Nucella Lamellosa Research Articles

An inducible morphological defence is a passive by-product of behaviour in a marine snail

Many organisms have evolved inducible defences in response to spatial and temporal variability in predation risk. These defences are assumed to incur large costs to prey; however, few studies have investigated the mechanisms and costs underlying these adaptive responses. I examined the proximate cause of predator-induced shell thickening in a marine snail (Nucella lamellosa) and tested whether induced thickening leads to an increase in structural strength. Results indicate that although predators (crabs) induce thicker shells, the response is a passive by-product of reduced feeding and somatic growth rather than an active physiological response to predation risk. Physical tests indicate that although the shells of predator-induced snails are significantly stronger, the increase in performance is no different than that of snails with limited access to food. Increased shell strength is attributable to an increase in the energetically inexpensive microstructural layer rather than to material property changes in the shell. This mechanism suggests that predator-induced shell defences may be neither energetically nor developmentally costly. Positive correlations between antipredator behaviour and morphological defences may explain commonly observed associations between growth reduction and defence production in other systems and could have implications for the evolutionary potential of these plastic traits.

High‐pressure freezing of spermiogenic nuclei supports a dynamic chromatin model for the histone‐to‐protamine transition

In this study, we present for the first time a description of the dynamic chromatin changes that occur during spermiogenesis in the internally fertilizing caenogastropod mollusc Nucella lamellosa. Chromatin condensation in developing sperm cells in some animals, such as the model biological system used here, involves the histone-to-protamine transition and proceeds through a patterning stage from granules to fibers to lamellae. This may be due to the physicochemical phenomenon of phase separation by spinodal decomposition, a dynamic mechanism known to generate pattern. This hypothesis is based entirely on published transmission electron microscopy photomicrographs using conventional fixation technology. We now report that spermatid nuclear patterning and subsequent condensation in testis of Nucella lamellosa fixed by high-pressure freezing and freeze substitution (HPF/FS) is similar to that in glutaraldehyde-fixed testis, and can be related to the processing of sperm nuclear basic proteins (SNBPs).

Past predation risk induces an intertidal whelk (Nucella lamellosa) to respond to more dilute concentrations of its predator’s scent

Unless sensory control is coupled with developmental flexibility, organisms are unable to produce adaptive phenotypes in response to environmental risk cues. However, empirical examples of adaptive phenotypic plasticity focus largely on development and rarely on sensory control. Here, I ask whether past exposure to predation cues affects an intertidal whelk’s (Nucella lamellosa) sensitivity to the scent of a known predatory crab (Cancer productus). I pre-conditioned whelks for 30 days with the smell of crabs eating other whelks and then, after a period of rest (14 days in fresh seawater free of predator effluent), re-introduced them to different concentrations of waterborne crab scent. Relative to controls, pre-conditioned whelks expressed crab-defences at significantly lower concentrations of crab effluent, suggesting the pre-conditioning reduced their risk–response threshold. Results remind us that the full scope of factors controlling adaptive phenotypic plasticity in natural populations remains underappreciated.

Prioritized phenotypic responses to combined predators in a marine snail

Although many species face numerous predators in nature, the combined impact of multiple predators on the inducible defenses of prey has rarely been studied. Prey may respond with an intermediate phenotype that balances the risk from several sources or may simply respond to the most dangerous predator. I examined the separate and combined effects of the presence of shell-breaking (crabs, Cancer productus) and shell-entry (seastars, Pisaster ochraceus) predators fed conspecific snails on the defensive shell morphology and antipredator behavior of a marine snail (Nucella lamellosa). When exposed to each feeding predator separately, snails responded with a combination of morphological defenses that reflect the attack mode of the predator and a generalized behavioral response. Snails responded to feeding crabs by increasing refuge use and producing a thick, rotund shell. Snails responded to feeding seastars with increased refuge use but produced elongate shells with high spires that allowed for greater retraction of the soft tissue. Seastar-induced phenotypes reduced susceptibility to seastars relative to crab-induced phenotypes, but crab-induced phenotypes did not significantly reduce susceptibility to crabs, indicating an asymmetrical functional trade-off. When feeding predators were combined, snails produced a morphological phenotype similar to that expressed in the presence of the predator that imposed the highest mortality at the population level, suggesting that predator-induced morphology was prioritized according to predation risk. These results suggest that prioritizing conflicting defenses according to predator danger may be a common strategy for prey responding to combined predators, particularly in conjunction with generalized behavioral responses that reduce overall risk in multiple-predator environments.

Clumping behavior as a strategy against drilling predation: Implications for the fossil record

Drilling gastropod predators are of particular interest to paleontologists, because predatory drill-holes in marine invertebrates serve as one of the rare sources of data for the study of ancient predator-prey interactions. Modern laboratory studies are an important part of predation research providing valuable ecological insight and constraining fossil evidence and interpretations. Previous studies have shown that mussels use clumping behavior against durophagous predation [Okamura, B., 1986. Group living and the effects of spatial position in aggregations of Mylitus edulis. Oecologia 69, 341-347.; Lin, J., 1991. Predator-prey interactions between blue crabs and ribbed mussels living in clumps. Estuar. Coast. Shelf Sci. 32, 61-69.], but its role against drilling predation had not been explored. In this study, we explore the effect of clumping on predator success (drill-hole frequency) and prey handling (drill-hole position) using the mussel, Mytilus trossulus, as prey and the gastropod, Nucella lamellosa, as drilling predator. We assigned mussels to two groups: in one, mussels were allowed to clump together with their byssal threads, and in the other, they were kept separate. We observed a significant decrease in the drilling frequency within the group containing clumped mussels, confirming that clumping acts as a successful anti-predatory strategy against drilling predators. The use of clumping as an effective strategy against multiple types of predators may relax the trade-offs associated with aggregated lifestyles [Bertness, M.D., Grosholz, E., 1985. Population dynamics of the ribbed mussel, Geukensia demissa: the costs and benefits of an aggregated distribution. Oecologia 67, 192-204.]. The increased benefit and unchanged metabolic cost of clumped living alters estimates of individual fitness with evolutionarily significant implications (e.g., eliminating the need to invoke group or species selection to explain the adaptive benefit of an aggregated lifestyle). In spite of potential differences in prey handling and grappling due to clumping, mean drill-hole placement and variation in drill-hole placement showed no significant differences between the two groups. These observations suggest that comparison of predation intensities across clumping and non-clumping taxa must consider the anti-predatory effect of this behavior.

Drilling under threat: An experimental assessment of the drilling behavior of Nucella lamellosa in the presence of a predator

Using the drilling muricid, Nucella lamellosa (Gmelin 1791) and its prey, the mussel Mytilus trossulus (Gould 1850), the impact of a secondary predator, the crab Cancer gracilis, on drilling was investigated experimentally. The frequency of incomplete holes was compared under two conditions: (1) when the gastropod's natural predator, C. gracilis, was present and (2) when it was absent. The results indicate that the presence of a secondary predator can affect drilling activity, leading to a significant increase in the frequency of incomplete drill holes. The introduction of a secondary predator can also decrease the overall drilling frequency. The size distributions of completely and incompletely drilled mussels suggest that in the presence of the secondary predator the decision by the gastropod to either abandon or continue drilling its prey might be influenced by how much time it has already invested into drilling or the size of the prey item. These results are important for the ecological and evolutionary implications of incomplete drill holes frequencies, especially with regard for their use as proxies for evolutionary prey improvement.

SHELL-LESS NUCELLA LAMELLOSA (GMELIN) FROM THE ROCKY INTERTIDAL ZONE OF SAN JUAN ISLAND, WASHINGTON

In the summer of 2004, seven Nucella lamellosa snails from the rocky intertidal zone were found to have detached from their shells after collection. The snails continued to live and function normally for several weeks after discovery. The loss of the shell may have been a reaction to stressful environmental stimuli.

SHELL-SELECTION BEHAVIOR OF THE HERMIT CRAB PAGURUS GRANOSIMANUS IN RELATION TO ISOLATION, COMPETITION, AND PREDATION

Hermit crabs select shells based on size, weight, species of gastropod, and shell condition. However, in many environments, empty, undamaged gastropod shells are in short supply and this shortage may influence hermit crab shell selection behavior. In this study, the effects of isolation, competition, and predation on shell selection behaviors were investigated using Pagurus granosimanus (Stimpson), a hermit crab from San Juan Island, WA. The hermit crabs were provided with a choice between undamaged, slightly damaged, or very damaged Nucella lamellosa (Gmelin) gastropod shells and were subjected to either isolation (control treatment), water infused with the chemical cues of conspecific hermit crabs (competition treatment) or water infused with both predator (Cancer magister, Dana), and dead conspecific chemical cues (predation treatment). In all 3 experimental treatments, after a trial duration of 20 min, hermit crabs preferentially selected the undamaged shell. However, the frequency of shell switches varied significantly between the three experimental conditions. Hermit crabs in the control treatment switched between shells most frequently and hermit crabs in the competition group switched least frequently. Additionally, larger hermit crabs switched shells more frequently than smaller hermit crabs in all experimental conditions. In settings where competition is the primary environmental stress, such as in the San Juan Islands, the reduced frequency of shell switching may have a long-term effect on hermit crab defense against predation, in turn reducing the reproductive success and population size of hermit crabs.

TESTING THE ROLE OF SPINES AS PREDATORY DEFENSE

Spines are frequently considered to be an important physical defense against predators. This experiment shows that spines do not always function successfully as physical protection. Using natural predators and prey (the drilling muricid gastropod Nucella lamellosa (Gmelin 1791) and the mussel Mytilus trossulus (Gould 1850)) this experiment used artificial spines in different configurations and densities to try to assess the role of spines as predatory defense. The presence of spines did not inhibit the predator from choosing ornamented prey. Greater spine density did not improve the probability of surviving a predator encounter. Although mean handling time increased to some extent with higher spine density, the outcome of the encounter was the same. Presence or density of spines did not deter predators from attacking prey, and experimental prey with greater spine-density experienced greater mortality than did specimens with fewer spines. Drillhole dimensions differed slightly between the treatments, probably as a consequence of difficulties for the gastropod to maneuver its accessory boring organ (ABO) in between the spines.

Foraging Decision Rules and Prey Species Preferences of Northwestern Crows (Corvus caurinus)

AbstractCategorization of similar prey types and the application of decision rules by dietary generalists can enhance the efficiency of foraging decisions and facilitate the inclusion of novel prey types in the diet. While considerable research attention has been directed toward investigation of these concepts in invertebrates, few have assessed categorization and decision rules used by generalist vertebrate predators. In this study, we experimentally investigated decision rules and prey preferences of northwestern crows (Corvus caurinus) feeding on littleneck clams (Tapes philippinarum) and whelks (Nucella lamellosa). We presented crows with three species‐size combinations: small clams (2.0–2.9 cm length) paired with large whelks (4.0–4.9 cm), small clams paired with medium whelks (3.0–3.9 cm), and large clams (4.0–4.9 cm) with large whelks. Profitability estimates based on observations of crows feeding on these prey species indicated that clams were always the more energetically profitable option; however, in prey choice trials crows consistently selected the heavier prey species, regardless of differences in profitability. These results show that crows apply a general decision rule according to which they select heavier prey items when feeding on hard‐shelled prey requiring similar handling techniques, and that while such decision rules may approximate optimal choices they may not always follow predictions based solely on prey profitability. We discuss these results in the context of behavioural flexibility of generalist predators, and predicting impacts of intertidal avian predators on prey populations.

DRILL HOLES PRODUCED BY THE PREDATORY GASTROPOD NUCELLA LAMELLOSA (MURICIDAE): PALAEOBIOLOGICAL AND ECOLOGICAL IMPLICATIONS

Drill holes, used widely by biologists and palaeontologists to study predator-prey interactions, provide rich quantifiable data on drilling carnivores and their victims. A laboratory experiment, involving over 50 individuals of the drilling gastropod Nucella lamellosa (Gmelin) and several hundred individuals of its natural prey, the mussel Mytilus trossulus (Gould), was employed to test the informative value and validity of several drill-hole parameters. The majority of attacks (∼88%) were accomplished by drilling, providing a record of predation intensity that is only slightly underestimated. In three out of nine cases, prey killed without drilling exhibited an incomplete drill hole, so that incomplete muricid drill holes need not record failed predatory attacks. Drill-hole dimensions correlate with predator size, but the size and thickness ofprey shell do not affect drill-hole size. The spatial distribution of drill holes on prey shells does not suggest any obvious site-selective stereotypy in drilling behaviour. The drill-hole morphology is relatively invariant in terms of vertical profile, but highly variable in outline. Although none of the holes produced in the experiment could readily be mistaken for a naticid drilling, the high variability in outline could be misinterpreted (especially if data came from the fossil record) as evidence for presence of multiple types of predators.

Functional significance of shell sculpture in gastropod molluscs: test of a predator-deterrent hypothesis in Ceratostoma foliatum (Gmelin)

A predator-deterrence function for the varices of the muricid gastropod Ceratostoma foliatum was tested. In the first set of experiments, snails of five treatment groups were presented over a 10-week period to one of three predators: sunflower stars ( Pycnopodia helianthoides Brandt), red rock crabs ( Cancer productus Randall), and kelp-greenling fish ( Hexagrammus decagrammus Pallas). The five treatment groups were: snails with all varices removed, snails with one only of the right, middle, or left varix removed, and snails with all varices intact. The kelp-greenling fish ate no snails and were discarded from subsequent experiments. Seastars consumed significantly more snails with all varices removed than any of the other treatment groups. Crabs ate significantly more snails with all varices- and right varix-removed compared with the other three groups. Thus, snails with all varices intact were less likely to be eaten by either crab or seastar predators. Scoring the shells of Ceratostoma, but leaving the varices intact had no effect on consumption rates by either seastars or crabs. In a second set of experiments, the smooth-shelled Nucella lamellosa (Gmelin) was presented as a food item along with Ceratostoma with all varices removed and Ceratostoma with all varices intact for an 8-week period. Seastars clearly preferred the smooth-shelled Nucella over the other two groups. In contrast, crabs ate Ceratostoma with all varices removed at a greater rate than control Ceratostoma and Nucella. Energy content of dry flesh of the two snail species was almost identical, suggesting that other factors were involved in governing selection of one prey species over the other. In both sets of experiments, ingestive conditioning learning was not apparent for either the seastars or the crabs. Crabs were videotaped while feeding on Ceratostoma with all, one only, or no varices removed. The videotapes revealed that a combination of chipping the shell around the aperture with the chelipeds, then snapping it in half, was the method most often used to gain access to the soft parts of the shell. However, snails with all varices removed were more often snapped in two without any preliminary chipping, presumably because the lack of varices made them easier to break apart. There was no relationship between snail treatment and the time it took to break into the shell.

Calcification in marine molluscs: how costly is it?

Although crucial to our understanding of skeletal evolution in marine invertebrates, the cost of calcification has remained elusive for a simple reason: CaCO3 is an inorganic material. Its cost thus derives solely from the metabolic expenses of accumulating, transporting, and precipitating CaCO3 and cannot normally be separated from other metabolic costs. Traditionally, calcification cost has been ignored and total shell cost has been assumed to derive solely from skeletal organic matrix. The cost estimated here was permitted by the substantial natural variation in shell thickness in two rocky-shore gastropods (Nucella lamellosa and Nucella lapillus). In both the field and laboratory, data from three separate experiments revealed that groups of snails producing extra shell material under a particular set of experimental conditions also consumed extra food. The cost of calcification was estimated by computing the extra energy assimilated per unit extra shell produced at a common rate of tissue growth and then subtracting the cost of the organic matrix. At 1-2 J/mg of CaCO3, the calcification cost reported here is roughly 5% of that for the predominantly proteinaceous organic fraction of molluscan shells on a per-gram basis. This may explain why calcareous microstructures high in organic content have become less common evolutionarily.

Responses of a Rocky Shore Gastropod to the Effluents of Predatory and Non-predatory Crabs: Avoidance and Attraction.

Laboratory experiments revealed that the rocky shore gastropod, Nucella lamellosa (Gmelin), could discriminate between the effluents of predatory and non-predatory crabs. N. lamellosa turned away from seawater that had passed over the large predatory crab, Cancer productus Randall. This avoidance behavior was observed in snails from two localities that, based on differences in shell form, presumably experienced different levels of predation intensity. The scent of the non-predatory crabs Pugettia producta (Randall) and Lopholithodes mandtii Brandt had no effect on the turning behavior of snails from either site. Surprisingly, snails from both sites were attracted to the scent of a small shore crab, Hemigrapsus nudus (Dana), but moved at random in response to a common prey item Balanus glandula Darwin. These results suggest that N. lamellosa can assess from a distance the relative risks posed by different species of crabs, and respond appropriately. The unexpected attraction to H. nudus suggests that N. lamellosa may use this effluent to home in from a distance on potential refugia, because H. nudus are often associated with crevices and the undersides of boulders where N. lamellosa would be less vulnerable to larger predators.

Predator foraging behavior: effect of a novel prey species on prey selection by a marine intertidal gastropod

Diet breadth in predators has often been linked to maximization of energy intake in foraging models. The intertidal predatory gastropod Nucella (Thais) lamellosa (Gmelin) was presented with natural and novel prey species to examine the components of prey choice. In Washington (USA), Nucella consumes the high-quality barnacle Balanus glandula Darwin and low-quality Semibalanus cariosus (Pallas). In Alaska and British Columbia, the barnacle Semibalanus balanoides (L.) is also available as prey. S. balanoides was presented to Nucella from the San Juan Islands, Washington, in the laboratory to measure prey profitability and handling costs, and in field experiments to measure prey choice. The novel S. balanoides represents a high-quality prey, with profitability and handling costs equivalent to the highest-quality natural prey B. glandula. In the field, Nucella immediately added S. balanoides to its diet. This addition appears to be a result of active prey choice. This modification in foraging strategy is a function of the ability of Nucella to accurately assess changes to its food resource, and is consistent with the predictions of foraging models of predators which maximize energy intake.

Settling barnacle larvae avoid substrata previously occupied by a mobile predator

Settlement by the larvae of the barnacle Balanus glandula (Darwin) in the field is decreased on slate tiles that have been previously occupied by a predator of postmetamorphic stages, the whelk Nucella lamellosa (Gmelin). Settlement by another barnacle species, Semibalanus cariosus (Pallas), was not as greatly influenced by the same treatment. The effect on B. glandula also occurs when the substratum is treated with traces of the whelk by either forcing the foot over the plate or rubbing the plate with crushed individuals. This reduction in settlement can persist up to 3 wk after treatment of the substratum. A similar but lesser effect occurs after treatments with traces of a potential biological disturber of settling larvae, the limpet Tectura scutum (Rathke), but also occurs with mucus from the brown alga Fucus distichus (L.), which is not a demonstrated hazard to the barnacles. Mucus is naturally released by all of the above organisms and may be the cause of the reduced settlement. Control manipulations using a nonraucus-producing animal tissue, the pectoral muscle of the chicken Gallus gallus (L.), produced only a slight decrease in barnacle settlement. Mucus could reduce settlement either by acting as a cue for avoidance of high-risk areas, altering other settlement cues, or physically inhibiting attachment. However, not all mucus inhibits settlement: another investigator demonstrated that prior occupation by another predatory whelk induced greater settlement by another barnacle species; and we found that mucus from the dorid nudribranch Archidoris montereyensis (Cooper) increased settlement by B. glandula. Thus, our results suggest that the mucus might possibly act as a cue to the larvae, and we conclude that traces of mobile animals can influence the settlement of sessile animals. Since the threat of whelks to barnacles is delayed until some time after settlement, we hypothesize that the barnacle may be taking into account the long-term future risks (i.e., “the ghost of predation future”) when making the decision to settle. The avoidance response of the barnacle to the traces of limpets and macroalgae offers an alternative explanation (differential settlement) to patterns often attributed to biological disturbance (differential postsettlement mortality).

Ability of some gastropod egg capsules to protect against low-salinity stress

The ability of the egg capsules of three intertidal gastropod species to protect embryos against low-salinity stress was examined. Encapsulated embryos of Ilyanassa obsoleta (Say), Nucella lamellosa (Gmelin), and N. lima (Gmelin) were far more tolerant of transfer to water of reduced salinity than were embryos which had been prematurely removed from egg capsules and transferred to low-salinity sea water directly. However, the walls of N. lamellosa and N. lima capsules were found to be permeable to salts and at least to small carbohydrate molecules (glucose). Correspondingly, indirect evidence for all three species and direct evidence for N. lamellosa indicates that the osmotic concentration of intracapsular fluid declines to near ambient after transfer of egg capsules to dilute medium. Experiments conducted using embryos of N. lamellosa suggest that the egg capsules may protect embryos by reducing the rate at which the osmotic concentration of intracapsular fluid decreases rather than by reducing the magnitude of the decrease.

New marine hosts for Parorchis acanthus, Cryptocotyle lingua, Maritrema megametrios, and Maritrema gratiosum, trematodes of birds from British Columbia, Canada

New molluscan, crustacean, and avian hosts were found for four species of digenetic trematodes in Vancouver, British Columbia, from 1973 to 1977. The rediae and cercariae of Parorchis acanthus (Nicoll) were discovered in Nucella lamellosa (Gmelin). Adults were recovered after 19 days from experimental feedings of the metacercariae to a newly hatched domestic chick. The cercariae of Cryptocotyle lingua (Creplin) from the snail Littorina scutulata Gould were used to infect young fish, Leptocottus armatus Girard, Oligocottus maculosus Girard, and Platichthys stellatus (Pallas). These fish, infected with the metacercariae, were fed to newly hatched gulls, Larus glaucescens Naumann, and mature worms were found in the anterior half of the intestine after 14 and 21 days. The metacercariae of Maritrema megametrios Deblock and Rausch, found in Orchestia traskiana Stimpson and Gnorimosphaeroma oregonense (Dana), became ovigerous in Locke's solution at 40 °C at 48 h. Natural infections were found in Larus Philadelphia (Ord). The metacercariae of Maritrema gratiosum Nicoll, found in Balanus glandula Darwin, also became ovigerous in vitro. Adults were found with two other microphallid species in the intestine of one Bucephala islandica (Gmelin).