Amer. Malac. Bull. 31(1): 51–55 (2013)
Do micro snails follow conspecific mucous trails? Experiments with Vallonia excentrica
(Pulmonata: Valloniidae)
Cooper T. Johnson and Timothy A. Pearce
Section of Mollusks, Carnegie Museum of Natural History, 4400 Forbes Avenue, Pittsburgh, Pennsylvania 15213, U.S.A.
Correspondence, Timothy A. Pearce: [email protected]
Abstract. We examined whether the terrestrial micro snail Vallonia excentrica Sterki, 1893 detects and follows conspecific mucous trails. A
trail-layer snail moved on a transparent 5 x 5 cm plastic sheet to establish a mucous trail then was removed. A trail-follower snail of the same
species was allowed to move on the same plastic sheet. Of 30 trials, 24 trail-followers encountered the laid trail. We compared with null models
the distance that the trail-follower trail was coincident with the laid trail, and the turning angle of the trail-follower trail upon meeting the laid
trail, to determine that V. excentrica follows conspecific mucous trails more, and showed sharper turning angles upon meeting a trail, than
expected by the null model.
Key words: trail-following, mucus, null model
Terrestrial gastropods use mucus in a number of ways,
including movement, decreasing desiccation, providing adhesion, defending against predators, as antibacterial defense,
and as a vehicle to transfer pheromones (Denny 1983, 1989,
Cook 1992).
Snails might follow mucous trails in many ways, for example, for homing or finding other individuals. Mucous
trail-following might be a useful way to travel through a
complex world. During movement, land snails lay down
mucus then crawl over it and leave the mucous trail behind.
In addition to simply crawling across the mucus they
laid down, snails can use mucous trails in navigation, for
example, some gastropods follow their own mucous trails
home (Cook 1979a; 1979b). Because snails leave mucous
trails when they move, other individuals that can detect mucous trails could conceivably gain information from the
trails and might react to those trails, such as following or
turning away. Euglandina rosea (Férussac, 1821) followed
fewer conspecific trails and for shorter distances after copulation, suggesting that they use trail-following for finding
mates (Cook 1985). The marine snail Littorina littorea
(Linnaeus, 1758) could detect the age of mucous and followed trails of starved snails shorter distances (Edwards and
Davies 2002).
Many gastropods can detect the polarity (direction the
trail was laid) of mucous trails (Denny 1989), so this information could be used for finding mates (Davis 2007) or by
predatory snails for finding prey. The snail-eating Euglandina
rosea follows trails to find prey, showing preference for wider
mucous trails but otherwise no selection for prey species
(Gerlach 1999). Although some studies have reported that
E. rosea were unable to distinguish polarity of the trails
(e.g., Cook 1985), Davis-Berg (2012) showed they could detect trail polarity, while Clifford et al. (2003) and Shaheen
et al. (2005), studying the chemical nature of trail-following
behavior, reported that they could detect trail polarity of their
own species but not that of prey. Similarly, Mesodon thyroidus
(Say, 1816) was able to detect polarity of conspecific mucous
trails (Davis 2007). Some gastropods can detect and respond
to the age of the trail as well as the physiological state of the
trail-layer and many snails are able to detect or follow interspecific and conspecific mucous trails (Karowe et al. 1993,
Davis 2007). The fact that the snail-eating snails Haplotrema
concavum (Say, 1821) and Euglandina rosea can differentiate
among prey species from their mucous trails suggests the
ability to identify prey type from mucous trails (Pearce and
Gaertner 1996, Holland et al. 2012).
Snails might also follow mucous trails for efficiency.
They might not need to produce as much mucus if they crawl
across the mucus of another individual (Karowe et al. 1993,
Davies and Blackwell 2007) and indeed, individuals following
mucous trails are known to move more quickly than on bare
substrates (Davis 2007). Making mucus accounts for 9–26%
of an individual’s energy budget (Calow 1974, Denny 1980).
Mucus contains a very large portion of water, 90% to more
than 99% water (Livingstone and de Zwaan 1983, Denny
1983) so it can be costly from a moisture perspective for snails
living in dry environments. Following a fresh mucus trail
might help the follower to conserve water.
Even if land snails don’t follow trails, they might detect
trails. When the snails Haplotrema concavum and Mesodon
thyroidus crossed trails, specific tentacle movements indicated that they detected the trails (Pearce and Gaertner 1996,
Davis 2007).
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AMERICAN MALACOLOGICAL BULLETIN
Although mucous trail-following has been studied in
larger land snail species, it has not previously been studied in
micro snails (less than 5 mm diameter). Approximately half
the known species of land snails are smaller than 3 to 4 mm
and we have very little understanding of their basic biology.
While ecological and evolutionary forces might differ between micro snails and large species of gastropods, they also
share many biological needs, so it is possible that smaller species might be expected to follow trails just as larger species do.
Indeed, some micro snail species have low population densities
yet if they need to find each other to mate, mucous trailfollowing might be very important for facilitating their rendezvous. However, if smaller-sized snails have reduced needs,
such as less need to conserve mucus, then trail-following
might not be as prevalent in micro snails.
We examined whether the micro-snail Vallonia excentrica Sterki, 1893 detects and follows conspecific mucous
trails. This flat-spired species is small, being about 2.5–3 mm
diameter (Pilsbry 1948, Gerber 1996).
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31 1 2013
trials in those roles is exceedingly small, and even if the same
pair in the same roles had been used in one trial, our conclusion would be the same.
We defined trail-following to be when the test subject’s trail
was within 2 mm of the trail-layer’s trail. If the follower trail
crossed the laid trail more than once, we scored the total
trail distance within 2 mm, i.e., the sum of all trail coincidences.
As a surrogate to examine whether snails detected mucous trails, we scored turning angle, as the deviation from
previous direction of movement, at the point where the test
subject met the laid trail. For example, with this measure that
could vary from 0 to 180°, a snail that continued without deviation would score 0°, while one that deviated 30° from its
previous direction, either to the left or right, would score 30°.
While we recognize the possibility that a snail might detect a
trail without responding, if a snail turning angle is greater
than expected by chance, that would be evidence that the
snail detected the trail.
MATERIALS AND METHODS
Snails used in the trail-following experiments were 20
Vallonia excentrica (deposited at Carnegie Museum of Natural History, CM 118703). They were collected from the north
side of Canfield, Ohio (41.06°N, 80.80°W) on 22 January 2011.
The snails were kept together in containers until testing.
All trials were run under a clear glass cover to minimize
air currents and to maintain humidity. To determine the behavioral response of snails to conspecific mucous trails, we
placed one individual (trail-layer) on a 5 x 5 cm plastic sheet
cut from a larger plastic transparency sheet (Avery brand).
Plastic sheets were placed on top of a moist paper towel.
The trail-layer snail was allowed to move freely until it
crawled off the sheet. The mucous trail was visualized temporarily with condensation from breath (which did not condense on the mucous trail) on the plastic sheet. A second snail
(trail-follower) was placed on the plastic sheet facing the trail
and allowed to move freely until it crawled off the plastic
sheet or nearly so. Then the trails were visualized with condensation from breath and the trails traced with a marking
pen, a different color for the trail-layer and the trail-follower.
We did not note directions that the trails were laid, although
in cases in which the snail crawled off the sheet, the end could
be inferred.
Individual trail-layer and trail-follower snails were selected arbitrarily as pairs with replacement from a common
container of 20 individuals. With 30 trials total, some individuals participated more than once. In only 24 of those trials
did the trail-follower encounter the laid trail. The chance that
the same trail-layer and trail-follower were used in subsequent
Figure 1. Examples of mucous trail interactions in Vallonia excentrica. A, trail-crossing but not trail-following. B, trail-following.
Solid line shows route of trail-layer; dashed line shows route of trailfollower.
MUCOUS TRAIL-FOLLOWING IN MICRO-SNAIL VALLONIA EXCENTRICA
Null model
To determine whether a test subject followed an existing
mucous trail, or responded to a trail by turning, we first needed to determine the frequencies of trail-following and turning
that would be expected under a random (null) model. To
generate a null distribution of responses, we used a modification of the coincidence index of Townsend (1974). We superimposed mucous trails on plastic sheets from individuals
moving in the absence of other mucous trails (i.e., we superimposed two trail-layer snails’ trails). We designated the snail
on one plastic sheet the trail-layer and the other one the trailfollower and then scored the distance each superimposed
“encounter” would have followed within 2 mm, and the turning angle where the trails would have crossed had they actually been on the same plastic sheet. We superimposed each
trail-layer trail 7 or 8 times and each trail-follower 7 or 8 times
with no two individuals ever used together twice. We scored
113 superimpositions, of which 80 actually crossed. We then
used the chi-squared (χ2) test to compare observed response
frequencies to those predicted by the null distribution. We
considered coinciding distances of < 7 mm to indicate crossing of the trail but not actual trail-following (we scored
coincidence as being within 2 mm of the laid trail), and distances ≥ 8 mm or greater to indicate trail-following. The
width of the trails varied from 0.4 to 0.5 mm. The foot length
53
in motion varied from less than one shell width to slightly
more than one shell width, up to about 3 mm long, similar to
what has been shown for Vallonia costata (Müller, 1774)
(Burch and Jung 1988). Trail-following of 8 mm would be
coincident 16 to 20 times the trail width and nearly three
times the foot length. These two categories of trail-following
distances also yielded expected values for the χ2 test greater
than 5.
RESULTS
In 24 of 30 trials, Vallonia excentrica came within 2 mm
of the laid trail. The trail-follower was within 2 mm of the laid
trail for 8 mm or more in seven trials, and 7 mm or less in 17
trials (e.g., Fig. 1.). They followed mucous trails more often
than expected by the null model (distances < 7 mm vs. 8–28
mm, χ2 = 12.5, d.f. = 1, P < 0.001) (Fig. 2).
Vallonia excentrica, upon crossing trails, went straight
less frequently and had sharper turning angles more frequently than expected by the null model (angles 0°, 10–40°,
50–90°, χ2 = 8.0, d.f. 2, 0.025 > P > 0.01) (Fig. 3).
Of 20 snails that turned when they encountered other
snail mucous trails, 13 turned left and 7 turned right. By
chance, one would expect 50% to go either way, and indeed,
Figure 2. Distance the trail-follower Vallonia excentrica crawled within 2 mm of an existing conspecific mucous trail, versus the expected null
distance.
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AMERICAN MALACOLOGICAL BULLETIN
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Figure 3. Turning angle of Vallonia excentrica upon encountering a laid trail, versus the expected null angle.
of the 56 null model encounters, 28 turned left and 28 turned
right. However, the observed turning direction did not differ
from random (χ2 = 1.8, 0.5 > P > 0.1). Similarly, the angle of
approach to a laid trail had no significant effect on the direction of turning by the trail-follower (χ2 = 0.2, P > 0.5).
DISCUSSION
Vallonia excentrica detects and follows conspecific mucous trails more, and shows sharper turning angles upon
meeting a trail, than expected by chance. The trail-following
is especially clear in the six individuals who followed trails for
distances of 10–28 mm.
The trail detection and following by the micro-snail Vallonia excentrica is similar to reports of trail-following of larger
snail species. The ability to detect and follow mucous trails
might be a general phenomenon of land snails regardless of
their size, implying that the ecological and evolutionary forces acting on snails as they change sizes might not alter their
abilities to detect mucous trails.
For micro-snails that are scarce, finding mates might be
facilitated by following mucous trails. However, there is some
question whether Vallonia Risso, 1826 species and other
small hermaphroditic snails actually mate to reproduce or
whether they reproduce through self-fertilization. Many
individuals lack a penis in many species of Vallonia, so
they are likely to reproduce by self-fertilization. However,
at least some individuals in some Vallonia costata (Giusti and
Manganelli 1986) and V. excentrica (Gerber 1996: 27–29)
populations have a penis, which would allow outcrossing. Although where they occur, V. excentrica are common, following mucous trails could be helpful for finding mates.
Some aspects of trail-following remain unknown in micro snails. We do not know whether they home, and if they
do, whether they use mucus in the process. The mucus of
larger snail species contains pheromones that can be used
for communication; it is likely that smaller snails use pheromones in a similar way, but we don’t know. Larger species
conserve mucus by following pre-produced mucous trails
(Davies and Blackwell 2007), but we do not know whether
small snails benefit in this way. We don’t know whether the
proportion of a micro snail’s energy budget required for
mucus production is similar to that of larger snails. We also
don’t know whether the composition of micro snail’s mucus differs from that of a larger snail. Since we haphazardly
but not systematically rotated the arena among trials, we
did not control for the possibility of magnetic orientation
(Wang et al. 2004), so we cannot address whether these micro snails can detect magnetic north. We don’t know whether they can detect trail polarity. Future research could
address these questions.
MUCOUS TRAIL-FOLLOWING IN MICRO-SNAIL VALLONIA EXCENTRICA
ACKNOWLEDGMENTS
We are grateful to Joy M. Johnson and Scott W. Johnson
for help with transportation and providing space for the
experiments. Mary Johnson and Linda Motosko provided
access to snail collecting areas. Candace Haski provided guidance and encouragement. Amanda Zimmerman and Fabio
Moretzsohn assisted with production of the figures. Two
anonymous reviewers and Fabio Moretzsohn provided helpful comments that improved the manuscript.
LITERATURE CITED
Burch, J. B. and Y. Jung. 1988. Land snails of the University of
Michigan Biological Station area. Walkerana 1: 1–177.
Calow, P. 1974. Some observations on the locomotory strategies and
their metabolic effects in two species of freshwater gastropods,
Ancylus fluviatilis Müll. and Planorbis contortus Linn. Oecologia
(Berlin) 16: 149–161.
Clifford, K. T., L. Gross, K. Johnson, K. J. Martin, N. Shaheen, and
M. A. Harrington. 2003. Slime-trail tracking in the predatory
snail, Euglandina rosea. Behavioral Neuroscience 117: 1086–
1095.
Cook, A. 1979a. Homing in the Gastropoda. Malacologia 18: 315–
318.
Cook, A. 1979b. Homing by the slug Limax pseudoflavus. Animal
Behaviour 27: 545–552.
Cook, A. 1985. Functional aspects of trail following by the carnivorous snail Euglandina rosea. Malacologia 26: 173–181.
Cook, A. 1992. The function of trail following in the pulmonate slug
Limax pseudoflavus. Animal Behaviour 43: 813–821.
Davies, M. S. and J. Blackwell. 2007. Energy saving through trail following in a marine snail. Proceedings of the Royal Society B, Biological Sciences 274: 1233–1236.
Davis, E. C. 2007. Investigation in the laboratory of mucous trail
detection in the terrestrial pulmonate snail Mesodon thyroidus
(Say, 1817) (Mollusca: Gastropoda: Polygyridae). American
Malacological Bulletin 22: 157–164.
Davis-Berg, E. C. 2012. The predatory snail Euglandina rosea successfully follows mucous trails of both native and non-native
prey snails. Invertebrate Biology 131: 1–10.
Denny, M. W. 1980. Locomotion: The cost of gastropod crawling.
Science, 208: 1288–1290.
Denny, M. W. 1983. Molecular biomechanics of molluscan mucous secretions. In: P. W. Hochachka, ed., The Mollusca, Vol. l,
Metabolic Biochemistry and Molecular Biomechanics. Academic
Press, New York. Pp. 431–465.
Denny, M. W. 1989. Invertebrate mucous secretions: Functional alternatives to vertebrate paradigms. Symposia of the Society for
Experimental Biology 43: 337–366.
Edwards, M. and M. S. Davies. 2002. Functional and ecological
aspects of the mucus trails of the intertidal prosobranch gastropod Littorina littorea. Marine Ecology Progress Series 239:
129–137.
55
Gerber, J. 1996. Revision der Gattung Vallonia Risso 1826 (Mollusca: Gastropoda: Valloniidae). Schriften zur Malakozoologie
8: 1–227 [in German].
Gerlach, J. 1999. The ecology of western Indian Ocean carnivorous
land snails. Phelsuma 7: 14–24.
Giusti, F. and G. Manganelli. 1986. “Helix” sororcula Benoit 1859
and its relationships to the genera Vallonia Risso and Planogyra
Morse (Pulmonata: Pupilloidea). Archiv für Molluskenkunde
116: 157–181.
Holland, B. S., T. Chock, A. Lee, and S. Sugiura. 2012. Tracking behavior in the snail, Euglandina rosea: First evidence of preference for endemic vs. biocontrol target pest species in Hawaii.
American Malacological Bulletin 30: 153–157.
Karowe, D. N., T. A. Pearce, and W. R. Spaller. 1993. Chemical communication in freshwater snails: Behavioral responses of Physa
parkeri to mucous trails of P. parkeri (Gastropoda: Pulmonata)
and Campeloma decisum (Gastropoda: Prosobranchia). Malacological Review 26: 9–14.
Livingstone, D. R. and A. de Zwaan. 1983. Carbohydrate metabolism
of gastropods. In: P. W. Hochachka, ed., The Mollusca, Vol. l,
Metabolic Biochemistry and Molecular Biomechanics. Academic
Press, New York. Pp. 177–242.
Pearce, T. A. and A. Gaertner. 1996. Optimal foraging and mucustrail following in the carnivorous land snail Haplotrema concavum (Gastropoda: Pulmonata). Malacological Review 29:
85–99.
Pilsbry, H. A. 1948. Land Mollusca of North America (North of
Mexico). Academy of Natural Sciences of Philadelphia, Monograph
3 2: i–xlvii, 521–1113.
Shaheen, N., K. Patel, P. Patel, M. Moore, and M. A. Harrington.
2005. A predatory snail distinguishes between conspecific and
heterospecific snails and trails based on chemical cues in slime.
Animal Behaviour 70: 1067–1077.
Townsend, C. R. 1974. Mucus trail following by the snail Biomphalaria glabrata Say. Animal Behaviour 22: 170–177.
Wang, J. H., S. D. Cain, and K. J. Lohmann. 2004. Identifiable neurons inhibited by Earth-strength magnetic stimuli in the mollusc Tritonia diomedea. Journal of Experimental Biology 207:
1043–1049.
Submitted: 30 June 2012; accepted: 13 November 2012;
final revisions received: 7 December 2012