in the synonymy of Latiromitra. The genus currently comprises 10 Recent and Neogene species, three in the Atlantic, and seven in the Indo-West Pacific, all in deep water at low latitudes. Teramachia chaunax Bayer, 1971, is placed in the synonymy of Latiromitra cryptodon (P. Fischer, 1882), and the Recent Benthovoluta sakashitai Habe, 1976, is placed in the synonymy of the Pliocene Latiromitra okinavensis (MacNeil, 1961). Volutomitra? vitilevensis Ladd, 1982 is placed in Latiromitra. Three new species are described: Latiromitra paiciorum sp. nov. (New Caledonia, 960-1100 m), L. cacozeliana sp. nov. (Vanuatu, 536-775 m), and L. crosnieri sp. nov. (Madagascar and NE of Fiji, 600-800 m). In addition, Mitra styliola Dall, 1927, from off Georgia, USA, is tentatively referred to Latiromitra.
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The feeding behavior of the gastropod Pleuroploca princeps, (Fasciolariidae) is reported. Eight species of gastropods were found to be preyed upon by P. princeps; two species of crabs were eaten as carrion. No signs of cannibalism were noticed, but intraspecific competition was observed.