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183 Table 7
a
Mark-recapture experiment 2
2
Source of variation MS MS 3 10
Df F
P Blocks
0.146 11.306 3 3
3.569 3.557 0.031 0.032
Snail species Sp 0.088 4.857
1 1 2.159 1.528
0.157 0.230 Snail origin So
4.366 164.868 1 1
106.859 51.867 , 0.0001 , 0.0001
Predator treatment P 0.684 9.034
1 1 16.752 2.842
, 0.001 0.107 P 3 Sp
– 11.057 – 1
– 3.479 NS 0.076
Error 0.041 3.179
21 21
a
Results of the randomized block factorial ANOVAs done on the shoreward-orientation index and net-shoreward movement of snails shoreward-orientation index net-shoreward movement. Small Littorina
sitkana and L. scutulata from the high- and low-intertidal levels were released at the low-intertidal level after being exposed to predation cues or control conditions see Section 2 for ¯ 24 h. Non-significant P . 0.10
interaction terms are not shown.
conditions P , 0.05, but L. scutulata snails were recovered at similar distances from their release point whether tested in the predator or the control treatment P . 0.05.
4. Discussion
Our field study strongly supports the hypothesis that Littorina sitkana and L. scutulata display shoreward movements in response to the risk of predation from low-intertidal
and subtidal predators. In particular, our two mark-recapture experiments indicate that the precision and or magnitude of such movements are adjusted to local conditions of
predation risk. To our knowledge, these results provide the first experimental evidence that antipredator behavior may contribute to the intertidal distribution of littorinids.
However, another ubiquitous snail of the western coast of north America, Tegula funebralis, also responds to the risk of predation by seeking higher and safer intertidal
areas Fawcett, 1984, and salt-marsh snails, Littorina irrorata, migrate up cordgrass stems during tidal inundation to avoid predation by the crab Callinectes sapidus
Warren, 1985; Vaughn and Fisher, 1988. Similarly, several species of Pacific limpets respond to predatory gastropods and seastars by fleeing shoreward or clamping tightly to
their home scars Phillips, 1976; Iwasaki, 1993.
4.1. Spatial variation in predation risk On wave-sheltered shores of the northeastern Pacific, L. sitkana and L. scutulata are
uncommon at low-intertidal levels, despite the fact that food abundance and physical conditions contribute to growth conditions being better in such areas e.g., McCormack,
1982; McQuaid, 1982, 1983; Behrens Yamada and Mansour, 1987. Recent studies indicate that predation by large crabs, and perhaps fishes, prevents L. sitkana from
exploiting lower, and more-profitable, intertidal levels McCormack, 1982; Behrens Yamada and Boulding, 1996. Our study supports this conclusion, and further dem-
onstrates that L. scutulata is also more susceptible to predators at low-intertidal than at high-intertidal levels. In the northern part of our study area, where snail mortality was
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highest during both the tethering experiment and the first mark-recapture experiment, there were numerous boulders below the 1-m level, which served as refuges to many
Cancer productus, Lophopanopeus bellus, and Hemigrapsus oregonensis. These three species of crabs prey on snails, although H. oregonensis mainly feeds on algae and is
somewhat ill-equipped to break the shell of adult snails Behrens Yamada and Boulding, 1998, and references therein. C. productus and L. bellus both could have crushed,
peeled and pulled snails off their tethers, but we believe the former was responsible for most mortality during our study see also Behrens Yamada and Boulding, 1998. C.
productus up to ¯ 20 cm in carapace width are known to migrate into higher intertidal areas when the tide is flooding Robles et al., 1989, and are perhaps more likely than
the much smaller L. bellus maximum carapace width of ¯ 2 cm to have traveled the . 5 m separating the shelters from the tethered snails. We often see C. productus crabs
foraging at our study site when the tide is high, and twice saw a crab eating a tethered snail.
Intertidal habitats are diverse and variable, so it should not be expected that littorinids and other small herbivorous gastropods will always be at greater risk of predation at
lower intertidal levels. For instance, seasonal foraging by shorebirds may occasionally cause predation risk to be greater at high, rather than low, intertidal levels e.g., Gibb,
1956. Also, crabs may be able to establish residence in unusually high intertidal areas where large rocks and fresh-water seepage offer adequate protection against desiccation
Behrens Yamada and Boulding, 1996. Finally, studies that have shown high snail mortality in low-intertidal areas were all done on wave-protected shores McCormack,
1982; Behrens Yamada and Boulding, 1996; this study, where crabs and fishes can forage when the tide covers the low intertidal. In areas that are exposed to the action of
waves and surge, these same animals will be less capable of intertidal foraging e.g., Menge, 1978; Boulding et al., 1999, and wave action may be what limits the lower
distribution of snails McCormack, 1982.
4.2. Littorinid shoreward movements: ultimate factors In wave-sheltered areas of the northeastern Pacific, the lower distribution of littorinids
correlates with levels of predation risk on different shores Behrens Yamada and Boulding, 1996; Rochette, unpubl. data. Although this correlation is likely caused in
part by varying mortality rates on different shores, our study indicates it may also result from the snails’ behavioral response to predation risk.
L. sitkana and L. scutulata snails from the high intertidal low predation risk that were transplanted lower on the shore high predation risk displayed a strong and
consistent tendency to move shoreward, some traveling 10–15 m in 2–3 days to regain their original level. Other studies have similarly found that littorinids tend to move back
homeward when transplanted above or below their normal intertidal position e.g., L. littorea: Gowanloch and Hayes, 1926; Gendron, 1977; L. planaxis and L. scutulata:
Bock and Johnson, 1967; L. sitkana: McCormack, 1982, and predation risk might be responsible for some of these movements e.g., McCormack, 1982.
The hypothesis that shoreward movements displayed by L. sitkana and L. scutulata were antipredator in nature is supported by the fact that snails moved more frequently
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185
and directly shoreward in high-risk parts of the study area mark-recapture experiment 1, and when exposed to the odors of predators feeding on conspecific and heterospecific
snails mark-recapture experiment 2. In the first mark-recapture experiment, better orientation did not translate into greater net-shoreward movement, probably in part
because of substrate heterogeneity; snails released where predation risk was high i.e., north had to negotiate cobbles 2–10 times their size, whereas snails released where
predation risk was low i.e., south were confronted with finer substrate and only a few small cobbles. In the second mark-recapture experiment, where an attempt was made to
control for substrate heterogeneity, net-shoreward movement also increased with predation risk in L. sitkana but not in L. scutulata.
Another result that supports the interpretation that shoreward movements were antipredator in nature is that larger, more vulnerable snails released at low levels during
the first mark-recapture experiment displayed more precise shoreward movements than smaller less vulnerable individuals. Alternatively, one may argue that small snails are
less likely to migrate shoreward because they have poorer locomotory capacities than large individuals, or since they are more susceptible to desiccation aperture area per unit
body mass decreases with size; e.g., McQuaid, 1982. However, even small snails showed an overwhelming tendency to move back shoreward L. sitkana, 94; L.
scutulata, 92, and all small and large snails used during the first mark-recapture experiment had been collected from the same high-intertidal areas 2.5 m. We therefore
believe that a somewhat weaker response to predation risk by small snails accounts for their less-precise shoreward orientation compared to larger, more vulnerable individuals.
The greater vulnerability of larger snails may seem surprising, because decapods generally prefer small-size molluscan prey Juanes, 1992. Several laboratory studies
indicate that crabs selectively feed on small littorinids when simultaneously offered different-sized snails Elner and Raffaelli, 1980; Behrens Yamada and Boulding, 1998,
whereas others show the reverse pattern Behrens Yamada et al., 1998. This dis- crepancy between studies is likely partly due to differences in the size and or species of
predators and prey used. Field studies, on the other hand, have consistently found larger littorinids to be at greater risk of predation than smaller individuals McCormack, 1982;
Behrens Yamada and Boulding, 1996; Boulding et al., 1999; this study.
4.3. Littorinid shoreward movements: proximate factors At the proximate level, the tendency of L. sitkana and L. scutulata to move shoreward
upon transplantation to low-intertidal areas could have been caused by differences in habitat characteristics between the collection and release sites, such as immersion time,
slope, light, and the presence of other animals or plants see Petraitis, 1982, and references therein. Furthermore, the movement of snails could have been influenced by
trails left by other snails e.g., Gendron, 1977; Chapman, 1986. However, our results indicate that predation cues also influenced snail behavior; snails moved more directly
shoreward when transplanted to portions of the study site where predatory crabs were more abundant, and when exposed to crabs feeding on other snails. Whereas results of
the first mark-recapture experiment could theoretically have been caused by differences in physical properties between the northern and southern portions of the study site, it
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seems more likely that differences in snail behavior were caused by differences in the relative abundance or activity of predatory crabs in these areas. At any rate, the second
mark-recapture experiment demonstrated unequivocally that snails respond to cues that are indicative of predation risk by displaying better oriented and longer shoreward
movements. This experiment was not designed to determine the cues involved, however, and snails might have responded to predator odors and or to chemicals leaching from
injured snails. There are numerous examples of marine gastropods which chemically detect predators and or injured conspecifics see Ansell, 1969; Feder, 1972; Hadlock,
1980; Kats and Dill, 1998 and references therein. In a recent laboratory study, Behrens Yamada et al. 1998 concluded that odors of conspecific snails being killed and
consumed by crabs elicited a strong response in L. sitkana, inducing snails to crawl to the top of the cages or to hide in crevices, but that snails did not respond to crab odors
alone. However, some studies have reported that littorinids can chemically detect their predators asteroids: Feder, 1963; decapods: Duval et al., 1994.
Several studies have warned against the potential effect of ‘disturbance’ e.g., collecting, manipulating, and marking on the movement patterns of snails see Petraitis,
1982; Chapman, 1986, 1999. Because all our snails were removed from their habitat and marked in the laboratory, we cannot assess the extent to which this disturbance
affected their behavior. However, disturbance is unlikely to have contributed to our study’s main conclusions, namely that snails respond to predation risk by displaying
oriented movements towards higher and safer intertidal areas. First, high-intertidal snails that were translocated to the high intertidal disturbed 1 moved laterally almost always
moved randomly, whereas high-intertidal snails released in the low intertidal disturbed 1 moved laterally 1 transplanted invariably moved shoreward. Note that the
random movements of snails translocated to the high intertidal did not result from a lack of opportunity to move further upward, as snails of both species did occur above the
high-intertidal release points. Therefore, transplantation to the lower-intertidal level, and not disturbance, is likely responsible for the directionality of snail movement. Similarly,
snails exposed to ‘high predation risk’ conditions moved more directly shoreward than snails exposed to ‘low predation risk’ conditions, even though ‘experimental’ and
‘control’ snails had been subjected to the same disturbances.
4.4. Behavioral differences between low- and high-intertidal littorinids Biotic e.g., food, predators and abiotic e.g., heat stress and desiccation conditions
in coastal marine environments vary markedly with intertidal height, causing conspicu- ous zonation patterns of plants and animals. Despite this steep gradient in environmental
conditions, littorinids often display relatively broad vertical distributions; at our study site, L. sitkana and L. scutulata were both found from the 1.0-m tidal mark to the
supralittoral fringe ¯ 3.5 m. We do not know to what extent L. sitkana and L. scutulata move between low- and high-intertidal areas over their lifetime. In the North Atlantic,
along the western coast of Spain, two ecotypes of the ovoviviparous snail L. saxatilis appear to have evolved in response to the varying selective pressures which occur at
different heights in the intertidal zone. These low- and high-shore ecotypes show extensive variation in phenotype, including shell and radula morphology, growth rates,
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187
physiological resistance to osmotic stress, and mating behavior, and much of this variation is under genetic control Johannesson et al., 1993; Johannesson et al., 1995;
´ Rolan-Alvarez et al., 1996; Johannesson et al., 1997. The maintenance of these
differences appears due to microhabitat preferences, assortative mating and reduced ´
viability of hybrids outside the contact zone Johannesson et al., 1995; Rolan-Alvarez et al., 1997. We are currently doing long-term field experiments and surveys to evaluate
the natural movement patterns horizontal and vertical of L. sitkana and L. scutulata, and the contribution of environmental and genetic factors to phenotypic differences
between high- and low-intertidal snails.
4.5. Interspecific variation in snail vulnerability, distribution and behavior The demographic and behavioral patterns of L. sitkana and L. scutulata showed many
similarities, as emphasized throughout most of our discussion, but also a few interesting differences. For instance, the thinner-shelled L. sitkana was more frequently killed by
shell-crushing predators than L. scutulata during our tethering experiment, more obviously so at the high species factor, P 5 0.022 than the low species factor,
P 5 0.30 intertidal level Fig. 2a,b; low mortality rates in the high intertidal might explain why the interaction between snail species and intertidal height was not
significant. In a recent study, Boulding et al. 1999 similarly recorded greater mortality rates of L. sitkana compared to similar size i.e., shell width L. scutulata when they
tethered snails above Fucus in the high intertidal. One potential explanation for this interaction between intertidal height and snail species is that the thicker-shelled L.
scutulata may better resist attacks from small high-intertidal crabs e.g., H. oregonensis and H. nudus than L. sitkana, but may be preyed upon as easily as its congener by
bigger crabs living in lower-intertidal areas e.g., juvenile and adult C. productus. This hypothesis warrants further investigation, as it suggests that L. scutulata may incur a
greater increase in survivorship than L. sitkana by exploiting higher-intertidal areas. Interestingly, the distribution of L. scutulata appeared more strongly skewed towards the
high intertidal than that of L. sitkana see Fig. 1. In particular, L. scutulata was less abundant than L. sitkana in the low intertidal i.e., 1.0-m level, even though it was 3.5
times more abundant overall than its congener at our study site.
We also found behavioral differences between L. sitkana and L. scutulata. During the first mark-recapture experiment, high-origin L. sitkana released in the low intertidal
moved greater distances shoreward than L. scutulata, both in the northern and in the southern parts of the study area. It is unlikely that these differences were simply the
result of interspecific differences in locomotory capacities e.g., foot size, because L. scutulata also tended to be less well oriented than L. sitkana P 5 0.087, and because
large L. scutulata did not move any further than small heterospecific snails P 5 0.94. Furthermore, during the second mark-recapture experiment, high-origin L. sitkana
moved more directly shoreward when previously exposed to foraging crabs than when held in control conditions, but high-origin L. scutulata were seemingly unaffected by the
predator treatment.
At first, one might be tempted to attribute the stronger shoreward movements and antipredator responses of high-intertidal L. sitkana versus L. scutulata to its greater
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vulnerability. However, that would be ignoring the fact that interspecific differences in snail mortality were only evident at the high-intertidal level see above, and those
results suggest that the adaptive value of crawling shoreward, in terms of reduced probability of mortality, would actually be greater for L. scutulata than for L. sitkana.
An alternative hypothesis for this interspecific difference in behavior is that L. sitkana is better adapted to the high-risk conditions of our study site than L. scutulata. Whereas L.
sitkana recruits are born in the same habitat where their progenitors lived, L. scutulata embryos and larvae spend more than 20 days Buckland-Nicks et al., 1973 in the
plankton and are thus likely to settle at great distances from the adults. Consequently, L. scutulata should experience higher levels of gene flow between populations than L.
sitkana, and should therefore display less genetic differentiation over small geographic distances e.g., Behrens Yamada, 1989. This pattern has been reported for several
ecologically similar species of prosobranch gastropods in which early-life stages differ in dispersal potential see references in De Wolf et al., 1998. Note, however, that greater
genetic differentiation among populations will not necessarily translate into greater phenotypic variation, because species with higher dispersal potential e.g., those
possessing a pelagic larvae may have evolved more labile phenotypes which can be adjusted to local conditions prevailing during the individual’s development e.g.,
Parsons, 1997, 1998. We are currently investigating the extent and mechanisms i.e., genetic adaptation versus phenotypic plasticity of phenotypic differentiation among
populations of L. sitkana and L. scutulata.
5. Summary and future research
