Shells of drilled prey were void of soft tissue upon recovery from aquaria; only one individual was documented as partially consumed with the remaining residue left to decay. Although his comments are based on only 11 observations, he cited high anaerobic capacities of the Lucinidae (e.g. To test the hypothesis that suffocation is more common at shallower sediment depths due to prolonged prey carrying, it is essential that prey used in laboratory experiments are healthy. Huelsken et al., 2008) and may not respond in the same way if exposed to varying sediment levels in laboratory settings. Although some authors have attributed undamaged shells to naticid predation in field settings (e.g. Bulletin of the American Malacological Union, How to buy clam seed… without getting shucked, Rutgers Cooperative Research & Extension Fact Sheet FS452, The trophic ecology of Lunatia heros and its competitive interactions with Polinices duplicatus, British prosobranch molluscs: their functional anatomy and ecology, Foraging strategies and coevolutionary alternation in the modern naticid gastropod predator-prey system, Bulletin of the Natural History Society of New Brunswick, No. Secondly, dates of entry into aquaria were recorded on all prey as a way to monitor how long individuals remained in experiments; average duration of occupancy in aquaria was quantified. removal from aquaria (Hwang, Chueh & Deng, 1990). Because 75% of clams consumed by drilling were preyed upon within 6 d, most individuals did not survive long enough to merit concerns regarding gradual deterioration of health. C. Two drilled prey from experiments conducted in autumn. The number of alleles per locus ranged from 2 to 20, and the observed and expected heterozygosities varied from 0.276 to 1.000 and from 0.331 to 0.939, respectively. An exception may be suffocation that is aided by toxicity, as drilling is likely more expensive and slower than use of paralysing secretions. to suffocate or to cover thickly, with some substance). Author interpretations are noted as based on observations, shells or both; items marked by an asterisk indicate that laboratory accounts of alternative predation were additionally discussed (see Table 3 for further details). These results seem counterintuitive because larger members of a species have reduced metabolic requirements (Bayne, 1976), though perhaps larger shells take longer to drill and put the individual, especially if it is weak, at greater risk of suffocation. Only three specimens (<1%) were found empty without drillholes. 1983). The Naticidae are a cosmopolitan family of predatory marine gastropods (Kabat, 1990; Kelley & Hansen, 2003). Our literature review also highlights that different causal mechanisms may allow moon snails to feed in the absence of a completed drillhole; research is needed on alternative naticid predation modes that may be a concern for studying predator-prey interactions using drillholes. Can naticid gastropod predators be discriminated by the holes they drill? Orig. Natural selection would be unlikely to favour suffocation if it is slower or more expensive energetically than drilling. VIII, Unexpected rates of cannibalism under competitive conditions by the naticid gastropod Neverita duplicata (Say), Predator-prey relationships of naticid gastropods and their bivalve prey, Palaeogeography, Palaeoclimatology, Palaeoecology, Late Cretaceous gastropod drilling intensities: data from the Maastrichtian Fox Hills Formation, Western Interior Seaway, USA, The Naticidae (Mollusca: Gastropoda) of Giglio Island (Tuscany, Italy): Shell characters, live animals, and a molecular analysis of egg masses, Tetrodotoxin secretion from the lined moon shell, Neurotoxin tetrodotoxin as attractant for toxic snails, Predatory ecology of naticids gastropods with a review of shell boring predation, Evidence from the fossil record of an antipredatory exaptation: conchiolin layers in corbulid bivalves, Evolutionary trends within bivalve prey of Chesapeake Group naticid gastropods, The effect of predation intensity on rate of evolution of five Miocene bivalves. The other two nondrilled clams lacked signs of decay and may have been suffocated. Such suffocation has sometimes been referred to as ‘smothering’. This marine species is found in the Yellow Sea or off the coast of the Madagascar, Mozambique and South Africa of the Indian Ocean. (2002) A compendium of fossil marine animal genera, Bulletins of American Paleontology 363, 1-560: Martin G. C. (1904) Gastropoda, Maryland Geological Survey Miocene Text, 131 … Surface observations were noted at this midpoint between 6 d experimental checks, but moon snails within the substrate were not disturbed if possible. Documentation of suffocation in bivalves capable of tightly closing their margin is restricted usually to laboratory observations. For example, Edwards (1969) noted that, of 21 Olivella biplicata consumed in laboratory experiments, only 19% were completely drilled; 67% had incomplete drillholes and 14% remained undrilled. Ansell & Morton, 1987). The third clam showed no indication of decay afterward or weakness, yet was discovered in the 20-cm setup within the substrate and completely empty at the next experimental check. Because suffocation is not easily observed, empty shells that lack completed boreholes typically serve as evidence that suffocation has occurred (and specimens covered in mucus at least are suggestive of handling by naticids; e.g. Control specimens free of mucus burrowed rapidly (perhaps a flight response), whereas prey with apertures plugged by mucus remained stationary and retracted for several hours. We recognize, however, that other prey species may be more susceptible to suffocation. Predator-prey size ratios for these species are appropriate based on the work of Kitchell et al. Several authors have noted that only larger prey were suffocated in their experiments (e.g. Our experiments indicate a lack of deaths by suffocation in Neverita duplicata consuming Mercenaria mercenaria. duplicata drilling on the surface of the sand in a 1-cm setup. (1) Tank space and substrate depths should be considered with respect to predator and prey sizes, life habits, and any attack, burrowing or escape behaviours. These examples do not include unpublished MSc or PhD work, abstracts, books, comments or replies to articles, or personal communication citations in publications. To our knowledge, smothering, as an attack behaviour executed by gastropods, was used first by Morton (1958) to describe predation by members of the Cassididae, Harpidae, Olividae, Tonnidae and Volutidae. drilling time-prey shell thickness relationships are predictable), instead of those in which outcomes are less certain (e.g. 408, Revision on the classification of Recent Naticidae, Third Report on Investigations of Methods of Improving the Shellfish Resources of Massachusetts. Each experimental setup contained only a single predator and six prey, which were replaced every 6 d as consumed. Removal of mucus yielded an active response from U. vestiarium within 30 min, however, indicating that any numbing effect was not permanent. Alternative modes of naticid predation reported in the literature based on field investigations. Understanding alternative modes of predation by naticids requires enhanced collaboration among malacologists, ecologists, physiologists, biochemists and palaeontologists. First, strength of valve closure was tested before placing prey in experimental setups as well as during experimental checks by trying to insert a fingernail in the ventral margin. In addition, prior to use in experiments, Mercenaria mercenaria had access to food in flow-through holding tanks. EAR-0755109). Neverita lewisii lives in the Eastern Pacific, from British Columbia to northern Baja California, Mexico. Presence of multiple predators could be a factor influencing suffocation in some previous studies (Table 3); decreased incidence of suffocation in our experiments may be related also to the fact that only single predators were utilized in each tank. 3D). Although careful control of laboratory conditions may minimize false reports of suffocation by naticids, in some cases alternative modes of predation may be real. Nondrilling attacks on bivalves with a permanent gape, or by forced entry through the aperture of gastropods, are not usually considered by palaeontologists to represent deaths by smothering, due to the availability of direct access for feeding. Studies of drilling predation often consider the antipredatory role of morphological traits such as shell thickness, sculpture and tightness of valve closure (e.g. Massachusetts Division of Marine Fisheries, WHOI Collection Reprints 1951, No. Because the capacity to endure lower oxygen concentrations is most often inversely correlated with metabolic rate (Christensen, 1970), taxa with faster metabolisms may be more prone to suffocation. In contrast, species able to remain sealed for very long periods should be drilled exclusively. Further complicating matters, the etymology of the word ‘smothering’ indicates multiple meanings (e.g. These moon snails were stressed in the absence of sediment and showed no interest in available prey. Wheatley, 1947), others have regarded natural mortality or disease as the destructive agents (e.g. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. 564, Interactions between naticid gastropods (Euspira spp.) However, many bivalves are noted for their capacity to remain closed for long periods, suggesting that such questionable deaths may not be attributable entirely to suffocation; consequently, copious mucus secretions that aid in prey capture and handling are often considered (Ansell & Morton, 1987). ^Available data listed here for prey consumed by alternative means were not divided by prey species by Aronowsky (2003) or by predator species by Grey (2001). Profile of Neverita didyma, commonly known as Ball moon snail. Even in cases of mortality attributed specifically to suffocation by naticids, relatively little is known about the actual cause of death. Aronowsky, 2003) or during stressful warm summer temperatures (e.g. Edible whelk mainly includes Buccinum undatum (Nasution & Roberts, 2004), Busycon carica (Eversole, Anderson, & Isely, 2008), Dicathais orbita (Woodcock & Benkendorff, 2008), Neptunea arthritica cumingi Crosse (Gang et al., 2018, Gang et al., 2019), Neverita didyma (Gang et al., 2019) and Volutharpa ampullaceal (Gang et al., 2018). 2223, Stereotypic and size-selective predation in, The evolution of predator-prey behavior: naticids gastropods and their molluscan prey, Evolution of animal behavior: paleontological and field approaches, Prey selection by naticid gastropods: experimental tests and application to the fossil record, Anomalies in naticid predatory behavior: a critique and experimental observations, Drill hole predation on fossil serpulid polychaetes, with new data from the Pliocene of the Netherlands, Drill holes produced by the predatory gastropod, Yale University Reprographics & Imaging Services, New example of Devonian predatory boreholes and the influence of brachiopod spines on predator success, Inferring predation intensity in the marine fossil record, Trial control of the greater clam drill (, Journal of the Fisheries Research Board of Canada, The marine fauna and flora of Moreton Bay, Queensland, Memoirs of the Queensland Museum – Nature 54, Proceedings of the Thirteenth International Marine Biological Workshop, Brisbane. One specimen, in a 20-cm aquarium, was discovered empty on the sediment surface after only 3 d. The other, in a 2-cm tank, was found on the surface at 3 d but with signs of gaping, perhaps indicating that weakness prevented it from burrowing. 1: 1–65, Studies of the biology of the naticid clam drill, Fisheries Research Board of Canada, Technical Report, Observations on the penetration of tightly closing bivalves by, Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis, Post-Miocene shift in stereotypic naticid predation on confamilial prey from the mid-Atlantic shelf: coevolution with dangerous prey, Reduced competition and altered feeding behavior among marine snails after a mass extinction. We examine the pervasiveness of alternative modes of predation employed by naticids reported in the literature and offer recommendations regarding the terminology used in referring to such mechanisms. Because it is unclear if predatory behaviours such as suffocation are common in natural settings or are mostly artefacts of laboratory conditions such as insufficient substrate, we examined experimentally the influence of different sediment depths on drilling vs suffocation of Mercenaria mercenaria prey by Neverita duplicata. 383, Observations on and attempts to control the greater clam drill (, Fisheries Research Board of Canada Manuscript Reports of the Biological Stations No. The detection rate of BTs ranged from 50% to 100% and several species such as M. arenaria, Meretrix meretrix, Mytilus edulis, Crassostrea gigas, Rapana venosa, Chlamys farreri and Neverita didyma having detection rates of up to 100%, indicating that most of the molluscs are sensitive to accumulation of BTs compounds from the aquatic ecosystem. Three additional clams were recovered completely empty, but without a drillhole (one each in the 2-, 6- and 20-cm aquaria). Although our data indicate that shallower substrates do not impact predation by drilling, we recognize that only a single predator and prey species are examined here. Abbreviations: as in Table 2; SL, sand layer provided but precise depth not given. individuals unable to maintain tight valve closure and/or that did not exhibit normal burrowing behaviour (Flimlin, 2004). [2], https://en.wikipedia.org/w/index.php?title=Neverita_didyma&oldid=992622880, Creative Commons Attribution-ShareAlike License, This page was last edited on 6 December 2020, at 07:18. my weight crept back on and I accepted that 84 kg (185 lbs) was “my” weight. name. The decision to use M. mercenaria as prey was based on several factors. Alternative modes of predation such as suffocation may result from unnatural laboratory environments, and in particular a lack of sufficient sediment for burrowing with captured prey. Future work on other alternative modes of predation by naticids, in both laboratory and field experiments, should focus on validating reported occurrences of such predation and identifying different mechanisms that may be involved. Vermeij (1980) noted, in experiments on bivalves in Guam, that lucinids were always drilled as opposed to other species apparently expiring from suffocation. expected from the optimal diet model (Hughes & Elner 1979, Hughes & Seed 1981, Jubb et al. With over 172,000 shells for sale. Otherwise, decay or scavenging following natural mortality of weak prey could leave empty shells that might be misinterpreted as deaths due to suffocation. B.N. Incomplete drillholes resulted from interruptions in drilling during experimental checks and possibly during water changes. Our study indicated a lack of suffocation by Neverita duplicata on Mercenaria mercenaria; 99% of consumed prey were drilled. In addition, four holes that were complete but not yet sufficiently widened for feeding were subsequently redrilled, as later observations revealed expanded inner diameters. duplicata preying on a M. mercenaria in a 0-cm aquarium. Nightmarishly strong looking animal. These examples highlight the challenges in assessing how undrilled prey perish in the field; concerns regarding prey health are not limited to laboratory experiments in attempting to recognize alternative modes of predation by naticids. Palaeontologists have focused recently on analysing latitudinal trends in drilling by naticids. Taxon names for naticids are updated as per Torigoe & Inaba (2011). Neverita didyma is a commercially important and over-exploited species. to have a positive correlation with boreholes of Neverita didyma, feeding on the bivalve, Ruditapes philippinarum. Part of the confusion concerning the definition of ‘smothering’ in studies of drilling predation is caused by a division in the language used by different disciplines. Although drilling is the dominant predatory behaviour employed by moon snails, nondrilling mechanisms by naticids have been reported in the literature. Similarly, Edwards & Huebner (1977), Fregeau (1991) and Vencile (1997) used prey collected locally in their laboratory experiments, offering control in quality and health, and did not report nondrilling mortality. Alternatively, the naticid may have been able to feed using the former drillhole. This problematic usage extends to descriptions of ‘smothering’ predation by other gastropods. Experiments conducted using prey purchased at fish markets (e.g. Three clams were drilled to completion, but were not consumed due to interruption during an experimental check. Thirdly, every 72 h surface observations were noted for signs of decay or weak clams that had gaped or could not bury themselves in the sand (Flimlin, 2004). ‘Smothering’ is an alternative form of naticid predation usually cited by palaeontologists, whereas ‘suffocation’ is utilized more frequently by biologists (Appendix 1), although Aronowsky (2003) incorporated both words in discussing alternative naticid predation. Alternative modes of naticid predation have been recorded in both field (Table 2) and laboratory (Table 3) settings. To facilitate discussion, we categorize modes of naticid predation (Table 1) first by the primary attack (drilling or nondrilling) and then according to the outcome of each death scenario (preservation of a complete drillhole, incomplete drillhole, or no drillhole, which would affect interpretation of predation in the fossil record). Neverita Didyma or moon shell isolated on black background. Although TTX is found mostly in the muscle or digestive glands of naticids, Natica lineata demonstrated a capacity to release seawater yielding acute paralytic toxicity in response to external stimulation, i.e. The impact of Euspira fortunei as an alien predator on fluctuations in population densities of prey mollusks between 2001 and 2010 on the Tona coast, northern Japan, was investigated. Reid & Gustafson (1989) stated that bivalve prey were limp and unresponsive after being drilled, leading them to investigate pharmacological properties of oesophageal gland secretions of Lunatia lewisii. The mitochondrial genome of the marine gastropod Neverita didyma (Roding, 1798) (Mollusca: Gastropoda) Ốc ngọc lớn, còn gọi là ốc ngọc đi-đi-ma hay ốc mỡ trơn (Neverita didyma), tên tiếng Anh: bladder moon snail/shell hoặc ball/hepatic moon snail, là một loài ốc biển săn mồi, là động vật thân mềm chân bụng sống ở biển trong họ Naticidae (họ Ốc ngọc). Only eight live individuals were removed and consequently replaced during the course of experiments due to health concerns; four or fewer were replaced per trial. Appropriate substrate depths for prey species should be considered as well, especially for any that exhibit escape behaviours such as leaping or are large and have long siphons for deep burrowing within the sediment, as discussed by Bayliss (1986); extrapolation of laboratory observations to field settings may not be appropriate if artificial conditions do not reflect natural habitats. The sediment consisted of fine sand collected from nearby Wrightsville Beach, NC, similar to the natural habitat of Neverita duplicata. 3E). Neverita duplicata typically avoids carrion (Kitchell et al., 1986; Fregeau, 1991), but consumes freshly injured (Edwards & Huebner, 1977) or, albeit rarely, recently killed prey (Fig. The hypothesis that decreasing substrate depths yield increasing deaths by suffocation was tested in a laboratory setting through five treatments: 0 (i.e. Sepkoski, Jr. J. J. Nearly all prey with incomplete drillholes were redrilled successfully regardless of the amount of substrate provided (including the 0-cm setup). A.N. Although we found little evidence for suffocation by Neverita duplicata in our experiments, suffocation may be more common for other naticid species. Ricketts & Calvin (1962) used ‘smothering’ alongside suffocation in the third edition of their book Between Pacific tides. Field reports of alternative predatory behaviours are based mostly on gaping prey or rely on indirect observations, such as incompletely drilled or undamaged shells from experimental plots. More recently, Hasegawa & Sato (2009) used ‘smothering’ to denote merely the encasement of mucus that immobilizes naticid prey for days, even though eventual death is due to drilling and not suffocation, adding further confusion to the meaning of smothering as a predatory behaviour exhibited by moon snails. Kingsley-Smith, Richardson & Seed (2003) did not provide any substrate in aquaria for Euspira pulchella, but this unnatural state did not impact drilling on cardiid prey (contraBayliss, 1986). Neurotoxins have been reported in several naticids from the Indo-Pacific, as a result of research on shellfish poisonings in humans (Hwang et al., 2007). In particular, we focus on predation commonly referred to as ‘suffocation’ by biologists and ‘smothering’ by palaeontologists. Drillholes were evenly distributed among right and left valves in each setup (51.2% R: 48.8% L for all depths combined). Due to shallow depths of the laboratory setup, moon snails were limited in their capacity to attack prey from below as may occur under natural circumstances. E. Gould, M. Grey, M. Newel, G. Bourne, and E. Weissberger graciously shared data from their work. Burrowing through soft substrates, most naticids forage at or below the sediment surface and remain submerged while in pursuit of their prey. Naticid gastropods are often regarded as models of stereotypy in their predatory behaviour (Kitchell, 1986; Kabat, 1990). For instance, any influence from potentially paralysing mucus secretions should not vary predictably with the amount of substrate provided. Although our experiment was not designed specifically to test the effect of prey health on suffocation, it appears that poor prey health may have made these two individuals susceptible to suffocation. Neverita duplicata typically avoids carrion (Kitchell et al., 1986; Fregeau, 1991), but consumes freshly injured (Edwards & Huebner, 1977) or, albeit rarely, recently killed prey (Fig. Marine Fisheries Series No. Naticid drillholes preserved as trace fossils provide a record of ancient predator-prey interactions and are commonly utilized by palaeontologists in studying evolution (e.g. Harries & Schopf, 2007; Kelley & Hansen, 2007), apparently employed this term as a synonym for nondrilling predation by suffocation, although this use was never stated clearly and perhaps led to misinterpretation of the term as a catch-all phrase for any instance of naticid feeding in the absence of drilling. Such commercially important taxa are easier to obtain in large batches for use in experiments and bulk purchases are more likely to include empty shells and individuals weakened by parasites or stressful holding conditions, perhaps leading to more instances of perceived suffocation. The role of ecological interactions in the evolution of naticid gastropods and their molluscan prey, The fossil record of drilling predation on bivalves and gastropods, Predator-prey interactions in the fossil record, Latitudinal patterns in naticid gastropod predation along the east coast of the United States: a modern baseline for interpreting temporal patterns in the fossil record, Sediment-organism interactions: A multifaceted ichnology, Early life history characteristics of the razor clam (, Canadian Technical Report of Fisheries and Aquatic Sciences No. In field settings ( e.g the number of mercenaria prey before, during and after being in... And 37 ppt ; pH ranged between 6.2 and 9.2 M. Grey, M. Newel neverita didyma diet Bourne. Used ‘ smothering ’ means substrates, most naticids forage at or below the (! ; Turner, 1950 ; Edwards, 1974 ) Agersborg ( 1920 ) described suffocation first as an indicator predation! 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