title for learn-about section on whelks & relatives in A SNAIL'S ODYSSEY
  Foods, feeding, & growth
  Topics in this secion include growth & maturation, considered here, and
, and
HATCHLINGS AS PREDATORS considered in other sections.
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Growth, regeneration, & maturation

  Considered here are studies on olive shells Callianax biplicata, dog-whelks Nucella spp., and Amphissa columbiana. There is an additional section below on effects of parasitism on growth & maturation of selected whelks.
Research study 1

photograph of researcher marking an olive shell Callianax biplicata with a dental drillPreliminary observations on field populations of olive shells Callianax biplicata by a researcher at the University of California, Berkeley indicate an absence of size-classes.  To study growth the author undertakes a mark-recapture experiment using a technique of filing a notch into the whorl just above the main body whorl.  Results of the study are not provided.  Stohler 1962 The Veliger 4 (3): 150.

Research study 2

photograph of whelks Nucella lamellosa showing thick- and thin-shelled morphsgraph showing interrelationships of shell growth, food availability, and soft-tissue growth in whelksBenefits to a snail in having a shell are apparent, but what about costs?  The obvious costs are those of manufacturing the shell, including organic matrix and mineralisation, and transporting the shell about.  But what about another cost, not so obvious, that a limit may be set on tissue growth by the maximum rate at which the shell is produced?  This would have important evolutionary implications, not just for whelks, but for any organism with a mineralised skeleton, such as corals and barnacles. A comparison of growth in 2 morphs of the whelk Nucella lamellosa at Friday Harbor Laboratories, Washington shows that both have similar soft-tissue mass and both produce shell material at the same rate but, because 50% more shell material is required for a thick-shelled individual, its rate of tissue growth is actually constrained.  In the schematic representation above Right,which best fits the data obtained in the study, note that neither morph has reached a maximum rate of soft-tissue growth, and neither has reached its maximum rate of food ingestion.  Thus, it appears to be limitation on shell growth that is holding back soft-tissue growth, possibly in both morphs, but certainly most evident in the thick-shelled one.  Palmer 1981 Nature 292: 150.

NOTE the 2 morphs are a thin-shelled, fluted form and a thick-shelled, smooth form

Research study 3

graph showing relationship in neogastropods and other snails between rate of regeneration of shell material and organic content of the shell matrixAs in all molluscs, shell growth in whelks occurs at the free edge of the mantle.  Damage, such as that from non-lethal predator attack as, for example, crabs, can be repaired at the shell edge or anywhere on the inside of the shell that the mantle contacts. Such internal repairs are often indicated by blisters on the nacreous part.  Mollusc shells have 2 components: an organic protein matrix that is surrounded and perfused by crystalline calcium carbonate.  Studies at the Bamfield Marine Sciences Centre, British Columbia on shell repair in different species of gastropods after experimental damage1 show that rates of regeneration are inversely related to organic content of the shell.  Thus, the greater the organic component, the slower is the regeneration (see graph on Right).  Since these experimental snails2 are not fed and have to rely on what is likely to be a “standard" level of energy store for the regeneration, the inverse relationship suggests that the production of the organic matrix is more metabolically3 demanding than the crystallisation of calcium carbonate.  Palmer 1983 Mar Biol 75: 287.

NOTE1  shells are damaged by clipping away a goodly proportion of the last body whorl with pliers.  Regeneration is measured as mass of shell added over roughly 40-d periods at 12-14oC.  Proportion of organic matter is determined from mass loss of dried shell after ashing

NOTE2  the 15 species used in the study include 7 neogastropods

NOTE3  the author cites unpublished data suggesting that protein synthesis may actually be up to 30 times more costly than calcification 

Research study 4

photograph of whelk Nucella ostrina courtesy Nate Charbonneau and Dave Cowleshistogram showing effects of shell damage and diet on shell repair in whelks Nucella ostrinaShell repair in a mollusc is energetically costly and would be predicted to lead to decreased growth and locomotion, and possibly enhanced vulnerability to predators. During reproductive season the recipient of shell damage may be faced with a potential tradeoff between subsequent reproduction and shell repair.  As noted in a study on Nucella ostrina at the Bodega Marine Laboratory, California, if repair detracts from reproduction, then it should occur only to the extent that unrepaired injuries decrease fitness.  It is surprising, then, to find that experimental damage to shells of N. ostrina collected at Bodega histogram showing effect of damage to shells of whelks Nucella ostrina on production of egg capsulesHead, California actually leads to increased growth, especially if the snails are fed ad libitum on barnacles Balanus glandula during the 34d of recovery (see histogram above). Damage, moreover, leads to increased production of egg capsules although, in this case, nutritional status does not significantly affect the results (see histogram lower Right).  

The laboratory part of the study thus shows that food availability can limit shell growth.  In the field part of the study, 367 snails are collected, some are damaged, then all are released.  Recapture of 139 of these after 31d shows that the shell-damaged specimens grow significantly more than undamaged ones (3.2 and 2.4mm, respectively).  Mortality of shell-damaged snails is also higher than undamaged ones.  Geller 1990 J Exp Mar Biol Ecol 136: 77. Photograph courtesy Nate Charbonneau and Dave Cowles, Walla Walla University, Washington wallawalla.edu.

NOTE  the experimental treatment consists of grinding the outer lip of the shell approximately 3mm to the level of the withdrawn operculum.  Field surveys in the Bodega Head region disclose up to 6% damaged N. ostrina shells in tidepools and 20% in surge channels

NOTE  interestingly, while females invest significantly more energy into production of egg capsules when they are damaged, actual embryo production is unaffected. The author provides results of statistical analyses for this, but not the actual data

Research study 5

How costly is it for a marine mollusc to produce a shell?  Estimates for this are confounded by the fact that costs for shell manufacture cannot normally be separated from other metabolic costs.  However, the fact that the whelk Nucella lamellosa in the Barkley Sound area of British Columbia produces extra-thick shells under certain environmental conditions allows the extra food costs required for this to be estimated. By feeding both thick- and thin-shelled morphs on barnacles Balanus glandula in the field and laboratory, and measuring amounts of somatic growth, shell growth, and food consumed over periods of up to 94d, the author is able to cost out shell production by the differences observed.  Results show that calcification costs photograph of thick-shelled morph of whelk Nucella lamellosaare 1-2Joules . mg CaCO3-1 deposited, or about 5% of that estimated for the cost of the organic proteinaceous matrix on an equivalent mass basis.  The calcification cost equates to only about 6% of the overall respiratory costs for Nucella. This is low, in part owing to the ready availability of CaCO3 in shallow oceanic waters.  Palmer 1992 Proc Natl Acad Sci USA 89: 1379.

NOTE  shell costs include not just accumulating, transporting, and precipitating CaCO3, but also producing an organic matrix around which the calcarous crystals form.  Cost of the latter is estimated from other data and, as noted by the author, some “educated guesswork”

NOTE  these morphs occur on quiet-water shores where predation by crabs is more common

Thick-shelled morph of whelk Nucella lamellosa
showing what appears to be new shell growth 1.5X

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  Some other examples of shell growth in neogastropods are shown in these photos:
photograph of whelk Nucella lamellosa showing new shell growth
Nucella lamellosa exhibiting not just new shell growth, but apparently transforming into an imbricated or fluted shell shape 2X
photograph of several individuals of the whelk Nucella ostrina of different sizes, courtesy Louis Gosselin, Thompson Rivers University, Kamloops, British ColumbiaNucella ostrina ranging from 1d (1mm) to 4mo (8mm) in age. Note the colour change. Photo courtesy Louis Gosselin, Thompson Rivers University, B.C. photograph of whelk Ceratostoma foliatum with a recently grown varix
Whelk Ceratostoma foliatum showing a newly grown right varix. Individuals with half-grown varices are rarely seen, perhaps because the varices are grown quickly 1.2X
Research study 6

photograph of thin- and thick-lipped specimens of the snail Amphissa columbianaResearch at Friday Harbor Laboratories, Washington on the intertidal snail Amphissa columbiana reveals 2 distinctly different growth forms, one with thin apertural lips; the other, with thick lips (see photographs).  In laboratory cultures over periods of up to 11wk on diets of minced scallops Chlamys sp., the first type grows quickly but never becomes sexually mature, while the second type grows slowly but is sexually mature. Tests whether shell-thickening could be a phenotypic-plastic response to the presence of predators (the red rock-crab Cancer productus) produce negative results.  Rather, it appears that like other species of columbellids, growth of A. columbiana mostly ceases when sexual maturation is attained.  This ontogenetic change in shell form is therefore a reliable indicator of sexual maturity  in this species.  Pernet 2007 Am Malacol Bull 22 (1): 7.

Research study 7
  Recent interest in long-term effects of global warming on marine ecosystems includes those resulting from increased acidification stemming from greater levels of atmospheric CO2.  Because there is no way to account for the decades-long chronic changes expected with the liklihood of metabolic acclimatisation that may occur during such long time-periods, studies to date on this subject are confined to relatively short-term acute tests of different pHs on various metabolic functions.  A study on growth of whelks Nucella lamellosa at the Bamfield Marine Sciences Centre, British Columbia takes 2 approaches. The first assesses acute effects of pH on rate of calcification while the other measures effects of the same pH levels on shell dissolution.  While the first is something that could show adaptive change over time, the second is based on a stoichiometric response of calcareous shell material to a certain pH, and would not be expected to show adaptive change over time.  Results of 6d experimental exposure to pH levels of 7.8 and 7.5 do reveal a significant (slope of regression) decrease in shell mass over controls in normal seawater (pH 8.0=385ppm CO2) but, when these values are corrected for loss of shell mass in empty control shells, the slopes of the regressions become non-significant (see graph).  The authors conclude that it is not production of new shell material that is being affected, graph showing effects of pH on shell formation and dissolution in whelks Nucella lamellosabut increased dissolution of existing shell material.  Their overall conclusion from these preliminary findings is that ocean acidification related to global warming may have greater effect on shell dissolution than on calcification processes.  Nienhuis et al. 2010 Proc: Biol Sci 277 (1693): 2553.

NOTE  levels used are those predicted to occur in the years 2100 (785ppm; predicted pH=7.8) and 2200 (1585ppm; predicted pH=7.5) at present rates of increase in atmospheric CO2 content .  The treatment levels used are created by bubbling test seawater of pH 8.0 with different concentrations of CO2.  Under these treatment conditions pH equilibrium is established within 1h

After correcting the shell masses of live snails for shell dissolution in the
less basic media, slopes of the regressions are no longer significant.  The 50%
correction is the more realistic one, because while the empty-shell treatment
(bottom line on graph) is being affected by the lower pH water both inside and
outside of the shell, a live snail would protect the inner shell surface with
its own tissues; thus, only the outer shell surface would theoretically be eroded.
  Note that this assumes that the snail’s hemolymph is being buffered from pH effects
from outside seawater, which it likely is, and this is discussed by the researchers

Research study 8

photograph of whelk Nucella lamellosa with axial sculpturingphotograph of whelk Nucella lamellosa with no axial sculpturingWhelks Nucella lamellosa in British Columbia come in two distinct morphs: a frilly thinner-shelled form adorned with scalloping, and a thicker-shelled form not so adorned (see photos). The lamellae on the first morph are formed in a more-or-less regular pattern and can be regenerated following shell damage. The pattern of regeneration, however, is different than one might expect. Rather than being replaced in their original configuration, researchers at the Bamfield Marine Sciences Centre find that snails with all shell sculpturing experimentally removed regenerate them in no particular order or pattern. Furthermore, feeding rate and initial body size significantly affect only growth in shell length, and not rate, placement, or spacing of the lamellae. At the experimental culture temperature used (9-12oC) and on a diet of acorn barnacles (unidesignated species), a new lamella is added on average every 9d, without significant hiatus (about 2d on average) but with considerable variability both within and among individuals. The study adds useful information to our knowledge of shell sculpturing in whelks. Webster & Palmer 2016 Biol Bull 230: 1.

NOTE referred to by the authors as axial lamellae or axial sculpturing, but not axial varices). The difference between lamellae and varices apparently is, in the authors’ view, that the former show no regular spacing or any significant pause in their growth as there is following production varices in other species

NOTE this is the value given by the authors for “time to grow one complete lamella”, but in a later section of the results entitled “Time to grow a lamella”, a value of 16d is reported. In a third section of the results also inexplicably entitled “Time to grow a lamella”, another value of 14d (for snails <29mm shell length) is given. All treatments appear to involve ad libitum feeding by similarly sized snails (15-36mm shell length) at the same culture temperature, so the differences likely represent the extent of variability noted by the authors


Effects of parasitism on growth & maturation of selected whelks

Research study 1

histogram showing relationship of size/age of mud snails Cerithidea californica with incidence of parasitismThe southern California horn snail Cerithidea californica inhabits high-intertidal mudflats and marshes in protected bays and estuaries.  It feeds on organic matter including diatoms and other plant matter.  Growth occurs during spring/summer, while winter is a dormancy period spent burrowed into the substratum.  Life span is about 8-10yr.  Interestingly, at least 17 trematode-worm species use these mud snails as intermedate hosts, with 12 being common in the study site of Bolinas Lagoon, California.  Parasitism is most common in larger snails, reaching 100% in individuals greater than about 32mm shell length (see graph).  The parasites mostly inhabit the gonad and, in so doing, lead to functional castration. Their presence robs their hosts of essential nutrients and energy, leading to stultification of growth of both sexes.  Effects on growth differ with species of parasite. Sousa 1983 J Exp Mar Biol Ecol 73: 273.

NOTE  birds are the definitive hosts 

Research study 2

A parasitised horn snail Cerithidea californica is predicted to be seriously stressed, and a question posed by researchers from the University of California, Berkeley is how well does it accommodate additional stresses of  temperature, salinity, and air exposure alone or in combination.  Environmental conditions in Cerithidea’s high-intertidal salt-marsh habitat in Bolinas Lagoon, California can be severe, and temperatures and salinities in excess of 30oC and 40ppt, respectively, are not uncommon in summer.  Experiments measuring percentage survival are conducted in the laboratory in 250ml glass beakers over periods ranging from 6-534h using different combinations of temperature (5-30oC), photograph of horn snails on a bed of green algae courtesy iNaturalistsalinity (0-60ppt), desiccation (dry, moist), light (variable day:night hr), dissolved oxygen (0.3-8.7ppm), and parasitised (yes vs. no).   Results show, surprisingly, that with only a single exception, infected and uninfected snails survive all combinations equally well.  Only in conditions of low levels of dissolved oxygen do infected snails die at higher rates than uninfected ones, a difference that is exacerbated by high experimental water temperatures. Sousa & Gleason 1989 Oecologia 80 (4): 456. Photograph courtesy iNaturalist.org.

NOTE  “parts per thousand”; oceanic seawater is about 35ppt

NOTE  “parts per million”; aerated seawater at room temperature is about 8.7ppm oxygen

Horn snails Cerithidea californica. Sub-algal surface
oxygen levels on a warm day may be as low as 0ppm
Research study 3

graph showing the relationship of size of horn snails Cerithidea californica with prevalence of trematode-parasite infestation histogram showing translocation results for experiments involving reproductive maturation in parasitised horn snails Cerithidea californicaA later study on reproductive maturation in Cerithidea californica by a researcher at the University of California, Santa Barbara reveals a negative association between maturation size and prevalence of infestation by parasitic trematodes at 18 sites in southern California and Baja California (see graph on Left).  A strategy of reproducing at a smaller size may be based on phenotypic plasticity where individuals adjust the timing of maturation to cues received from the environment, or it may represent past selection for early-maturing genotypes.  To determine whether the effects are strictly environmental or whether the populations differ genetically, the author undertakes reciprocal translocations of individuals between 2 sites in southern California with high and low prevalences of parasitism.  Results show that snails moved from one site to the other site mature at significantly different sizes, suggesting at least some genetic involvement (see histogram).  Conversely, snails translocated to the high-prevalence sites mature at smaller size than ones translocated to the low-prevalence sites, indicating an environmental effect.  Lafferty 1993 Oikos 68: 3; see also Lafferty 1993 Mar Ecol Prog Ser 96: 229 for an account of effect of parasitic castration on density of snails C. californica.

NOTE  the author is aware that the relationship depicted is likely sigmoidally shaped, but uses a linear-regression analysis for convenience

NOTE  the sites are Carpinteria Salt Marsh and Bolsa Chica State Beach, California, respectively

Research study 4

sign warning about swimmer's itch at Crescent Beach, British Columbiagraph showing relationship of shell size and infection rate for mud snails Ilyanassa obsoleta infected with trematode Austrobilharzia variglandisIt may be a surprise to know that swimmer’s itch is present in the sea as well as in freshwater. It is caused by a flatworm parasite whose life cycle alternates between birds, the definitive host, and snails, the intermediate host. In the example presented here, researchers at Simon Fraser University associate swimmer’s itch outbreaks at Crescent Beach, British Columbia with release of cercaria larvae of the trematode Austrobilharzia variglandis from host mud snails Ilyanassa obsoleta. The adult worms live in the guts of birds, mainly ducks. When reproductive, the eggs of the worms are defecated by the birds and hatch in the water to miricidia larvae. The miricidiae seek out mud snails, enter them, and grow to cercaria larvae that eventually leave the snail to hunt down a suitable bird host. If the circariae contact a warm-blooded human during their hunt, they attempt to burrow into the skin but do not survive. The results are itchy lesions that may lead to later sensitisation to cercaria antigens, making things worse the next time round. The mud snails at Crescent Beach arrived over a century ago from the east coast of North America, perhaps via import of eastern oysters for local aquaculture. Note in the graph that larger, photograph of mud snails Ilyanassa obsoleta at Crescent Beach, British Columbiaolder snails carry heavier parasite loads than smaller, younger snails. Whether the parasites negatively affect growth and maturation of their hosts is likely, but the extent to which this happens has not been determined. Leighton et al. 2003 Publ Fraser Health Authority, Government of British Columbia.

NOTE specifically, a category of trematode flatworms known as blood-flukes. In addition to swimmer’s itch, which on first exposure is usually just annoying, these parasites are responsible for schistosomiasis, a group of debilitating blood diseases that afflict hundreds of millions of humans worldwide


Mud snails Ilyanassa obsoleta are plentiful at Crescent Beach,
BC owing in part to abundant food in the form of organic
matter and scavengeable dead macro-organisms in the mud