title for learn-about section on whelks & relatives in A SNAIL'S ODYSSEY
  Foods, feeding, & growth
 

Whelks living in intertidal or shallow subtidal regions feed on various hard-shelled prey, mostly mussels and barnacles.  Olive shells in sand habitats have more diverse feeding modes and diets.  Cone shells are unique in their injection of modified radular cusps along with potent toxins into prey molluscs, polychaetes, and even fishes.

Topics in this secion include radular drilling, considered here, and
GROWTH & MATURATION,
CALIFORNIA CONE SHELLS: CUSPS USED AS HARPOONS,
USE OF SHELL SPINES IN FEEDING,
FACTORS IN DIET SELECTION,
DIETS
, and
HATCHLINGS AS PREDATORS considered in other sections.

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  Radular drilling
 

As most information on the mechanism of boring in whelks is known from research on east-coast and European species, a short introduction is included here before moving on to drilling by west-coast whelks, each in its own subsection.

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Introduction to drilling

 
Research study 1
 

drawing of whelk showing location and structure of the accessory boring organIn whelks such as Nucella lamellosa the mouth and radula are sited at the end of an extensible proboscis.  When drilling, the proboscis tip is applied to the shell of the prey, with an adhesive secretion sometimes released to help hold it in place, and drilling commences.  The drilling is a combination of radular scraping and secretion of shell-drawing of radula of whelk creating drill-hole in the shell of a molluscdissolving chemicals from a special glandular area on the mid-ventral front part of the foot known as the accessory-boring organ (ABO, see drawing on Left).  The radula scrapes in a defined pattern for a few minutes and the snail periodically adjusts its position relative to the drill hole (see drawing on Right).  Interspersed with the scraping is insertion of the ABO into the drill-hole, which occupies a longer time than the scraping part of the drilling.  The ABO is protruded by hemocoelic pressure from its recessed position in the foot into the borehole. The chemical nature of the secretion is not fully known, but hydrochloric acid, chelating agents, carbonic anhydrase, and other enzymes have been identified.  When completed, the borehole mirrors the size and shape of the ABO.  Carriker 1961 Am Zool 1: 263; for review see Carriker & Gruber 1999 J Shellf Res 18: 579.Photograph of Nucella lamellosa courtesy Linda Schroeder, Pacific Northwest Shell Club, Seattle, Washington PNWSC.

photograph of shell bits in the stomach of a muricid snail after drilling through a mussel shellMuch of the rasped off fragments of shell pass into the stomach and are enclosed in mucous wrappings (see photograph of the shell crystals on Right).  From the stomach the pellets pass through the intestine and are defecated.  The wrappings not only smooth the passage of the fragments through the intestine and anus, but also minimise their digestion in the acidic juices of the stomach.  This may be an energy-savings strategy so as not to waste digestive acids.  However, no one knows how much, if any, of dissolved calcium the snail may absorb for its own use.  However, calculations of shell matter swallowed by eastern oyster-drills Urosalpinx cinerea boring into mussels Mytilus edulis suggest that the amount of shell matter swallowed amounts to only about 14% of the shell in the borehole.  Once the hole is made, the proboscis is inserted and small quantities of saliva are released from the mouth. The proboscis is highly extinsible and the radula can reach to all the prey’s internal organs. Digestive enzymes are released to aid in the digestive process, and the resultantslurry is pumped into the stomach by the muscular proboscis. Carriker 1977 Biol Bull 152: 325.

illustration of whelk with its proboscis inserted into a prey mussel showing the extensibility of the feeding organ
Whelks Kelletia kelletii, separated from prey shrimp and fish by a plastic screen with holes, are able to stretch their probosces the entire distance to the prey

NOTE an enzyme that catalyses the dissociation of calcium carbonate into carbon dioxide,
water, and calcium oxide, the last being highly soluble in water

NOTE  the saliva may contain muscle relaxants or other toxins.  These have not yet been demonstrated in west-coast Nucella spp., but are inferred from work on related species.  In the European N. lapillus salivary extracts have been tested on isolated heart muscle of Mytillus edulis.  No effect is noted for the main or acinous salivary secretion, but the accessory or tubular salivary secretions produce marked relaxation of the heart muscle.  On the basis of their experiments the authors propose that salivary secretions could induce flaccid paralysis in the prey. The authors note that theirs is the first experimental proof of pharmacological activity the accessory salivary glands of any neogastropod.  Andrews et al. 1991 J Mollus Stud 57: 136. Additionally, aqueous extracts of salivary glands of south Atlantic/Gulf of Mexico-inhabiting Thais haemastoma are toxic to mice, and have hypertensive and tachycardial effects on other small mammals.  Huang & Mir 1971 J Pharm Sci 60: 1842.

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photograph of 2 whelks Kelletia kelletii with probosces extended

CLICK HERE to see a video of the same whelks Kelletia kelletii as shown above, extending probosces to seek out a dead prawn and fish. The video dramatically shows the extensibility of the proboscis.

NOTE video replays automatically

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Drilling by west-coast whelks

 
Research study 1
 

drawing of whelk Acanthinucella punctulata from below drilling a prey littorine Littorina scutulataphotograph of whelk Acanthinucella punctulata courtesy Gary McDonaldOn Santa Cruz Island, California the whelk Acanthinucella (Acanthina) punctulata preferentially eats littorines Littorina scutulata and L. planaxis.  It does so by drilling in a specific location on the columella. This location is directly over the place of attachment of the columella muscle to the shell, which happens to be the thickest portion of the prey’s shell.  Selection of this site has the double advantage of preventing the prey from escaping, as the predator’s foot is against the aperture of the prey, and weakening the site where the prey’s body is attached to its shell perhaps through injection of a toxin. An average-sized Acanthinucella takes about 14h to drill and 14h to eat a littorine in the field.  Other prey species of the whelk at Santa Cruz Island are barnacles Balanus and Chthamalus, but neither is a preferred prey. Menge 1974 Oecologia 17: 293. Photograph courtesy Gary McDonald, Santa Cruz, CA and Calphotos.

 
Research study 2
 

drawing showing disposition of boreholes by whelks Nucella lamellosa into the shell valves of mussels Mytilus trossulusdrawing of mussel with internal organs shown and with 330 boreholes made by whelks superimposed

 

 

 

 

 

 

 

 

 

 

Studies at the Bamfield Marine Sciences Centre, British Columbia on the disposition of 330 boreholes by whelks Nucella lamellosa on the valves of bay mussels Mytilus trossulus show the following: 1) a statistically non-random distribution of boreholes along and above the hump or “shoulder” of the valve (see figure on Left), 2) a lack of correlation of position with the thinnest parts of the shell, 3) a tendency for the holes to cluster over the heart, digestive gland, and stomach (see figure on Right), and 4) a possible avoidance of the adductor, or shell-closing, muscles.

Does the borehole distribution indicate a compromise between selection of a moderately thin drilling site to gain ready access to “meaty” organs, but to avoid harming the shell-closing muscles, thus denying, or delaying, access by scavengers? It would be nice if this were so, but there are other factors to consider.  The first is the long, prehensile proboscis that would seem to preclude the necessity for any careful positioning by the snail in order to gain access to all organs. Second, bivalve-boring whelks generally avoid the edges of the shells because the shell movements tend to disrupt firm attachment by the foot.  Finally, the boreholes are in the uppermost area of the shell which, through normal close-packing habit of the mussels, would likely be the region first encounted by a wandering snail.  So, is there a strategy here, or just happenstance?  Carefoot 1977 Pacific Seashores Univ Wash Press, Seattle.

 
Research study 3
 

Whelks Nucella spp. employ different methods of feeding depending upon the prey.  Acorn barnacles are drilled between the paired tergal plates or between the paired scutal plates, but not between a tergal and scutal plate.  Sometimes the plates are prised open without whelk Nucella lamellosa in the act of drilling a prey mussel Mytilus californianusdrilling.  Goose barnacles photograph of whelk Nucella ostrina positioned (ready to feed?) on the outer plates of a thatched barnacle Semibalanus cariosusPollicipes polymerus are drilled laterally between the rostral and scutal plates.  Limpets are eaten without drilling, or are drilled at the margin of the shell to form a nick through which the proboscis is inserted. West 1986 Ecology 67: 798.

Close view of N. lamellosa drilling a mussel shell M. californianus 5X. The snail
is facing to the Right

Nucella ostrina positioned
on a barnacle Semibalanus cariosus, possibly seeking a
good spot on which to drill 3X

 
Research study 4
 

All west-coast species of Nucella readily bore into and eat barnacles Balanus glandula.  In a comprehensive study of bore-hole site-preferences of these species in relation to geographic location, wave exposure, and age, researchers at the Bamfield Marine Sciences Centre, British Columbia find some unexpected results.  First, there is no significant geographic1 variation (over a range of 3000km) in drill-hole preferences by Nucella spp.  Second, there is no significant effect of wave exposure on drill-hole preferences.  Finally, there is no significant learning with age as to where to drill. 

schematic showing borehole disposition on prey barnacles Balanus glandula by small-sized whelks Nucella ostrinaschematic showing disposition of boreholes on prey barnacles Balanus glandula by large-sized whelks Nucella ostrinaThere is, however, a strong ontogenetic or age-based shift in location-preference for drill holes in all 4 species.  This is shown graphically for N. ostrina where small snails of 4-8mm shell length drill apparently randomly into all parietal2 and opercular plates of their barnacle prey, and show no preference for suture lines between plates (see figure on Left).  In contrast, large snails of greater than 15mm shell length largely restrict their attacks to the opercular region, and additionally show a strong preference for the margins of the scutal plates (see figure on Right).  This area, because it is the scutal and tergal plates that open to allow feeding, gas exchange, and so on, allows quickest and probably easiest access to the barnacle within. The authors discount learning as a possible explanation for the different preferences between young and old N. ostrina because individuals fed on mussels during their juvenile3 life, then shifted to barnacles, have attack patterns similar to ones fed all their lives on barnacles.  This suggests a genetic basis for the different behaviours.  One interspecific difference noted by the authors for large-sized whelks is that, unlike N. ostrina, which prefers suture-line attacks on the opercular plates, the other 3 species N. lamellosa, N. canaliculata, and N. lima  (the last from Torch Bay, Alaska) prefer to drill through the opercular plates. 

graph showing thicknesses of various shell plates in barnacles Balanus glandula with increasing size of bodyWhat explains this strong preference for the opercular-plate region over the parietal-plate region by large whelks4?  As shown in the graph lower Left, there is a differential change in morphology of Balanus glandula with size.  The opercular plates, most notably the scutal plates, increase in thickness with overall body size less rapidly than do the carinal/carinal-lateral plates of the parietal region.  Thus, small whelks may be less selective in their choice of drill sites because plate thicknesses do not differ as much in small barnacles as they do in large ones.  In comparison, large whelks may save time and energy by attacking the opercular plates, especially at the sutures, not just because less drilling is required, but because injection of toxin from the proboscis will cause the opercular plates to gape.  Small whelks could use a similar opercular plate-drilling strategy, but may end up being more vulnerable themselves to predators, such as snail-eating perches, in such an exposed location.  Hart & Palmer 1987 J Exp Mar Biol Ecol 107: 101.

NOTE1  collections as far south as Santa Barbara likely included an intermixed sampling of both N. ostrina and N. emarginata



NOTE2  there are 6 parietal and 4 opercular plates in B. glandula.  The parietal plates include 2 lateral, 2 carinolateral, one rostral, and one carinal.  The opercular plates include 2 scutal and 2 tergal (see schematic in upper Left figure)

NOTE3  with only a few exceptions the authors used snails reared from egg capsules in their experiments

NOTE4 more on drilling of barnacles by whelks can be found at: LEARN ABOUT ACORN BARNACLES: PREDATORS & DEFENSES: WHELKS

 
Research study 4.1
 

photograph of accessory boring organ of whelk Nucella lamellosaschematic model of dissolution of shell of a mussel when bored by a whelkDrilling by whelks Nucella combines the secretion of an acidic substance from the accessory boring organ (ABO) to break down the shell material with the rasping action of the radula to remove the loosened material.  The ABO consists of a cap on a short stalk, both containing an hemolymph-filled sinus (see photograph).  When in use it is everted onto the surface being drilled by hydrostatic pressure and withdrawn after by longitudinal muscles in the stalk.  Researchers at York University, Toronto have proposed a method of acid secretion in whelks N. lamellosa.  The cap (0.8mm dia) is comprised of a layer of tall, mitochondria-rich epithelial cells which terminate in a distinct brush border (microvilli) of about 250um height.  Within the microvilli of the brush border is present an enzyme known as vacuolar-type proton-transporting ATPase (V-ATPase).   Transformation of ATP into ADP in the mitochondria of the microvilli produce protons (H+ ions) that, along with Cl- ions,  are extruded into the borehole by V-ATPase pumps in the microvilli powered by energy released from ATP breakdown.  The protons and chloride ions form hydrochloric acid of about pH 4, sufficient to break down the CaCO3 component of the shell into calcium ions and carbonic acid (HCO3-), the latter ultimately transforming into bicarbonate, water, and carbon dioxide (see schematic model on Right).  The residual organic protein matrix of the shell is acted upon by other enzymes secreted by the ABO.  Rasping action of the radula cleans out the residue and the cycle is repeated.  Clelland & Saleuddin 2000 Biol Bull 198: 272.

 
Research study 5
 

photographs of boreholes made by whelks Nucella lamellosa in shells of mussels Mytilus trossulus courtesy Kowalewski 2004 J Moll Stud 70: 359Laboratory observations on Nucella lamellosa feeding on mussels Mytilus trossulus at Friday Harbor Laboratories, Washington indicate that 12% of successful attacks are made without drilling completely through the shell, with about one-third of these exhibiting an incomplete drill hole. Two examples of incomplete drill holes are shown in the photographs. Presumably, toxins are able to penetrate via the incomplete holes and cause the mussel to gape.

schematic showing borehole dispositions on a shell rendition of a mussel Mytilus trossulusOther results show that drill-hole dimensions correlate with predator size, but not with size and thickness of prey shell. Similar to what has been found in other studies, the positioning of boreholes on the mussel shells suggests no site-selective behaviour by the whelks.  Finally, drill holes made by the same whelk in different mussel shells vary considerably in outline shape (circular and elliptical), but almost all are cylindrical in cross-section.  This means that there is no way to identify an individual snail from its drill-hole morphology.  The major contribution of the study, from a non-paleontological point of view, seems to be that partially completed drill holes may not necessarily signify failed attacks.  Kowalewski 2004 J Moll Stud 70: 359.

NOTE instead of using an actual shell shape to depict these positionings, the author uses shape coordinates (Bookstein) relative to 4 "pseudolandmarks". These coordinate marks have been removed from the above depiction for clarity. The author provides dotted lines to deliniate the actual shell shape



Boreholes in mussel shells Mytilus trossulus
indicating one complete and 2 incomplete holes

 
Research study 6
 

graph showing successful and failed attacks by whelks on mussels when a crab predator of the whelk is presentphotographs of an incompletely drilled mussel shell Mytilus trossulusDrilling by whelks can be influenced by a variety of environmental factors, including temperature, salinity, and so on, but one factor not previously examined is the presence of a predator of the whelk.  This is investigated at Friday Harbor Laboratories, Washington for Nucella lamellosa feeding on mussels Mytilus trossulus in the presence of an upstream, screened-off crab Cancer gracilis.  The main effect of the crab’s presence is a greater frequency of whelks abandoning their prey  (89%, as compared with 43% when the crab is absent, see graph and photographs of an abandoned, partially drilled, mussel). An equally interesting observation is that in the presence of the crab the decision by the whelk to abandon its efforts or to continue drilling appears to be be influenced by how much time it has already invested and the size of the prey barnacle.  The data supporting these ideas are not fully convincing, however, and one hopes that we will hear more from the authors on this interesting subject.   Chattopadhyay & Baumiller 2007 J Exp Mar Biol Ecol 352: 257.

NOTE  the crab is accompanied by the remains of crushed N. lamellosa, which actually adds a second factor to the experiment, but which doesn’t affect the authors’ conclusion in any way

 
Research study 7
 

photographs of a borehole in a mussel Mytilus trossulus caused by a whelk Nucella lamellosaA recent study using scanning electron-microscopical (SEM) techniques shows that whelk bore-holes bear readily identifiable micro-rasping marks left by repeated passes of the radula.  The researchers compare contemporary drill-holes made by whelks Nucella spp. in freshly collected mussels and limpets in San Juan Island, Washington with holes in dead shells from the same location and in fossilised Miocene bivalves collected from sites in Europe.  The researchers find similar patterns in holes in all shells.  The results indicate the usefulness of SEM imaging for identifying predatory drill-holes in both contemporary and fossil specimens, and providing the means to  distinguish them from non-predatory holes.  Schiffbauer et al. 2008 Palaios 23: 810.

NOTE  whelks studied in laboratory feeding experiments include Nucella ostrina at the Friday Harbor Laboratories, Washington and N. lamellosa used by another researcher in an earlier study.  Live prey molluscs include mussels Mytilus trossulus and limpets Lottia spp.  Fossil bivalve shells are dated at around 14-17mya

 
Research study 7.1
 

graph showing relationship between "excavation" rate of drill holes by whelks Nucella lamellosa feeding on mussels Mytilus trossulusResearchers at Friday Harbor Laboratories, Washington provide data on feeding rates and feeding cost-benefits for whelks Nucella lamellosa eating mussels Mytilus trossulus.  By separating feeding into 3 activities that they term drilling, excavation, and consumption, however, the authors have needlessly confounded the issue.  As they seem to be one and the same, how can drilling be differentiated from excavating?  Thus, the summary comments that rate of drilling is “independent of predator size” and that rate of excavation is “proportional to the size of the driller” make no sense.  Nor does a linear plot of excavation rate against size of snail help in our understanding (see graph).  Based on our knowledge of scaling phenomena in living systems, this relationship is unlikely to be linear; rather, because of  the relationship between surface area/volume and metabolism, the factors of "excavation" rate and body size would be expected to scale allometrically with a negative slope.  One would not predict a straight-line relationship on an arithmetic plot. There is a need for further work on this subject. Chattopadhyah & Baumiller 2009 J Shellf Res 28 (4): 883.

NOTE  when yoiu create a hole in a piece of wood with a drill and bit, the amount of wood excavated is equal to the diameter and depth of the hole. Drilling volume equals excavation volume

 
Research study 8
 

Feeding and other behaviours in whelks Nucella lamellosa may be interrupted periodically air-exposure during low tide and the question arises as to which is the greater stress, being deprived of food or being deprived of water?  One anticipates that this question would be best answered by histogram comparing barnacle consumption by whelks Nucella lamellosa under different conditions of air-exposuresome sort of energetics measurements, but a researcher at Friday Harbor Laboratories, Washington investigates1 it somewhat differently. Five treatments over a 25d period are employed in which, daily, snails are: 1) air-exposed on the laboratory bench with no barnacle food for 5h (AIR-EXPOSED NO FOOD), 2) air-exposed on rocks with barnacle food for 5h (AIR-EXPOSED WITH FOOD),  3) immersed but their rocks with barnacle food are air-exposed for 5h (IMMERSED NO FOOD), 4) continuously immersed with food (CONTROL), and 5) continuously immersed but lifted from their rocks/barnacles briefly then immediately replaced (HANDLING CONTROL).  At the end of the experiment the total number of barnacles consumed by each individual snail over the 25d period is assessed2.  Results show that consumption is significantly less for snails exposed to air with no food than for snails kept immersed also with no food, and both “stressed” sets of snails eat significantly fewer barnacles than do the 2 control sets.  Although the results should be considered only tentative owing to lack of “parallelism3” in the treatments, the conclusion of the author is that daily episodes of emersion are more stressful than daily episodes of limiting food.  Price 2012 Am Malacological Bull 30 (2): 255.

photograph of whelk Nucella lamellose drilling a barnacle Semibalanus cariosus
NOTE1
  the study is part of a course offered at the Laboratories, and iis a fine, presumably “first-effort”, publication by the student involved

NOTE2  a separate control experiment of barnacles without snails enables a correction to be made of barnacle deaths from unrelated causes

NOTE3  for example, the significantly fewer barnacles eaten by air-exposed snails separated from their rocks and placed on the laboratory bench could have resulted, at least in part, by them withdrawing into their shells (this is not mentioned by the author), by extra desiccation from being separated from their (moist) rocks, and by the time required by them to re-position themselves on their barnacle food when replaced on their rocks underwater.  This last is discussed by the author


Nucella lamellosa eats a barnacle Semibalanus cariosus

 
Research study 9
 

Paleoecologists interested in fossil bivalve and other shells bearing boreholes are continually on the lookout for better means to identify the gastropod predators involved.  Size of borehole and secondary features such as countersinking have been helpful clues, as have microstructural traces on the borehole left by radular scraping.  In a recent study on the subject, researchers at Friday Harbor Laboratories, Washington use Environmental Scanning Electron Microscopy techniques to examine microtraces left within boreholes made by whelks Nucella lamellosa in shells of mussels Mytilus trossulus.  Additionally, they use dried radulae mounted on a small handle to scratch across wax surfaces and analyse these.  Results show that while microtrace fidelity varies considerably within and across individuals, the microtraces can provide “reasonable cross-section of mussel shell Mytilus trossulus showing layersapproximations” of radula dentition size and morphology. This is apparently not finely resolved enough, however, to provide good correlation with radula size, and thus the microtraces cannot presently be used as a proxy for size of predator or to differentiate one species of predator from another.  The authors pose an interesting follow-up research question: what protects the radula from being dissolved or chelated by its own accessory boring-organ secretions.  Tyler & Schiffbauer 2012 Palaios 27 (9): 658.

NOTE  this is basically a scanning-electron microscope for photographing specimens that are uncoated and/or “wet” (i.e., alive)

NOTE  high variabililty in microtrace morphology is attributed to 1) angle of attack and radular pressure, 2) shell hardness relative to radula hardness, and 3) duration of application of accessory boring organ, depth of penetration of its secretions, and solubility of the shell material

Section through mussel shell showing outer periostracum
(mainly protein), thicker prismatic layer (calcite, softer),
and inner nacreous layer (aragonite, harder)

 
photograph of radula of whelk Nucella lamellosa radula of whelk Nucella lamellosa mounted on a handle Tyler&Schiffbauer2012Fig3 close view of radula scratch marks in wax with measurements
Radula of Nucella lamellosa.The 3 main rows are used primarily for drilling Radula of N. lamellosa mounted on a probe tip ready for scratching wax Scratch marks of radula on a piece of wax. On a shell these would be the microtraces Close view of centrre cusp-mark scratch with measurements to compare with below L
close view of central cusp in radula of whelk Nucella lamellosa photograph of borehole in a mussel Mytilus trossulus photograph of radula scratch marks on a whelk's borehole in a mussel shell Mytilus trossulus photograph of borehole wall showing cross-cutting microtraces
Centre cusp that created scratch in above R. Note the 10.31um width in both photos Borehole in mussel shell created by whelk Nucella lamellosa Radula rasp-marks (microtraces) on wall of borehole Cross-cutting microtraces on borehole wall indicating different attack angles of radula
 
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