Research study 3

Research study 4

Larvae of black turban snails Chlorostoma funebralis settle in the higher regions of the intertidal zone and live there for several years before migrating downwards to lower areas.   Here, they contact sea-star predators, most notably ochre stars Pisaster ochraceus.   Defensive response by Chlorostoma to touch or close presence of predatory sea stars is sideways twisting followed by quick escape crawling, or releasing their hold on rocks and dropping to the sea bottom.  Feder 1963 Ecology 44: 505; Paine 1969 Ecology 50: 950.

Escape responses of Chlorostoma funebralis, involving shell-twisting and sometimes direct crawling up, onto, and over a potential predator, are graded depending upon whether or not the test species is a known predator.  Physical contact with several sea-star and whelk species in Pacific Grove, California elicits strong escape responses. 

The only test species eliciting no, or only weak, responses in Chlorostoma are the bat star Asterina miniata and leather star Dermasterias imbricata. The first is an omnivorous scavenger, lives on muddy-bottom habitats, and rarely, if ever, encounters C. funebralis. The second, however, Dermasterias, is predatory on a wide variety of invertebrates including sea urchins, sea stars, and spongest.  Its lack of effect on Tegula is therefore somewhat surprising and may warrent further investigation.  Yarnall 1964 Veliger 6 (Suppl): 56.

NOTE  tests involve touching a tube foot (sea star) or piece of sole of foot (whelk) to Chlorostoma, then grading the intensity of response.  The author uses 4 categories of response in the study (strong, medium, weak, and absent) but, for economy of space, only percentages of Chlorostoma individuals (N = 50 for each pairing) showing strong responses are reported here.   “Touch” controls with a clean steel probe give an average of 12% strong responses out of 450 trials (50 with each test species)

Results from various extirpation experiments at Hopkins Marine Station, California using black-turban snails Chlorostoma funebralis suggest that the osphradium, located within the mantle cavity near to the ctenidium (see illustration), is the main chemoreceptive organ. Because of its location in the forward mantle cavity it would provide the first warning of upstream presence of, in this case, a predatory sea star Pisaster ochraceus. Other sensory devices, including tentacles, and mantle and foot edges, seem to be mainly chemotactile in function. There is some suggestion that stimulation of the osphradium enhances sensitivity of these other receptor organs. On stimulation the immediate response of a snail is to run. Burke 1963-64 The Veliger 6 (Suppl.): 18. Drawing of dissected whelk courtesy Richard Fox, Lander University, South Carolina.

NOTE the author does not include mock operations as controls in some of the experiments, so accepting the results includes accepting that trauma from incisions and removal of body parts has not significantly affected subsequent behaviour

Of the species of Chlorostoma (Tegula) inhabiting rocky-shore and kelp-forest regions along the west coast two, C. (Tegula) funebralis and C.(Tegula) brunnea, live in mid-low/shallow subtidal regions where they regularly contact predatory sea stars Pisaster spp. and Pycnopodia helianthoides.

Two other species, Promartynia (Tegula) pulligo and C. (Tegula) montereyi, live primarily on the bottom portions of Macrocystis spp. and other large subtidal kelps and have less contact with Pisaster spp.  On some central California shores, C. (Tegula) brunnea, if not on the sea bottom, may be found on the tops of large kelps where it also has no contact with Pisaster. Lowry et al. 1974 Biol Bull 147: 386; Riedman et al. 1981 Veliger 24: 97.

At least 4 trochid-snail species co-inhabit beach areas in Santa Catalina Island, California with several sea-star and whelk predators.  Three of these, Chlorostoma aureotincta, Norrisia norrisi, and Pomaulax undosa will run from contact with Pisaster giganteus and other sea-star and whelk predators, but the fourth, Chlorostoma eiseni, stays put.  The authors credit this behaviour with a 65% thicker shell and less digestible tissues in C. eiseni as compared with its congenitor C. aureotincta. 

If juvenile Pisaster are fed shell-less tissues of the two Chlorostoma species, growth is similar, suggesting that the species do not differ in nutritional value (Left-hand histogram).  However, growth of juvenile sea stars on intact snails is significantly slower on a diet of C. eiseni than C. aureotincta, possibly owing to the longer time taken for sea stars to digest the tissues of the former (Right-hand histogram).  In laboratory comparisons of digestibility, tissues of aureotincta are digested 3-fold quicker than those of eiseni.  Moreover, the overall time for Pisaster to eat a single C. eiseni in the lab is 11h versus 4h for C. aureotincta.  Schmitt 1981 J Exp Mar Biol Ecol 54: 251.

NOTE  growth data for another asteroid species, not shown here, is similar to those presented for Pisaster giganteus

NOTE  the tests use 50% H₂SO₄ over 30min at 40^oC

The snail Norrisia norrisi in Santa Catalina, California likes to inhabit large kelps¹. In its lofty kelp habitat it has about a 4% chance each day of being dislodged. If this happens and it crawls on the sea bottom, it suffers 10-fold greater mortality than it would in the kelp habitat.  One of its benthic predators is the octopus Octopus bimaculatus, which drills² and eats it.  If the octopus fails to drill completely through the shell of Norrisia, which happens quite often, the drill holes attract settling larvae of the barnacle Megabalanus californicus³ and the shell may become heavily fouled with these barnacles.  About 30% of the snails have barnacles growing on them.  If heavily fouled the snails have difficulty crawling back to the relative safety of the kelps.  When they attain their perches, they are dislodged twice as frequently and remain longer on the sea bottom than unfouled snails.  On the sea bottom, especially with their load of barnacles, they run the risk of being captured and consumed by benthic predators, such as octopuses, lobsters, and whelks. The author's measurements on locomotory rates indicate that moderately to heavily fouled snails are at least 25% slower than unfouled ones.  Moreover, data from laboratory tests on susceptibility of Norrisia to sea-star predators show that fouled snails have an 8-fold greater risk of being eaten than unfouled ones.  It’s double jeopardy: if the octopuses fail to kill Norrisia outright, their drill-holes become fouled with barnacles and indirectly lead to greater risk of death from other sources.  Schmitt et al. 1983 J Exp Mar Biol Ecol 69: 267.

NOTE¹  the kelps are Macrocystis pyrifera and Eisenia arborea.  Counts by the researchers show that 97% of N. norrisi inhabit these kelps, while the remainder live on the sea bottom

NOTE² the authors report that of 269 live Norrisia examined, 29% have been drilled by an octopus, and many of these are also encrusted with barnacles.  Why the octopuses fail so often to kill a snail is not known

NOTE³ this barnacle is virtually the only epibiont found on Norrisia in the study area

The upward crawling behaviour of Chlorostoma funebralis in the presence of potential predators can greatly influence the species’ lower limit of distribution.  In southern California the lower limits of C. funebralis are generally higher than in northern California, possibly because of the greater abundance of predators in the southern regions.  Predators in this area include ochre stars Pisaster ochraceus, several crabs Cancer spp., and octopuses Octopus bimaculoides and O. bimaculatus – the last two of which are lacking at northern sites.  Predator intensity at each site is scored by direct quadrat counts and observation of transient predators (e.g., octopuses and crabs), and by indirect counts using the presence of characteristically crushed and drilled shells as indicative of crab kills and octopus kills, respectively.  Note in the graph on the Left that as the “predator score” increases (i.e., greater predat-ory intensity) at the 13 sites studied, so the lower limit of distribution Chlorostoma rises. 

Reciprocal translocations of snails from one location to another, in some cases to different heights on the shore, provide supportive data.  For example, snails from San Luis Obispo and San Mateo, released on the shore at San Luis Obispo, move quickly upwards, regardless of whether they are released low on the shore or high on the shore (see graph lower Left). Results for the reciprocal transplant, from both locations and released on the shore at San Mateo, are shown in the graph at the lower Right. Note that snails from the high "predator-score" location (San Luis Obispo) consistently move higher on the shore after translocation, in accordance with the author's predictions.

Also noteworthy is the generally lower heights attained by the two sets of funebralis in the translocation to San Mateo (graph on Right). The “predator score” is lower at the San Mateo site than at the more southerly San Luis Obispo site (4 vs. 6, respectively).  This general pattern is repeated in many other translocations.  The author proposes, based on these field experiments and on laboratory observations that the snails may be responding to chemical exudations from the predators.

The explanation for snails translocated from the southern population (San Luis Obispo) always ending up higher on the shore than snails from the northern population (San Mateo) may owe to long-term differences in the intensity of predation by octopuses, which are much rarer in the intertidal zone in northern California.  However, an alternative explanation also provided by the author might be that acclimation to cooler, moister conditions at the more northern site (San Mateo) could keep the northern snails lower on the shore when translocated to the southern site.  This may also explain why the southern snails (San Luis Obispo) move higher on the shore than the northern snails (San Mateo) when translocated to the more northerly site.  Finally, funebralis generally is larger in the northerly populations than in the southerly ones, and larger snails are usually found higher on the shore than smaller ones.  Fawcett 1984 Ecology 65: 1214; photo of Octopus bimaculoides courtesy of Roger Hanlon, Woods Hole, Massachusetts.

NOTE  there are 12 sites in California ranging from San Diego County in the south to Sonoma County in the north, and one site at Pt. Anderson in Washington

NOTE  in this example, the 2 sites are separated latitudinally by about 300km

Top shells Pomaulax gibberosa in British Columbia often harbour a commensal polynoid worm that sometimes shows itself outside of the snail’s mantle cavity.  Whether the worm comes out to bite at a potential predator, similar to the behaviour of a mutualistic worm in keyhole limpets Diodora aspera, is not known.

In this photo the snail has partially emerged from the
seawater in an aquarium tank. The worm may have come
out to investigate the sudden change in living conditions 0.7X

One doesn’t think of snails as having different behaviours but, just as in “higher” animals, individuals in a snail species will behave differently than other individuals.  One snail, for example, may crawl relatively more quickly than another, or seek a mate and hunt for food or shelter at different times and in different ways than another.  Likewise, predatory sea stars will exhibit their own behavioral variability in activity levels and patterns.  How these variations might interact proximally to mediate predation rates, and ultimately to determine whether the variability is maintained or eliminated in community is examined for snails Chlorostoma funebralis and one of its predators, the ochre star Pisaster ochraceus, by researchers at the University of California, Davis.  The researchers assess behavioral characteristics of each of 37-46 snails (representing a single test batch), enclose them in an outdoor “mesocosm” for 2wk with a single P. ochraceus, and record who gets eaten.  Eighteen replicates are done.  Results show that the best behavioral correlate for maximum survival of a snail, not surprisingly, is good predator avoidance combined with being large in size.  As would be expected, these effects are mediated by predator behavioral “type”.  Thus, greater predator-avoidance behaviour is favoured with active sea stars, while lesser predator-avoidance behaviour is favoured with inactive sea stars.  The authors note that both trends will tend to favour maintainance of trait variations within the 2 populations.  Pruitt et al. 2012 The Am Nat 179 (2): 217.

NOTE  the authors give a good example of such interactions.  A “bold” snail will benefit from seeking out food in high-risk foraging areas, but does so at the risk of greater predation

One behavioral attribute relating to activity used by the
authors is the extent to which an individual snail
Chlorostoma funebralis will crawl vertically out of
water to escape a predatory ochre star Pisaster ochraceus