subtitle for learnabout section of A SNAIL'S ODYSSEY
  Predators & defenses
  ntertidal life, especially in the upper shore regions, may be especially risky because of exposure to a greater variety of terrestrial, aerial, and aquatic predators than would be experienced in subtidal areas.  Other than the shell and operculum, which offer physical protection, and the checker-board patterns of Littorina scutulata and L. plena, which may provide camouflaging protection, winkles have no defenses against predators.  The main predators of littorinids are crabs, fishes, and birds, and of lacunids and slipper limpets, sea stars. 
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Predation on adults by crabs

  The topic of predators & defenses is divided into predation on adults by crabs, considered here, and PREDATION ON LARVAE, PREDATION ON ADULTS BY FISHES, PREDATION ON ADULTS BY SEA STARS, and CAMOUFLAGING PROTECTION considered in other sections.
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Research study 1-2

schematic showing overlap in vertical distributions of several snail-crushing crabs and their littorinid prey Littorina sitkana and L. scutulata at Cantilever Pier, San Juan Island, WashingtonStudies at Friday Harbor Laboratories, Washington suggest that crabs foraging in the intertidal region during times of tidal immersion may be important predators on Littorina spp.  At least 5 species of shell-breaking crabs are active intertidally, depending upon degree of wave exposure, with 2 species of Hemigrapsus ranging highest in the zone, and 3 other species, Lophopanopeus bellus, Cancer productus, and C. oregonensis, working the lower levels (see graphic on Left).  All data are for a wave-exposed site, except for Lophopanopeus which are for a partly sheltered site.  The widths of the vertical arrays are proportional to densities of crabs, with crabs reaching about 100 per square meter and littorines about 400 per square meter. 

Experiments in which crabs are caged with a wide size range of Littorina sitkana show that all species of crabs of a size range 5-7g live mass are capable of breaking shells and eating even the largest littorine, up to 13mm shell length. Numbers of prey eaten per day vary greatly between the different crab species. The authors conclude that Hemigrapsus nudus, and also probably H. oregonensis, are not important predators on littorines when alternative food such as algae is available.

The authors suggest that littorines could inhabit the full vertical range of the intertidal zone were it not for predators attacking from below and setting the lower limits of the snails’ distributions.  Above tidal heights of about 1.3m, when increasing air exposure from the tides limits foraging by even the hardiest crab species, the littorines begin to enter spatial refuge from this predatory source. Behrens Yamada & Boulding 1996 J Exp Mar Biol Ecol 204: 59.

NOTE  Hemigrapsus nudus and H. oregonensis are scavengers, and both species include seaweeds in their diets

NOTE the authors provide data for 3 sites in the San Juan Islands, but only one data set is shown in the schematic above

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Research study 3

histogram comparing predation on tethered littorinid snails Littorina subrotundata, L. sitkana, and L. scutulata at wave-exposed and wave-sheltered sitesStudies at the Bamfield Marine Sciences Centre, British Columbia using 3 species of littorinids tethered to the substratum at intertidal locations show that predation is significantly less at wave-exposed sites than wave-sheltered sites (see histogram on Right). Note also that the thin-shelled species Littorina subrotundata is eaten significantly more than the 2 thicker shelled histogram comparing predation rates on 3 different sizes of littorinid snails Littorina sitkana at 2 wave-sheltered sitesspecies L. sitkana and L. scutulata.

In another experiment in which 3 sizes of Littorina sitkana are tethered in 2 wave-sheltered sites, there is a tendency at one of the sites for predators to select larger-sized individuals over smaller-sized ones (see histogram on Left).  About 30-40% of the larger snails eaten are “peeled” open, a signature strategy used by crabs, especially red rock crabs Cancer productus. Selection of larger individuals may relate to ease of handling and/or more energy gain per unit handling cost by the crabs. Boulding et al. 1999 J Exp Mar Biol Ecol 232: 217.

photograph of littorinid snail Littorina sitkana tethered to the substratum, courtesy Elizabeth Boulding, University of GuelphNOTE  a 50cm piece of monofilament line is glued to the shell apex and attached to a screw in the rock.  Does this interfere with normal behaviour of the snail and/or make it more susceptible to predation?  Scientists who use this method of monitoring their test subjects tend to sidestep the issue.   However, in even moderate wave-action the line must exert considerable drag forces on the snail and, if the snail is not actually detached from the substratum, its behaviour, especially that of a small individual, must be affected.  In this regard, the authors remark that tethering artifacts are likely minimal because the snails graze, seek refuges, and even copulate while tethered.  Does the tether make the snail more susceptible to predation? Probably not, and the tether is useful in holding the remainder of the shell for later examination


Littorina sitkana with monofilament
tether glued to the apex of its shell 1X

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Research study 4

photograph of red rock-crab Cancer productus with claws akimbohistogram showing effect of predatory crabs on growth of littorinid snails Littorina sitkanaWinkles Littorina sitkana are able to sense predatory crabs Cancer productus from a distance and change their own behaviour. This is shown in laboratory studies at Friday Harbor Laboratories, Washington where winkles are allowed to graze over a 34-d period in cages placed within larger aquarium tanks each containing another cage with either: 1) no crab (CONTROL), 2) crab with no food, and 3) crab eating L. sitkana.  Within a short time from the start of the experiment the winkles try to hide or escape, grazing is interrupted, and over the 34d period there is an 85% depression of growth, but only in winkles exposed to water flowing past crabs that are feeding on conspecific snails (see acompanying histogram).  There is no significant effect on winkles downstream from non-feeding crabs.  Behrens-Yamada et al. 1998 J Exp Mar Biol Ecol 220: 213.

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How do we interpret these results? Consider the following options, then CLICK HERE for explanations.

Winkles respond to the presence of crabs in cages by hiding away and not feeding. 

Winkles respond to the presence of a crab in a cage that is crushing and eating conspecific winkles by hiding away and not feeding. 

Winkles benefit from reduction in growth because they remain in size refuge from predation from red rock crabs. 

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Research study 5

a littorinid snail Littorina sitkana crawls on red algaehistogram comparing mortality of tethered littorinid snail Littorina scutulata at high and low intertidal heightsEffects of predators on modifying distributions of sessile intertidal invertebrates is fairly well understood by west-coast researchers, but these effects are not so well known for motile invertebrates such as littorinid snails. Under predation pressure the snails could be eaten or forced to a higher and safer intertidal zone.  This is investigated in several field experiments at the Bamfield Marine Sciences Centre, British Columbia using 2 species of littorines, Littorina sitkana and L. scutulata, and the predatory red-rock crab Cancer productus. 

Results show that snails tethered1 to the shore for 3d in areas frequented by C. productus are more often consumed at their lower distributional levels (1m above 0 chart datum) than at higher (2.5m) levels, suggesting that the crabs may be setting the lower levels of distributions of the snails (see histogram).  Note in the figure that both large and small tethered snails survive better in the high-intertidal region than in the low-intertidal region.

However, if untethered snails are marked2 and translocated3 from low-risk, or high shore, levels to high-risk, or low shore, levels, within 2-3d they crawl back up the shore to regain their original level.  Large snails are more responsive in this regard than small snails, so the crabs may be contributing to intertidal size gradients in both species of Littorina. The end result is more large snails at higher levels in both species.  Furthermore, if L. sitkana are contained in cages in the laboratory and exposed for 24h to the odours of C. productus crushing and eating conspecific snails in nearby cages, and then released in the low intertidal region, they are more likely to undertake an upshore migration than control snails. Results for similar experiments with L. scutulata are less clear. The authors note that their study is the first documentation of antipredator behaviour contributing to distributional patterns of littorinids, although such behaviour is known for other west-coast gastropods, Chlorostoma and LottiaRochette & Dill 2000 J Exp Mar Biol Ecol 253: 165.

NOTE1  tethers are monofilament line (130µm diameter) glued to the shell apex.  Although tethering is used only to assess predation intensity at different intertidal levels in the study, the authors discuss potential statistical biases resulting from use of tethers (interference, tangling, increased drag, and so on). The authors present data for both long and short tethers but, as the data seem not to differ, only results for short tethers are presented here

NOTE2  coloured enamel spray paint is used to mark the snails.  The authors do not mark control snails for “re-release” at each site to assess effects of handling and painting; rather they assume from other studies that marking has no significant effect on survival or susceptibility to predators.  Generally >90% of marked snails, both dead and alive, are recovered

NOTE3  the authors use the term “tranplant” to refer to snails being moved from, say, high to low intertidal regions, and “translocate” to refer to being moved, say, from one high intertidal location to another high location, but only the latter term is used in this ODYSSEY account

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Research study 6

graphs comparing responses of littorines to predation risk following various degrees of "predator conditioning"When a winkle is exposed to risk of predation from crabs, it exhibits anti-predator behaviour and forages less, but how might this effect differ after varying durations of perceived risk and under different levels of risk?  The question has been addressed in other animals, including birds, and is known as the predation-risk, time-allocation hypothesis.  Here, it is tested in laboratory experiments at Simon Fraser University, British Columbia using Littorina spp. exposed to temporal variation in perceived predation risk from crabs Cancer productus and M. magister. The selection of test subjects is a good one, for in the field the risk of predation from crabs varies for littorines both spatially and temporally depending on changing tide levels and movement of crabs from one prey patch to another on the shore.  In response to predation risk, Littorina exhibits various anti-predator behaviours, including leaving the water, withdrawing into shells, and hiding in crevices.  Each of these reduces potential foraging time. In laboratory experiments the researchers first "pre-condition" individual Littorina to caged crabs for differing lengths of time (this equates to differing levels of “perceived risk”), then record their foraging time in both high-risk and low-risk situations. A snail pre-conditioned to a "perceived high risk" is exposed for most of the time to the scent of a crab (i.e., high risk), punctuated by a short period of no crab scent (i.e., low risk). A snail pre-conditioned to "perceived low risk" is treated to the opposite regime. Different regimes yield test subjects with graded levels of perceived risk. Each snail is then exposed to either a crab in a cage (= a high predation-risk situation) or to no crab in a cage (= a low predation-risk situation), and its movements monitored. The degree of a snail's movement during this treatment is equated to potential foraging time.

The experimental design is complex, as is the idea, but the results seem straightforward. They show that during high-risk periods a significantly greater number of snails forage as time at a perceived high risk increases (see upper graph). During low-risk periods, however, no significant relationship exists between number of snails foraging and time of perceived high risk, although this would have been predicted as well by the hypothesis (lower graph). The authors consider the possibility of confounding effect of habituation but, if present, it would be seen in the “low risk” part of the experiments and it isn’t.  The authors note that their study provides the first empirical support for the idea that foraging will occupy a larger proportion of high-risk periods as the proportion of time subjected to high predation-risk increases.  In view of this, the authors caution that the commonly used protocol of exposing foragers to a single pulse of heightened risk may tend to overestimate true investment in anti-predator behaviour.  Hamilton & Heithaus 2001 Proc Roy Soc Lond: Biol Sci 268: 2585.

NOTE  snails used are mainly a mix of L. scutulata and L. sitkana, but possibly also included are some L. plena and L. subrotundata

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Research study 7

schematic showing choice chamber used in tests of littorinid snails Littorina scutulata for avoidance of predator-scented waterphotograph of grapsid crab Hemigrapsus nudusWater-borne chemical cues from potential predators are known to induce avoidance behaviour in many different gastropod species, including littorines. Laboratory studies at the Bamfield Marine Sciences Centre, British Columbia using a 2-choice flow-preference device suggest that past “chemical” experience with predatory crabs Hemigrapus nudus in the field will influence subsequent behaviour of a prey snail Littorina scutulata. Thus, snails from a site where H. nudus is abundant tend to avoid water containing chemical cues from the predator, but snails from a site lacking the predator tend not to. The first data set is on the first line of the table below, showing a significant 21:9 split between control and predator sides of the test chamber, respectively. The second data set is on the second line, showing a non-significant 13:17 split, respectively. More interestingly, the researchers’ results point to a “risk hierarchy” being present, where avoidance increases from control seawater (no risk), to predator cues (low risk), to injured-conspecific cues (intermediate risk), to combined predator/injured-conspecific cues (high risk). Keppel & Scrosati 2004 Anim Behav 68: 915.

NOTE  although the authors use a traditional approach, there are some methodological considerations.  For example, only 6 sets of "runs" are done in the choice device, with no replicates. A control to test for apparatus bias is apparently done, but results not reported.  The choice plate should have been cleaned thoroughly after each table of preference data for snails Littorina scutulata tested in a choice apparatus with scent of predatory crabs in the incoming waterrun and likely was, but this is not mentioned.  The “hierarchy” is determined by comparing magnitude of Chi-square values - not a statistically robust procedure. Scrutiny of the data reveals that if only 10 snails out of 180 tested had made different choices, the Chi-square ranking of 4 of the 6 tests would have been reversed. None of this detracts from the interest of the study but, like a good "stage performance", the audience is left asking for more. Perhaps this is a preliminary report, to be followed by a more complete study.  For example, along with replications already noted, crabs and snails from other sites could be tested.  Better still, could the design be modified to yield parametric statistics, perhaps actual locomotory rates, to permit use of a more robust statistical analysis?

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Research study 8

photograph of crab shelters used in study of shell-mass increasing effect of proximity of predatory crabs Hemigrapsus on littorinid snails Littorina subrotundataphotograph of 3 species of littorinid snails Littorina sitkana, L. subrotundata, and L. scutulata/plenaIn addition to influencing the behaviour of a snail prey, water-borne chemical cues from potential predators are also known to induce defensive changes in shell form and affect overall growth rates.  This is observed in the direct-developing littorine Littorina subrotundata in Barkley Sound, British Columbia where individuals living in predator-rich habitats (shore crabs Hemigrapsus nudus) tend to have more massive shells than ones living in predator-poor habitats.  In support of this idea, laboratory experiments at the Bamfield Marine Science Centre, British Columbia in which L. subrotundata are kept in cages downstream from caged H. nudus feeding on conspecifics, show that the shells of most snails increase significantly in size compared with those of snails kept in the absence of this stimulus.  This suggests that at least some of the variation observed in the field may owe to this adaptive phenotypic plasticity. Dalziel & Boulding 2005 J Exp Mar Biol Ecol 317: 25; for a prediction of results 10yr in the future using modelling methodology see Boulding et al. 2007 J Evol Biol 20: 1976.

NOTE  the 2 species tend not to overlap in their intertidal distributions, so that exposure of Littorina to the crabs is thought by the authors to mimic to some extent an invaston of a novel shell-crushing predator into a marine gastropod population (see Research Study 9 below).  However, to sidestep the issue, the authors construct shelters for the crabs in areas inhabited by L. subrotundata, then compare shell masses of snails collected from areas close to the shelters with ones collected further away (actual distances not specified by the authors)

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Research study 9

graph comparing mortality of 2 species of littorinid snails, the thick-shelled specie Littorina sitkana and the thin-shelled species L. subrotundataWhat happens when a predatory crab becomes newly established in an area previously devoid of predators, and has free licence to prey on a population of thin-shelled littorines?  An interesting theoretical and predictive study on evolution of fitness in a littorinid species is initiated in Barkley Sound, British Columbia by building small concrete shelters1 into which single crabs Hemigrapsus nudus are placed.  The crabs tend to remain in their shelters during high tides but emerge during nighttime low tides to forage on littorines and other food.  The researchers now tether2 individuals of a thick-shelled species Littorina sitkana and a thin-shelled species L. subrotundata at various distances from the shelter and monitor their mortality over a 180-d period.  Both littorinid species deposit eggs that hatch to juveniles without a free-living larval stage, thus leading to the research hypothesis that exposure to predation would select for a population of thicker-shelled individuals. 

Results show, indeed, that thin-shelled L. subrotundata are eaten in preference to thick-shelled L. sitkana (see graph). Moreover, predation is essentially absent at distances more than a few meters from shelters, whether on one side of the shelter or the other. This creates the potential for strong directional selection for increased shell thickness in populations close to the shelters, but does not change selection in those farther away.  To mimic the size increase caused by this selection, the authors now tether large-sized snails, with similar results as before (data not shown here). These data are incorporated into a model that predicts what the mean increase in shell thickness in L. subrotundata would be after 10-20 generations3.   Actual measurements 10y later by the authors of shell thickness in littorines close to the shelters (<1m) and in ones collected further away (>5m) show good agreement to the predicted values.  Furthermore, before-and-after population-density data indicate no significant drop in population numbers as a result of the simulated crab “invasion”.  This suggests that rather than being driven to extinction by the sudden incursion of a predator, rapidly developed defenses of a threatened population could allow its numbers to rebound to the carrying capacity of the habitat. The population would thus survive invasion of a type simulated here.  Boulding et al. 2007 J Evol Biol 20: 1976.

NOTE1  the shelters permit the crabs to live on a wave-exposed beach that would otherwise not have been colonisable. See Research Study 7 for photograph

NOTE2  the tethers are 50cm in length and consist of fine monofilament line attached at the anchor end to a stainless-steel screw fastened into a crevice, and glued at the other end to the apex of a snail (see Research Study 2 above for photograph). Mean shell mass in the first tethering experiment is 20mg for L. sitkana and 13mg for L. subrotundata

NOTE3  studies on other non-west coast littorinid species show that adaptive responses in shell-thickness can develop within 17 generations from being invaded by a predatory shore crab

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Research study 10

drawings of 14 species of snails used in study of retraction depth in snails as an anti-predator strategyElongated shells with lots of space for pulling into would seem a good anti-predator strategy for snails, especially ones co-existing graph comparing retraction distance and shell elongation in 8 genera of west-coast snailswith crab predators that chip away at the aperture edge or with sea-star predators that extrude their stomachs into spaces. Although it is widely assumed that longer shells would allow the occupant to retract more fully, this has never been tested empirically.

Collection and measurement of retraction depths in 14 species of intertidal snails at the Bamfield Marine Sciences Centre, British Columbia show, indeed, that shell length or "shell elongation" is a good predictor of retraction depth across genera. However, within a genus, such as Littorina and Nucella, where there is little variation in shell form, such a relationship is lacking.  In view of their results, the authors discuss the possibility that different environmental factors may affect shell elongation and withdrawal depth independently.  Edgell & Miyashita 2009 J Moll Stud 75: 235.

drawing of snails showing how retraction depth is measured in a living animalNOTE  measurement of  retraction depth is done by first stimulating a snail to withdraw fully by prodding. A blunt needle is then inserted and the retraction distance measured as degree of "angular retraction" (see drawings lower Right). "Shell elongation" then becomes a dimensionless measure expressed as shell length divided by breadth. These measures permit shells of different shapes to be compared

NOTE  the selection includes 8 genera, including 2 west-coast species of Littorina, plus an additional 2 littorines from the Atlantic coast

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Research study 11

graph showing preference of a snail-eating crab Hemigrapsus nudus for thinner-shelled littorinids Littorina subrotundata over thicker-shelled L. sitkanaThe shell-thickening effect of predatory crabs on littorines is well documented, but are these effects continuous throughout the life-span of the predator?  This question is addressed in a series of experiments at the Bamfield Marine Sciences Centre, British Columbia using littorines Littorina subrotundata and L. sitkana, and predatory shore crabs Hemigrapsus nudus.  First, to test whether the crabs actually prefer thinner-shelled prey, 3 size classes of crabs are allowed to feed in the laboratory on a range of different shell-thicknesses of littorines. 

Results show, as expected, that the crabs selectively eat thinner-shelled individuals over thicker-shelled ones.  Interestingly, when thinner-shelled L. subrotundata are presented to a range of sizes of crabs simultaneouly with thicker-shelled L. sitkana, smaller crabs are found to be significantly more “picky” about what they eat than larger crabs (see graph).  Thus, smaller crabs select more of the the thinner-shelled prey species than the thicker-shelled one, while larger crabs tend to eat equal numbers of the two (claws in H. nudus, especially males, grow allometrically, enabling thicker-shelled prey to be more readily crushed as a crab grows).  The investigation is valuable in that instead of comparing individuals of a species from 2 populations that differ in shell thickness, as has been done in previous studies, the authors use individuals from a single population.  This provides more convincing evidence that predation may have been a key selective factor leading to divergence of thicker-shelled forms from thinner-shelled ones, such as appears to have happened on wave-sheltered shores.  Pakes & Boulding 2010 J Evol Biol 23: 1613.

NOTE  interpretation of results in this study is made difficult by the complexity of statistical analyses and also by several figures promised by the publisher to be included in the PDF version, but apparently not in the version available to the UBC library. Selection differential, a fairly important concept in the paper, is explained by the authors as "selection intensity on a trait", but is defined only by a complex set of formulae and a reference to the publication of the author who originated the concept

NOTE  other experiments show that the preference for the thinner-shelled species L. rotundata is not simply a reflection of higher nutritional value or preferred flavour. In choice tests shell-less flesh of the 2 species is consumed equally well by the crabs

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