How do periwinkles adapt to their environment

The reported maximum flow speed that each snail resisted is expressed as the corresponding maximum free stream velocity recorded in the flume pipe. This is the maximum water speed at the center of the pipe at a given valve aperture angle.

Adult snails should experience marginally lower flow speeds than this, but the small juvenile snails were affected by the boundary layer formed close to the substrate S2 File and experienced lower local speeds.

However, we use the free stream velocity as a reference flow speed for all measurements, as it represents the speed of the moving waves. For the snails sampled along the transect only, aperture and spire views of the shell were photographed Fig 1C and 1D. From these images, shell area SA , outer OA and inner IA aperture areas following [ 21 ] and two different shell length measurements L1 and L2, each with an orthogonal width measurement W1 and W2 were all measured using the Image J software [ 39 ].

L1 was the distance from the tip of the spire to the most distant point of the shell, and its corresponding width W1 was its maximum orthogonal distance. L2 was the maximum distance from the front in a crawling motion of the aperture to the back of the first coil, and W2 was the maximum distance orthogonal to L2 Fig 1C. In addition, the underside of the foot for each snail during crawling on a transparent surface was photographed and the foot area FA was measured from this photograph S1 Fig.

The foot area of 13 snails could not be photographed because the snails did not come out of the shell and these individuals were discarded from down-stream morphometric analyses requiring foot area.

The absolute values of foot and aperture areas were divided by the shell area to get size-independent estimates relative foot area; RFA, relative outer aperture area; ROA, and relative inner aperture area; RIA. Shell area SA was used as a proxy for size. The cause of dislodgement is the water force exerted on a snail's surface and it scales to the square of the water velocity [ 40 ], the maximum free stream velocity variable was therefore squared before fitting a cline of flow resistance versus position on the transect.

The simple cline function for a phenotypic trait used in [ 41 ] was fitted to traits and positions of individual snails by maximising the likelihood with the mle2 function of the package bbmle [ 42 ] in a custom R script. Initial values of these parameters were estimated by visualizing plots. The residuals from each cline fit, that is the difference between the measured value and the fitted value, were used as variables for further analysis.

Traits that strongly contributed to the snails' capacity to resist water flow were expected to have residual correlation with the residuals of the water velocity. Shapiro's test showed deviation from normality of residuals of shell area, inner aperture area and shape 1. The spearman correlation coefficient was used for trait residuals that deviated from normality, otherwise, pearson correlation coefficient was used.

To test the independence of the morphological traits, after allowing for clinal variation across the habitat transition, we also performed pairwise tests for correlations between residuals of the morphological traits. Figures were created in R with the package ggplot2 and Gimp 2 for further layering. The free-stream flow velocity in the high-speed flume stabilized after roughly a second from opening of the valve and remained stable for at least 4s S2 File. Both the acceleration of flow and the maximum flow velocity increased with increased level of valve opening.

The maximum free-stream velocity reached was 0. These velocities do not attain the maximal speeds that can exist in the field but cover most typical water speed conditions for breaking waves in the study area S3 File. After the initial acceleration of flow there were cyclic events of deceleration followed by acceleration indicating the presence of large-scale eddies in the pipe S2 File similar to irregularities likely to be common in nature. The transition from boulder to cliff habitat was accompanied by diminishing density of Fucus seaweed and, finally, its complete disappearance, suggesting increased levels of wave stress Fig 2.

All morphological traits changed along the Bezier path Fig 3 and S4 File. Shell area, relative foot area and relative outer and inner aperture areas increased towards the wave exposed habitat.

Lines are the best fitting sigmoid functions describing the clines in the traits, with y values on the left of the graph. The best fitting cline for the squared flow resistance SFR is plotted as a bold black curve, with y values on the right of the graph. A black arrow marks the position of the transition from boulder to cliff habitat and a green arrow indicates the disappearance of Fucus sp. Among the six morphological traits measured, the residuals for three traits correlated positively with higher residual resistance to water flow: shape 2 a more laterally compressed shell , relative outer aperture area, and relative foot area Table 1 , Fig 4.

No correlation was found with the remaining traits. Effects of individual traits remained difficult to separate because all of the morphological variables showed pair-wise correlations with each other, even after removing the clinal effects S1 Table. Residuals of the three phenotypes with significant association with the snails' flow speed resistance are plotted against the residuals of squared maximum free stream velocity resisted.

The median and mean values for each category are represented respectively as a thick horizontal bar and a filled diamond. The whiskers extend to the most extreme data point within 1. Black regression lines illustrate the positive relationship between the trait residuals and flow resistance residuals. Small amounts of random variation were added in the x dimension to facilitate the visualization of all data points.

This may be due to the problem, described earlier, that we were unable to see if the tiny juveniles were properly attached or not before the water flow was turned on. Number of snails that resisted various maximum water speeds free stream velocity. Note that the x-axis is not a linear scale. Intertidal gastropods can reduce the risk of wave-dislodgement by at least three mechanisms. First, adaptive behaviours such as occupying crevices and a rapid switch to activity when submerged after a low tide to avoid being swept ashore by the first waves can reduce dislodgement risk [ 34 ].

Second, an appropriate body and shell morphology may reduce hydrodynamic drag and lift forces [ 25 ]. Third, an increased adhesive force exerted by the foot may reduce the risk of dislodgement [ 23 , 25 — 27 ]. Hitherto, it has been shown that snails of the wave ecotype of Littorina saxatilis tend to seek shelter in crevices or similar structures in laboratory tanks [ 8 ], and are more active than snails of the crab ecotype [ 34 ] matching the expectation of a behaviour appropriate to wave-exposed conditions.

In the current study, the second and third mechanisms that may further contribute to a lower risk of dislodgement in wave-exposed habitats were assessed experimentally.

Over the boulder to cliff transect, the progressive disappearance of Fucus seaweeds indicated increased wave action [ 37 — 38 ] and at the same time our experiments showed a larger resistance to hydrodynamic forces among the snails from the cliff outcrop than among those from the boulder habitat. Furthermore, we showed that such resistance was higher in snails with a larger foot area and a wider outer aperture area, largely supporting suggestions made earlier without experimental support [ 19 , 23 , 25 , 27 ].

Additionally, we found that snails facing a flow with a shell more laterally compressed had higher resistance than snails that were wider when facing the flow—but note that the advantage provided by specific shell proportions is difficult assess due to correlations with other shell characteristics S1 Table. For a given height, shells with a high S2 value have a smaller cross-sectional area towards the water flow, when oriented with the head towards the flow, and this orientation was preferred by the snails as soon as they experienced the first gentle flow of water.

One additional observation made during the experiments with the flume was that the shell of the snails from the crab ecotype vibrated considerably more while exposed to the rapid flow than the shell of the wave ecotype snails. This suggests that shell shape of the wave ecotype delays flow separation and reduces turbulent eddy generation.

We observed that size and relative foot area had the steepest clines along the transect, while clines for the two shape variables and the inner and outer aperture areas were much more shallow Fig 3. Interestingly, the size and foot area clines did not overlap in position; the center of the size cline was shifted towards the cliff end of the transect and coincided approximately with the disappearance of the Fucus , while the center of the foot area cline coincided with the transition from boulder to cliff substrate S4 File.

Multiple effects may cause clines not to overlap. For example, this could reflect that different selective forces may transition at different locations, or that the strength of opposing selective forces is asymmetric. One hypothesis is that if crab selection is primarily on shell size and thickness, the shell size decreases abruptly when Fucus disappears, where the shore crabs mostly hide pers. Foot area would increase at the boulder to cliff transition, due to the more dangerous hydrodynamic forces on cliffs.

Indeed, even though snails may be dislodged by crabs in the boulder habitat they are likely caught among the boulders and remain in their habitat. On the cliffs however, dislodgement will most likely result in the displacement of the snail into the sublittoral zone where live L.

A second hypothesis is that selection by crab predation favouring big shells is stronger than the threat of wave dislodgement at the transition, and pushes the center of the size cline toward the cliff habitat, while affecting foot area less.

Repeated analyses of clines in other contact zones are needed to corroborate or refute these suggestions, but preliminary results suggest that the size cline is most often displaced towards the cliff habitat pers.

Many studies indicate that organisms in wave-swept environments are limited in size [ 40 ]. This observation may suggest that shell size affects the ability of snails to cope with water flow, especially if smaller individuals benefit sufficiently from reduced velocities deep in the boundary layer.

Nonetheless, even if smaller organisms expose a reduced area to the flow and thereby reduce the drag force, they also have a comparably smaller foot to hold on to the substratum. Consequently, for isometric shapes there may be no size difference in the resistance to flow other than the benefit of the boundary layer, with negligible effect on adult snails but see below for juveniles. However, a smaller size will increase access to small crevices in the wave habitat and, in this way, facilitate the sheltering of snails from wave forces and other types of stressors, such as heating and desiccation [ 28 , 29 ].

Surprisingly enough, the small juvenile snails raised in the laboratory performed very well under rapid flows, with velocities resisted matching those tolerated by adults of the same ecotype. Due to their tiny sizes 0. Since the flow-induced drag and lift forces on a snail scale with the square of the local flow velocity around the snail [ 40 ], the very small juvenile snails were thus exposed to much lower forces than the adult snails, which contributed to their high capability to resist similar free stream velocities.

Offspring of wave and crab ecotype snails from two other islands had also different water flow resistance. This ecotype specific difference was found between juveniles and between adults snails raised in still water in the laboratory.

Firstly, this shows that the pattern found in the first island sampled was not unique but was general to this type of environmental transitions and ecotype contact zones.

Secondly, it indicates that the differences in flow resistance observed are largely heritable even though our study design does not exclude maternal effects. Finally, it shows that this difference is observable very early in the life of the snails and that it persists in life even in absence of environmental stimuli. Already in the range of 0 to 2. Nonetheless, the upper limit reached in the flume are flow speeds that are not excessively rare in the field, especially in the cliff habitat S3 File.

One hypothesis is that, since these violent events can induce high mortality in intertidal communities [ 45 ], they are strong selective events for the phenotypes that favor intertidal snails' resistance to dislodgement [ 18 , 46 ]. Years with storms induced a significant increase in aperture areas in a population of Littorina striata living on an exposed site compared with years without storms [ 46 ]. In Littorina obtusata , an exceptionally strong storm was found to reduce mean shell height and also, counter-intuitively, to reduce mean aperture area [ 18 ].

If intertidal snails occasionally face these powerful events, it is to be noted that in our study, no snail collected in the boulders could withstand a speed of 2. In the present experiment, the snails were placed in a flume without structures that slowed down the water flow, and therefore exposed to water velocities that are close to the free stream velocity.

In the field, snails will probably avoid the maximum speeds of breaking waves by finding refuge in cliff crevices or among boulders and mitigate physical stress of storms. The comparison of the measurements obtained experimentally with the conditions that can exist in the field suggests that the snails' use of the microenvironment to reduce local flow speed is crucial to maintaining their grip in stormy conditions.

Our results support the expectation that a common intertidal gastropod, Littorina saxatilis , is locally adapted to withstand strong water forces in populations inhabiting cliff surfaces where snails are from time to time heavily exposed to waves. Traits most involved in this adaptation are foot area, the outer shell aperture area, and the lateral compression of the shell shape, while size seems not to play a role in resisting rapid water currents.

The adaptive phenotypic components were shown to be heritable and effective already in 2-week-old hatchlings. We thank Irena Sencic for her help with fieldwork, and Thomas Johannesson and Thore Hilmersson for constructing the high-speed flume. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract The periwinkle Littorina saxatilis has repeatedly evolved both a small, fragile and globose "wave ecotype" confined to wave-swept shores and a large, robust and elongated "crab ecotype" found in nearby crab-rich but less-exposed shores.

Introduction A correlation between an environmental factor and a phenotypic trait is not sufficient to infer that there is local adaptation of the trait in response to that factor. In contrast to our study, Raffaelli found that shells of L.

However, despite the higher crab abundance in conjunction with higher predation pressure on the sheltered sedimentary shore in this study, periwinkles produced comparatively weak and thin shells. Thus, predator abundance and pressure seem to be of minor importance for shell morphology of L.

Third, different shell morphologies may result from different levels of intra-specific competition. Competition for food, resulting from high population densities has been shown to affect variation in snail size Sherrell Furthermore, Kemp and Bertness showed that in dense snail populations with slow individual growth rate, periwinkles have elongate and thicker shells in comparison to specimens with rounder, globose shells in sparse populations.

However, despite high densities of periwinkles on the sedimentary shore, L. Additionally, Fenske supposed that available resources in the Wadden Sea at Sylt are sufficient to maintain a high population density of L.

At the sedimentary shore, we found a higher prevalence of both trematode parasites and shell boring polychaetes P. The association with both trematodes and shell boring polychaetes may largely account for the observed lower abundance of large L. Among metazoans, trematodes are the most common parasites of intertidal organisms and their complex life cycles almost always involves a gastropod as first intermediate host Mouritson and Poulin Trematode-infected L.

Furthermore, infected periwinkles have a reduced mobility. Following grazing migrations during low tide parasitized periwinkles might be too slow to find sheltered sites and, thus, might experience higher predation pressures by crabs approaching with the incoming tide.

Moreover, parasitized snails might arrive late at snail aggregations where they are consequently situated at the periphery. This will make them more susceptible to crab predation because of a higher probability of being among the first-encountered individuals Davies and Knowles Not all size classes of L. Lauckner showed that periwinkles below 12 mm shell height are not infested and that prevalence of parasites increases with increasing shell height.

Thus, trematode parasites cause mortality predominantly in larger snails and may be one important factor for low abundances of snails above 18 mm shell height on the sedimentary shore. Similarly, the prevalence of shell boring polychaetes P. Whether an infestation with P. However, periwinkles infested with shell boring polychaetes have a greatly reduced shell strength and are preferentially eaten by shore crabs C. This indirect effect also affects large periwinkles that are normally outside the food spectrum of C.

Hence, the comparatively high prevalence of P. The lack of small-sized periwinkles on the rocky shore of Helgoland is more difficult to explain. Hylleberg and Christensen show that small L. Hence, the higher wave exposure may be an important mortality factor for juvenile snails on the rocky shore.

Additionally, low numbers of juvenile L. Small periwinkles can retreat in deep crevices and thus are hardly detectable by an investigator. Within these crevices juvenile periwinkles may also escape predatory crabs. Behavioural changes in L. Molis, unpublished data. Thus, we cannot exclude that also other factors such as competition or failing recruitment may responsible for low numbers of small L. In summary, we conclude that the differences in shell size distribution between L.

Littorea populations of the two environments result from biotic factors which mainly affect the L. Albrecht A Soft bottom versus hard rock: community ecology of macroalgae on intertidal mussel beds in the Wadden Sea.

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Evolution — Ecology — Ecol Lett — As the scientists discovered, the marine gastropod Littorina littorea common periwinkle , which has very successfully colonized the Northern Atlantic shores, has found a peculiarstrategy for even more efficient detoxification.

Studying the molecular differences between the proteins among various species, the scientists solved the solution structure of the periwinkle metallothionein by using nuclear magnetic resonance techniques and compared it with other known structures and sequences.

Surprisingly, the periwinkle's protein comprises three independent domains, while other known metallothioneins have only one or two. Each of the three domains contains nine cystein residues binding a cluster of three cadmium ions, thus the total 27 cystein residues can incorporate nine cadmium ions. This sheds light on the adaptation strategy: "Increasing the number of domains simply increases the metal-binding capacity of the protein and thereby potentiates its metal-detoxification capacity," the authors wrote.

Regarding the structural features, the complex formed with cadmium is very similar to that of the Roman snail form, which can efficiently discriminate between the copper ions vital to snails and toxic cadmium. And apart from simply coping with cadmium-rich environments and selecting copper from other heavy metals, the cysteine-rich metallothioneins are considered as important oxidative-stress-response proteins.

Stress is one of the major encounters of the common periwinkle, which can survive rough seas and drought at the same time. Materials provided by Wiley. Note: Content may be edited for style and length.