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Diet, prey narcotization and biochemical composition of salivary glands secretions of the volutid snail Odontocymbiola magellanica
Abstract and Figures
Odontocymbiola magellanica is a neogastropod very common in Patagonian shallow waters. It feeds exclusively on molluscs inhabiting the same benthic community. Field studies showed that prey preferences are live gastropods (54%) and bivalves (46%). When no living prey are available they change their trophic behaviour to carrion or cannibalism. Feeding mechanisms observations showed that prey are not asphyxiated by the snail's foot as suggested before for the Volutidae family; they are narcotized by saliva introduced in a cavity made by the foot where prey are immobilized. Saliva is produced by the salivary (SG) and accessory salivary glands (AG) and has a pH around 10, relaxing prey muscles, which are consumed alive. Secretions from AG and aqueous extracts of SG and AG were mainly composed of proteins and glycoproteins, though SDS-PAGE gels revealed that salivary proteins were richer in higher molecular weight bands. Fractionation of secretions from AG on Bio-Gel P-100 yielded only one peak. SDS-PAGE showed that it consisted of only one band (MW 51.3 kDa). Microanalysis of cations showed a higher concentration of calcium and magnesium in the accessory salivary gland. Hypotheses of function of different glands are given in relation to feeding behaviour and anatomy of O. magellanica.
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... Here, diving is u tilized by artisanal fishermen to catch bivalves and gastropods due to the ongoing ban of dredges and trawls, implemented as a response to the d epletion of bivalve populations since mid-1970 ′ s (Ciocco et al., 2006;Orensanz et al., 2003Orensanz et al., , 2005Orensanz et al., , 2007Soria et al., 2016). The Tehuelche scallop is occasionally preyed upon by these gastropods (Averbuj et al., 2 012;Bigatti et al., 2010aBigatti et al., , 2010b, and artisanal fishermen take a dvantage of its proximity to catch them during fishing operations ( Bigatti et al., 2015;Cumplido, 2016;Orensanz et al., 2007). O. magellanica and B. cochlidium are captured for family consumption and locally commercialized (Cumplido, 2016;Bigatti et al., 2015), but it was only first regulated in 2018. ...
... The east domain has a persistently high biomass of secondary producers due to high rate of larval retention as a result of nutrients from the continental shelf being "trapped in" (Amoroso and Gagliardini, 2010;Amoroso et al., 2011). O. magellanica is a carnivorous predator gastropod (Bigatti et al., 2010a(Bigatti et al., , 2010b) that would benefit from the high production of bivalves in the east domain, such as the scallop Aequipecten tehuelchus (Amoroso, 2012;Ciocco, 1991;Orensanz, 1986) and the clam Leukoma antiqua (Escati-Peñaloza et al., 2010). On the other hand, the high abundance of B. cochlidium in both domains could be related to a greater supply of food throughout the gulf, since this species feeds primarily on carrion and is able to also feed on live bivalves (Averbuj et al., 2012;Pastorino and Simone, 2021). ...
... Regulation through closures in time and space requires information on the distribution of the resource as well as its vulnerability to harvest (Perry et al., 1999), presumably high in species with internal fertilization and embryonic direct development, depositing spherical egg capsules attached to hard substrata (O. magellanica; Bigatti et al., 2010aBigatti et al., , 2010b or to the female shells (B. cochlidium; . ...
Marine gastropods are key items in small-scale fisheries worldwide, generating employment and high economic value in international markets. In North Patagonian Gulfs (Southwestern Atlantic), gastropods are landed as by-catch in bivalve artisanal fisheries, and thus no official statistics are reported. Recently, the first regulation of marine gastropod catches was established based on size at maturity for some edible species. However, additional biological-fishery data are necessary for developing a management plan if a regulated small-scale fishery is to be established. We provide the first preliminary estimation of the harvestable stock and other basic biological parameters of gastropods in the San José Gulf (SJG), a Natural Protected Area in Northern Patagonia. Density assessments are usually carried out using dredges or trawl nets that damage marine substrata, and thus we used data from non-destructive, drifting underwater visual census in transects, integrated with a Geographic Information System. We estimated the biomass, density, CPUE and the harvestable stock of Odontocymbiola magellanica and Buccinanops cochlidium, the main species currently landed in SJG. Visual surveys were conducted in 85,000 m², where both species were present in depths ranging from 5 to 20 m depth. For O. magellanica, the maximum densities were 0.02–0.04 individuals m⁻² with maximum CPUE of 12.8 kg diver⁻¹ 15 min⁻¹ and estimated harvestable biomass of 837.05 kg (S.D. = 189.96), whereas for B. cochlidium densities were 0.32–0.60 individuals m⁻² with maximum CPUE of 9.25 kg diver⁻¹ 15 min⁻¹ and 365.12 kg (S.D. = 81.86) of harvestable biomass. The delayed maturity and reproductive strategies of both species, among other biological parameters, require a precautionary approach. The total exploitable biomass estimated in our work clearly highlights the need for a very selective, small-scale fishery, operating under a well enforced management plan regulating their capture to ensure its sustainability in a Natural Protected Area.
... Marine gastropods show great diversity of diets (Bigatti, Sacristán, Rodríguez, Stortz, & Penchaszadeh, 2010) and exert a strong influence on the structure of marine ecosystems through their foraging activities (Anderson & Underwood, 1997). Predator species, for instance, may reduce the abundance of dominant species and raise the local diversity by favoring poorly competing species (Kelaher, Levinton, & Hoch, 2003;Paine, 1966). ...
... Omnivory can also be advantageous to gastropods in development. Curtis and Hurd (1979) among marine gastropods (Bigatti et al., 2010;Cyrus & Peters, 2014). ...
... For instance, cannibalism was observed in 4.7% of individuals present in aggregations of the volutid snail Odomtocymbiola magelanica (Bigatti et al., 2010), a similar frequency as in our study. Cannibalism is usually related to food shortage; however, the presence of conspecific shells in stomachs of individuals of O. minuta was higher in months in which the total number of food items recorded was also high (May and August at Araçá, and February and November at Barequeçaba). ...
Marine gastropods exert a strong influence on the structure of marine ecosystems through their foraging activities, yet little is known about how environmental differences in space and time may affect their feeding behavior. To enhance the knowledge about the trophic ecology of coastal benthic species, we investigated temporal and spatial variations in the diet of the sandy beach gastropod Olivella minuta. We collected individuals of O. minuta seasonally, over one year, at two sandy beaches with different morphodynamic characteristics (Araçá Bay, an ultra-dissipative tidal flat, and Barequeçaba Beach, a dissipative beach) and analyzed the stomach contents of specimens of O. minuta. We identified ~15,000 food items, which we grouped into 14 categories. Thirteen food categories were found at each area, but significant differences in diet were observed between sites and sampling periods. Individuals from Araçá consumed an overall larger quantity and diversity of food items, which consisted mainly of foraminiferans, polychaetes, and crustaceans. At Barequeçaba, diatoms were the most important item, followed by crustaceans and polychaetes. Temporal variation depended on sites: the number of food items in the stomachs of individuals of O. minuta and dietary composition was roughly constant over time at Araçá, whereas larger variations were observed at Barequeçaba. Although O. minuta has been previously characterized as a carnivore/scavenger, our results show that the diet of this species varies in space and time and comprises a large variety of food resources. The species thus plays a role in the cycling of both vegetal and animal organic matter. This generalist behavior may allow individuals to shift their diet according to habitat alterations and food availability, thereby enhancing the persistence and resilience of O. minuta in different environments or future climate change scenarios.
... The conoidean venom gland derives from the glandular mid-oesophagus merged with the oesophageal gland, and in addition to it, all Conus species possess SG, and some predominantly vermivorous species have a large ASG. Whereas both SG and ASG have been shown to produce bioactive compounds in non-conoidean neogastropods (Bigatti et al. 2010;Bose et al. 2017;Gerdol et al. 2018;Kuznetsova et al. 2022;Modica et al. 2015;West et al. 1994), their role in cone snails has been continuously neglected. One exception is the study on Conus pulicarius (Biggs et al. 2008), which revealed SG-specific expression of two alpha-conotoxin-like precursors. ...
... The transcriptomes of the quickly emptied VG and ASG are dominated by neuropeptides (conotoxins, other conopeptides targeted to neuronal circuits, including neuropeptide F), whereas SG mostly produces peptides with proteolytic activity. It is therefore likely that VG and ASG are primarily involved in the envenomation (Bigatti et al. 2010;West et al. 1994), whereas the main function of SG may be different, and the most obvious one is the pre-digestion of the prey once it is engulfed in the rostrum. It, however, does not explain the presence of putative neuropeptides L-superfamily conotoxins and multi-ShKT-like precursors in the SG. ...
Venomous marine gastropods of the family Conidae are among the most diversified predators in marine realm—in large due to their complex venoms. Besides being a valuable source of bioactive neuropeptides conotoxins, cone-snails venoms are an excellent model for molecular evolution studies, addressing origin of key innovations. However, these studies are handicapped by scarce current knowledge on the tissues involved in venom production, as it is generally assumed the sole prerogative of the venom gland (VG). The role of other secretory glands that are present in all Conus species (salivary gland, SG) or only in some species (accessory salivary gland, ASG) remains poorly understood. Here, for the first time, we carry out a detailed analysis of the VG, SG, and ASG transcriptomes in the vermivorous Conus virgo. We detect multiple transcripts clusters in both the SG and ASG, whose annotations imply venom-related functions. Despite the subsets of transcripts highly-expressed in the VG, SG, and ASG being very distinct, SG expresses an L-, and ASG—Cerm08-, and MEFRR- superfamily conotoxins, all previously considered specific for VG. We corroborate our results with the analysis of published SG and VG transcriptomes from unrelated fish-hunting C. geographus, and C. striatus, possibly fish-hunting C. rolani, and worm-hunting Conus quercinus. In spite of low expression levels of conotoxins, some other specific clusters of putative venom-related peptides are present and may be highly expressed in the SG of these species. Further functional studies are necessary to determine the role that these peptides play in envenomation. In the meantime, our results show importance of routine multi-tissue sampling both for accurate interpretation of tissue-specific venom composition in cone-snails, and for better understanding origin and evolution of venom peptides genes.
... The size of the prey-capture apparatus often limits the consumption of prey above and/or below a certain size threshold in many predators, including gastropods (Paine, 1976;ap Rheinallt, 1986;Nilsson & Brönmark, 2000;Chiba & Sato, 2012). Our field observations suggest that the foot of N. arthritica plays an important role in the capture and handling of prey, and similar findings have been reported for other predatory gastropods (Morton, 1985(Morton, , 1986Scolding, Richardson & Luckenbach, 2007;Bigatti et al., 2009Bigatti et al., , 2010Chiba & Sato, 2012). The mean size and standard deviation of both whelk and prey consumed are given for each species. ...
The whelk Neptunea arthritica (Buccinidae) is a common fishery species in Hokkaido, northern Japan. Although ecological information is needed for fisheries management, there is only one paper examining the foraging ecology of this species and it reported that N. arthritica preyed mainly on the invasive mussel Mytilus galloprovincialis. To date, no studies have examined utilization of native prey species by this whelk. Here, we report the findings of a study on the native prey utilization by N. arthritica in an area where M. galloprovincialis is not present. We conducted line transect sampling every month from May 2018 to May 2019 on the western coast of Hakodate Bay, southwestern Hokkaido, Japan. Prey items were composed mostly of gastropods (72%), followed by bivalves (24%) and only a small amount of carrion (<4%). Overlapping spatial distributions were observed among size classes of N. arthritica, while the prey utilization varied with body size. Small individuals (<30 mm in shell height) preyed mainly on the small colloniid gastropod Homalopoma sangarense, while larger individuals (>40 mm) preyed mainly on two tegulid gastropods (Chlorostoma lischkei and Omphalius rusticus) and two venerid bivalves (Protothaca euglypta and Ruditapes philippinarum). There were positive size relationships between whelk body size and prey size for prey categories (Vetigastropoda, Caenogastropoda and Bivalvia) and even for the same prey species (H. sangarense, O. rusticus and P. euglypta). These results suggest that N. arthritica is a predator of mobile gastropods, especially during its early life stage, in areas without the invasive Mediterranean mussel. It is possible that the foraging strategy of N. arthritica may differ quite markedly between areas with and without the invasive mussel.
... Their salivary glands are divided into two lobes: the anterior secretes mucus and proteins believed to be enzymes for external digestion of prey tissues, whereas the posterior lobe secretes sulphuric acid, a chelating agent to help dissolution of prey calcareous shell and probably a paralysing toxin (Andrews et al. 1999). Conversely, a strongly alkaline saliva with a pH around 10 is produced by the volutid Odontocymbiola magellanica (Bigatti et al. 2010). Toxins can also be secreted by ordinary salivary glands, at least in species lacking accessory salivary glands. ...
The phylum Mollusca is one of the largest and more diversified among metazoan phyla, comprising many thousand species living in ocean, freshwater and terrestrial ecosystems. Mollusc-feeding biology is highly diverse, including omnivorous grazers, herbivores, carnivorous scavengers and predators, and even some parasitic species. Consequently, their digestive system presents many adaptive variations. The digestive tract starting in the mouth consists of the buccal cavity, oesophagus, stomach and intestine ending in the anus. Several types of glands are associated, namely, oral and salivary glands, oesophageal glands, digestive gland and, in some cases, anal glands. The digestive gland is the largest and more important for digestion and nutrient absorption. The digestive system of each of the eight extant molluscan classes is reviewed, highlighting the most recent data available on histological, ultrastructural and functional aspects of tissues and cells involved in nutrient absorption, intracellular and extracellular digestion, with emphasis on glandular tissues.
... BT levels in sediments and in gastropods were positively correlated (r 2 = 0.855; P < 0.05; n = 4), suggesting that xenobiotic accumulation in O. magellanica occurs mainly through contaminated sediments, rather than water or the food chain. This gastropod lives most of the time buried in the substrate and moves to capture live prey on mixed or hard bottoms (Bigatti et al. 2010). According to Berto et al. (2007), desorbed TBT is not the only bioavailable form, and it is important to stress that the absence of TBT in sediments does not necessarily imply safe removal from the system. ...
Butyltins (BTs) were found in sediments and body tissues of the edible gastropod Odontocymbiola magellanica, in which imposex has been recorded since 2000. BTs in sediments ranged from < MDL to 174.8 ng (Sn) g−1 for TBT, < MDL to 19.2 ng (Sn) g−1 for DBT, and < MDL to 71.8 ng (Sn) g−1 for MBT. In body tissues BTs varied from < MDL to 147.1, < MDL to 77.0 and < MDL to 345.3 ng (Sn) g−1 for TBT, DBT and MBT, respectively. BT concentrations were higher in gonads and digestive glands than in the albumen gland and foot (edible). The highest concentrations of BTs in both sediments and gastropods were found in the harbour area, decreasing with distance to the harbour and areas with less maritime traffic. The Biota-Sediment Accumulation Factor (BSAF) in the different organs was between 0.02–0.42, 0.09–0.35 and 0.08–5.25 for TBT, DBT and MBT, respectively. There were positive correlations between concentrations of BTs in sediments and gastropod body tissues, suggesting that xenobiotic accumulation in O. magellanica occurs mainly through contaminated sediments, rather than water or the food chain. Considering current sediment quality guidelines, our results indicate that acute toxic effects would be expected from TBT exposure, which represents a serious environmental threat for the benthic community. Although the levels of BTs found in the foot of this edible gastropod did not exceed the recommended Tolerable Daily Intake in polluted areas, they should be monitored to ensure the safety of seafood consumers. The alternative antifouling biocides Irgarol and Diuron were not detected in sediments.
... The Tehuelche scallop is occasionally preyed upon by the gastropods Adelomelon ancilla (Zabala et al., 2013), Odontocymbiola magellanica (Bigatti et al., 2010), and Buccinanops cochlidium (Averbuj et al., 2012), the octopus Enteroctopus megalocyathus (Ré et al., 2009), the seastar (Cosmasterias lurida) (Ciocco and Orensanz, 2002), and the ratfish (Callorhynchus callorhynchus) (Di Giácomo et al., 1994). ...
Two pectinid species are commercially exploited in the southwestern Atlantic: the Tehuelche scallop, Aequipecten tehuelchus (d’Orbigny, 1846), and the Patagonian scallop, Zygochlamys patagonica (King, 1832). The fisheries supported by these two species are radically different from each other. The Tehuelche scallop is the target of small inshore fisheries that operate within the northern Patagonian gulfs, involving dredging and commercial diving. In spite of the small volumes landed at present, these fisheries are of considerable significance for the local economies. The Patagonian scallop fishery is an industrial operation conducted by three to four factory trawlers that process the catch at sea. Catches in the order of 50,000 t per year now rank this fishery among the most important scallop fisheries in the world. In this chapter, we review knowledge about these two species, their fisheries and experimental results that may have significance for the development of Tehuelche scallop aquaculture.
Charonia tritonis (Charoniidae), one of the largest marine gastropods and an echinoderm specialist, preys on Crown-of-Thorns starfish (CoTS), a recurring pest that continues to be a leading cause of coral mortality on Indo-Pacific reefs. Widespread historical exploitation has impacted their numbers, with standing populations considered rare throughout their habitat. Their life-stage attributes, i.e., teleplanic larvae, planktotrophic phase spanning years permitting transoceanic dispersal, and recruitment to coral reefs through oceanic influx with intense larval mortality, have likely hindered their recovery. Decline in numbers is hypothesised to account partially for periodic CoTS outbreaks, yet predator-prey dynamics between these two species that might influence this are poorly understood. The C. tritonis excretory secretome elicits a proximity deterrence effect on CoTS, the nature of which is under investigation as a possible tool in CoTS biocontrol scenarios. However, specificity and zone of impact in situ are unknown, and whether the mere presence of C. tritonis and/or predation pressure has any regulatory influence over CoTS populations remains to be established. The fundamental taxonomy and distinctive characteristics, biology and ecology of C. tritonis is summarized, and knowledge gaps relevant to understanding their role within coral reefs identified. Information is provided regarding exploitation of C. tritonis across its habitat, and prospects for conservation interventions, including captive rearing and stock enhancement to repopulate local regions, are discussed. Its predator-prey ecology is also examined and potential to mitigate CoTS considered. Recommendations to direct future research into this predator and for its inclusion in a CoTS integrated pest management strategy to improve coral reef health are offered.
The fast attack by Scaphella junonia on Americoliva sayana was filmed in captivity. Volutidae described in the literature first envelop their prey with the foot, ingesting them in the "foot chamber" thus formed. Scaphella junonia first attack prey in open water, then may use foot to move them around. [Published on 2018-08-28 in the "Fast Track" section of the Bulletin of Marine Science online.]
A new deep-sea species of Volutidae in the genus Tractolira is named from material collected by the United States Antarctic Program in and around the Ross Sea, eastern Antarctica, and from one locality in the Subantarctic region. Tractolira delli new species is most similar to T. sparta Dall, 1896, from which it differs in having a relatively wider shell, less prominent spiral sculpture, with narrower threads, and by the absence of strong axial ribs at least on the first three teleoconch whorls. The other Antarctic congener, Tractolira germonae, has a thicker, dark-brown periostracum (instead of a thin, light-yellow one), a proportionally smaller inductura, and lacks surface sculpture.
Adelomelon ancilla, a volutid commonly found in shallow water in northern Patagonia, is a top predator in the benthic communities of this region. This species presents an anemone (Antholoba achates) epibiosis that may protect it from predators. Adelomelon ancilla captures prey by tightly engulfing it with the foot, and ingests them, generally alive, after narcotizing their muscles. A narcotizing substance, produced by the accessory salivary glands, is released through the proboscis into the prey while the latter is tightly enveloped within the foot, allowing for prey narcotization. In this space, water is not abundant and, therefore, the salivary secretion reaches a high concentration, with a pH of around 10. Analysis of prey obtained in situ indicated that A. ancilla mainly consumes bivalves (88.9%), gastropods (9.5%) and, rarely, sea urchins (1.6%). Ingestion of the prey usually occurs while the predator is buried in the substrate, and may last for several hours. The anatomy of the alimentary system and the pH of various organs involved in prey capture and digestion are presented along with a comparison with feeding mechanisms among other species of Volutidae.
