The Feeding Strategy of the Predatory Gyrineum Natator
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Journal of Natural History, 2015 Vol. 49, Nos. 9–10, 483–507, http://dx.doi.org/10.1080/00222933.2014.953614 The feeding strategy of the predatory Gyrineum natator (Gastropoda: Neotaenioglossa: Ranellidae) in the Cape d’Aguilar Marine Reserve, Hong Kong, with a review of sulphuric acid use in prey access by the Tonnoidea and experimentally derived estimates of consumption Brian Morton* School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China (Received 28 January 2014; accepted 7 August 2014; first published online 10 November 2014) Under conditions of otherwise enforced starvation in filtered seawater and with only oysters (Saccostrea mordax) to feed on, an individual of Gyrineum natator consumed > 98%, on average, of its body weight of oyster tissues each week (> 14% per day). When other potential food, such as sediment, organic debris and other newly settled sessile organisms, was available to a similar-sized con- specific living in conditions of unfiltered seawater (in addition to oysters), the oysters only accounted for 1.52% of its average weekly diet (0.21% per day). This was because of the 12 proffered oysters, only four were consumed in contrast to the 12 eaten by the individual in filtered seawater. All the oysters were accessed through large holes made in their shells. It is generally understood that the salivary glands of confamilial ranellids produce secretions of sulphuric acid from greatly enlarged salivary glands and this is demonstrated herein for G. natator also. It is believed that it was these secretions that made the holes in the oyster shells. It, therefore, seems that G. natator uses sulphuric acid to attack prey only when more easily obtained food is not available. It may also be used in defence. A comparison of consumption rates for a range of scavenging and predatory gastropod taxa shows that representatives of the Nassariidae consume (much) more than preda- tors because of their opportunistic lifestyles. Gyrineum natator generally eats similar amounts to other predators, although the increased difference in estimated consumption (~10%) between this species and another similar-sized ranellid, Linatella caudata, might be because the latter did not use sulphuric acid to access its prey. Its enforced use in this study of G. natator, therefore, might represent the increased costs of using the acid to access the proffered oyster prey. Keywords: consumption; oyster prey; attack method; sulphuric acid; salivary glands Downloaded by [University of Cambridge] at 05:05 08 April 2016 Introduction The Tonnoidea comprises approximately seven families of predatory gastropods (Bouchet and Rocroi 2005) although the systematics of this diverse group of caeno- gastropods is still debated. Moreover, the feeding biology of most representatives of these familial taxa are undescribed, adding to the systematic confusion. The best understood tonnoideans in terms of their feeding biology are representatives of the Tonnidae and Cymatiidae (or Cymatiinae), as will be discussed. Conversely, the diets and feeding strategies of the Ranellidae are poorly known. *Email: [email protected] © 2014 Taylor & Francis 484 B. Morton The Ranellidae (or Ranellinae) with the fossil Ranella olearium Lamarck being recorded widely from Central Europe, and with the family’soriginsinthe Paratethys of the Miocene (97–26 million years ago) (Landau et al. 2009)com- prises a rich assemblage of relatively small predators. Hitherto, however, the only study of any other representative of the family (or subfamily) was by Morton (1990a), who described the feeding biology of Linatella caudata (Gmelin), bearing in mind that this genus too has been placed by some in the Cymatiinae. Notwithstanding, L. caudata was shown to feed, in Hong Kong, upon a variety of sheltered rocky shore species, most notably the arcoid Barbatia virescens (Reeve) followed by the rock oyster Saccostrea cucullata (Born), and then the ascidian Styela plicata Lesuer plus, less favoured, the barnacle Balanus amphitrite Darwin and the turban shell Lunella coronata (Gmelin). Morton (1990a)also showed that L. caudata possesses sulphuric-acid-secreting salivary glands but the predator did not, however, seem to use this acid to access its prey, but rather the radula was used to scrape a hole in either the shell or test and the proboscis was inserted into the penetrated animal. It was concluded that perhaps the acid was used for defence, to externally digest its accessed prey or, possibly, to attack less accessible prey. Gyrineum natator (Röding) is distributed widely throughout the Indo-West Pacific (Henning and Hemmen 1993). It has been recorded from the Seto Inland Sea in the north (Inaba 1982) south to Omishimi Island, Yamaguchi Prefecture, southern Japan, (Beu 1999), south to the Yellow Sea, the East China Sea, Taiwan Strait, South China Sea, Vietnam, Malaysia, Singapore, Brunei, Sunda Strait (Indonesia) and the Andaman Sea. In the Indian Ocean it occurs as far west as the Arabian Gulf and all down the East African coast as far as Beira, Mozambique. It is also distributed well into the Pacific Ocean as far east as New Guinea and the Maldives, although it has not been reported from the Philippines and neither New Caledonia nor Australia (Beu 1998), but other species do occur here (Wilson 1993). The exposed rocky shore G. natator appears to be the ecological equivalent of sheltered rocky shore. L. caudata in Hong Kong waters (Morton 1990a). In Hong Kong, G. natator was reported by Taylor (1980), from an analysis of gut contents, to principally eat green algae, although the remains of polychaetes, amphipods, sponges and holothurians (spicules), were also identified – suggesting that these were consumed either with the algae or represented carrion or, possibly, predation behaviour. Similarly, in the Cape d’Aguilar Marine Reserve in Hong Kong, where Downloaded by [University of Cambridge] at 05:05 08 April 2016 the species is common, G. natator was found to be feeding upon, again from an analysis of gut contents, algae, bryozoans and sponges (Taylor and Morton 1996). It was concluded, therefore, that the species is a generalist browser. Such a conclu- sion was also reached for G. natator by Neo et al. (2001), who showed that in Thailand (Phuket), the species fed mainly on algae (47%), sponges (43.5%) and hydroids (31.2%) and occasionally, and possibly, polychaetes and barnacles – as in Hong Kong. The aims of this study were to investigate the method(s) of feeding and consump- tion exhibited by G. natator under conditions of starvation in the laboratory and, thereby, elaborate on the above, field-derived, generalization that the species is an indiscriminate browser of intertidal and shallow subtidal epibionts. And, thereby, also, if possible, set its feeding behaviour, diet and consumption into the overall picture of tonnoidean predation that has been little elaborated. Journal of Natural History 485 Materials and methods Feeding behaviour Permission was given for 14 individuals of G. natator to be collected from the Cape d’Aguilar Marine Reserve and experimented upon. As an initial experiment, the 14 individuals of G. natator were held in aquaria of the Swire Institute of Marine Science of the University of Hong Kong on the shores of the Cape d’Aguilar Marine Reserve, along with individuals of the species that typically occur with it under the smaller and moveable boulders that occupy the shallow sub-tidal waters of Lobster Bay within the reserve (Morton and Harper 1995, Figure 6). Such species commonly included the gastropods Monodonta labio (Linnaeus) and Nerita albicilla Linnaeus, the bivalves Hormomya mutabilis (Gould) and Chama reflexa Reeve, the sea star Coscinasterias acutispina (Stimpson) and the sponge Tethya aurantia (Pallas). The institute’s sea- water supply is untreated so that aquarium-entrained species are held under near- ambient conditions. After 1 month of observations, this experiment was abandoned because none of the species had been consumed by G. natator, and this will not be reported upon further. Field observations, however, recorded that individuals of G. natator were often associated with small, scattered, individuals of the rock oyster Saccostrea mordax Gould that occur in more sheltered mid- to low-tide pools and cryptic habitats also in Lobster Bay. Accordingly, another longer-term, but still trial, experiment was established in which two of the 14 individuals of G. natator of approximately the same shell height, that is 34.6 and 33.6 mm, were held in separate trays of, again, ambient seawater [20°C (± 2°C) and 32‰ salinity] each with 12 rock oysters that had all been carefully removed from the shores outside the marine reserve using a solid scalpel and small hammer so that none of them was damaged. The oysters were also cleaned of any adhering material and organisms with a toothbrush and checked carefully for any sign of shell damage. Twenty-four more cleaned oysters were held under identical conditions as the two experimental aquaria, but without G. natator, as mortality controls. Similarly, two other G. natator individuals were held in separate trays and remained unfed except for what the seawater supply provided. One of these trays was cleaned, as with the experimental conspecific with oysters, whereas the other control was not. One of the two experimental aquaria and one of the two G. natator controls were supplied with unfiltered ambient seawater whereas the second experimental aquarium was supplied with seawater (at the same rate) that had been filtered Downloaded by [University of Cambridge] at 05:05 08 April 2016 through a fibreglass column. The floor and walls of the latter aquarium only (plus one of the controls; see above) were, moreover, cleaned scrupulously every day for 16 weeks when, as will be described, the experiment ended. Hence, the G. natator individual occupying this aquarium (and its control) had nothing to feed on except the oysters, whereas the other individual had oysters plus any sediment or “fouling” organisms that settled out from the ambient seawater and which it could potentially consume.