/. Moll Stud (1997), 63, 389-399
© The Malacological Society of London 1997
OTHER PAPERS
INTERFERENCE AND RESOURCE COMPETITION IN TWO
LAND SNAILS: ADULTS INHIBIT CONSPECIFIC JUVENILE
GROWTH IN FIELD AND LABORATORY
TIMOTHY A. PEARCE
Museum of Zoology, Mollusk Division, University of Michigan, Ann Arbor, Michigan 48109 USA
(Received 17 July 1995; accepted 11 November 1996)
(Cameron & Carter, 1979; Dan & Bailey, 1982;
Bailey, 1989). Furthermore, intraspecific
Interference and resource competition by adults
crowding can indirectly affect subsequent local
inhibited growth rates of conspecific juveniles of the
population density because it affects adult sizes
land snail species Mesodon thyroidus and Neohelix
(Williamson, Cameron & Carter, 1976; Cook &
albolabris in separate field and laboratory experiCain, 1980; Tattersfield, 1981; Baur, 1988a;b)
ments, but not in laboratory experiments on
and individual growth rates (Oosterhoff, 1977;
Anguispira altemata. In 1 m2 field cages at nearCameron & Carter, 1979; Charrier, 1981;
natural densities under ambient food and water conChevallier, 1982; Dan & Bailey, 1982; Lucarz,
ditions, juvenile M. thyroidus apparently competed
1982; Lucarz & Gomot, 1985; Cook, 1989; Baur
with adults for food or water or both resources, growing more slowly when living with two conspecific
& Baur, 1992), both of which themselves can
adults, but being unaffected by adult presence when
influence fecundity, survival, and activity.
food and water were augmented. Neohelix albolabris
In experiments on land snails in which
juveniles were similarly unaffected in field cages by
researchers
eliminated or controlled density
presence of two adults when food and water were
independent factors such as weather, and denaugmented. In contrast, interference, not resource
sity dependent factors such as disease and precompetition, apparently explained growth inhibition
dation (Oosterhoff, 1977; Cameron & Carter,
in laboratory cages at densities considerably greater
than natural densities, with non-limiting food and
1979; Charrier, 1981; Lazaridou-Dimitriadou &
moisture; both M. thyroidus and N. albolabris juve- Daguzan, 1981; Dan & Bailey, 1982; Lucarz,
niles grew more slowly as conspecific adult number
1982; Carter & Ashdown, 1984; Lucarz &
increased from zero to three.
Gomot, 1985; Cook, 1989; Staikou & Lazaridou-Dimitriadou, 1989; Baur, 1990; Baur and
Baur, 1990; 1992), the decreased performance,
INTRODUCTION
known as crowding effects, experienced by
snails is likely to be due to competition. There
The factors influencing land snail population are two types of competition: resource competisizes, while poorly understood, may include tion (= exploitative competition) in which indiboth density independent factors such as viduals compete directly for a limited resource,
weather and density dependent factors such as and interference competition in which individupredation, disease, and competition. Intraspe- als harm each other while pursuing resources
cific crowding can directly influence local popu- that may or may not be limiting (Krebs, 1994).
lation density of some land snail species
Resource competition, for example competithrough its affect on individual fecundity
tion
for food (Cowie and Cain, 1983; Daguzan
(Yom-Tov, 1972; Wolda & Kreulen, 1973;
and
Verly,
1989) or moisture (personal obserCarter & Ashdown, 1984; Lucarz, 1984;
vation),
is
sufficient
to explain crowding effects
Daguzan & Verly, 1989; Baur, 1990; Baur &
in
some
experiments
on land snails. Although
Baur, 1992), survival (Lazaridou-Dimitriadou
many
workers
report
that food does not seem
& Daguzan, 1981; Dan & Bailey, 1982;
to
be
limiting
to
land
snails (Hunter, 1978;
Reichardt, Raboud, Burla & Baur, 1985; Tilling, 1985; Staikou & Lazaridou-Dimitriadou, Peake, 1978; Cain, 1983), some have found that
1989; Baur & Baur, 1990), and locomotory rates food does appear to be limiting (Butler, 1976;
Williamson, Cameron & Carter, 1977). Moisture strongly influences snail activity (Solem,
Address for correspondence. Dr. Timothy A. Pearce, Delaware
1974; Riddle, 1983; Boag, 1985; Imevbore,
Museum of Nilural History, Box 3937, Wilmington, DE 19807, USA
ABSTRACT
TIMOTHY A. PEARCE
390
1990), and since snails must move to acquire
resources, shortage of moisture might effectively limit food availability, and snails could
compete for moist resting sites.
However, resource limitation seems unable
to explain crowding effects in situations when
food or other resources were not limiting. In
such situations, crowded land snails showed
reduced fecundity and slower individual growth
rates (Oosterhoff, 1977; Cameron & Carter,
1979; Charrier, 1981; Lazaridou-Dimitriadou &
Daguzan, 1981; Dan & Bailey, 1982; Lucarz,
1984; Carter & Ashdown, 1984; Lucarz &
Gomot, 1985; Reichardt etal., 1985; Stephanou,
1986a; Staikou & Lazaridou-Dimitriadou,
1989) that, because resources were apparently
not limiting, are likely to have been due to
interference competition. Intraspecific interference in land snails has received little study.
In this study I examined the effect of conspecific adults on the juvenile growth rate of
three land snail species, Mesodon thyroidus
(Say, 1816) and Neohelix albolabris (Say, 1816)
(both Polygyridae), and Anguispira alternata
(Say, 1816) (Discidae) in northern Michigan,
USA. For M. thyroidus I tested whether food
and moisture could be limiting resources in
field cages by comparing growth rates of
juveniles in the presence or absence of conspecific adults under ambient and elevated food
and moisture conditions. To examine whether
effects of conspecific adults on growth rates
were due to resource competition or to intraspecific interference, I tested juveniles of the
three snail species with conspecific adults in
laboratory cages, providing non-limiting food
and moisture. Finally, I compared growth rates
of M. thyroidus and N. albolabris having different numbers of conspecific adults in laboratory
and field experiments in which food and water
were non-limiting to evaluate the importance of
intraspecific interference in the field.
METHODS AND MATERIALS
Study area and organisms
I conducted field experiments and gathered specimens for laboratory study at the University of Michigan Biological Station in the northern part of
Michigan's Lower Peninsula in Cheboygan County,
USA. (45°33'3O* N Latitude, 84°41' W Longitude).
The field site is an area of upland hardwood forest on
well-drained sandy soil. Common trees include Populus grandidentata Michaux (big tooth aspen), Acer
saccharum Marsh, (sugar maple), Acer rubrum L.
(red maple), Quercus rubra L. (red oak), and Pinus
strobus L. (white pine). Common understory plants at
the site include Pteridium aquilinum (L.) Kuhn.
(bracken fern), Pedicularis sp., and Vaccinium sp.
(blueberry). The forest has been regenerating since it
was logged and bumed in 1911.
Mesodon thyroidus, Neohelix albolabris and
Anguispira alternata are. large (adult shells 15 to 25
mm diameter) snails that coexist in woodlands
throughout northeastern North America (Hubricht,
1985), often in the same microhabitats. Mesodon
thyroidus and N. albolabris in northern Michigan
can reach maturity in their second year. Anguispira
alternata probably takes longer, perhaps 3 years, to
mature. I could readily identify adults of the two polygyrids because their shells have determinate growth,
forming a reflected lip that probably coincides with
sexual maturation (but see Williamson, 1976; Cowie,
1984). The shell of A. alternata continues growing
throughout life, though more slowly at larger sizes. I
considered A. alternata with shell diameters greater
than 13 mm to be adult. I have seen M. thyroidus and
N. albolabris mating in the forest in the spring time,
and all three species can probably mate and lay
clutches of eggs (about 12-18 eggs for M. thyroidus
and N. albolabris, about 15 to 25 eggs for A. alternata)
whenever the weather is moist for enough time that
they can obtain sufficient food. My tagging studies
indicate that M. thyroidus and N. albolabris can live
at least 3 years as adults in thefield,and in my laboratory cages, A. alternata has lived at least 4 years after
reaching a size that is probably sexually mature.
Previous reports give field population densities in
other parts of the United States for Mesodon thyroidus as 0.28 to 1.24 snails per m2 (Blinn, 1963) and
for Neohelix albolabris as 0.019 to 0.23 snails per m2
(G.F. McCracken, unpublished abstract) and 0.33
snails per m2 (Asami, 1988). I subjectively estimate
natural density of M. thyroidus in the study area to be
about 0.1 snails per m2 and that of N. albolabris to be
about 0.3 snails per m2. Natural density of Anguispira
alternata at the site is of the same order as the other
two species.
Anguispira alternata and Mesodon thyroidus are
reported to be fungivores (Archer, 1939; Blinn, 1963;
Burch & Jung, 1988). I have observed all three
species in thefieldeating a variety of living and dead
plant material, fungi, and carrion. In the laboratory
they readily ate lettuce, fish food, and chicken food.
Study of the movements of a small number of individual snails (Pearce, 1992) suggests that activity
ranges of Anguispira alternata are relatively small
(one had a range of ca 40 m2 over 100 days) and they
tend to be on or near trees or fallen logs. The activity
range of one Neohelix albolabris was larger (ca 80 m2
over 100 days), while one Mesodon thyroidus seemed
to be more itinerant with the largest activity range (ca
800 m2 over 100 days). Snails typically crawled less
than 2 m per night if they moved at all; the farthest
any of the three species crawled in one night was 8 m.
General methods
Shell growth rate is an easily measured indicator of
performance. Because adult shells do not grow (or
ADULTS INHIBIT JUVENILE LAND SNAIL GROWTH
grow slowly in Anguispira altemata), I examined
growth rate of juveniles in all experiments. Preliminary trials showed the effects of adults on juveniles to
be easier to detect than the effects of juveniles on
juveniles, so I examined effects of adults on juveniles
in all experiments.
To determine growth rate, I measured change in
shell diameter over time. In field experiments with
larger juveniles I measured diameter with vernier
calipers. In laboratory experiments, I measured
juvenile snails visually using a microscope having a
calibrated eyepiece micrometer or a camera lucida
that allowed me to view both a scale and the snail. In
some experiments I also measured new shell growth
along the suture over time, obtaining similar results
and the same conclusions as with diameters; I do not
report suture growth results here.
Field experiments
To study if resource competition occurs in thefieldat
near-natural densities, I determined whether food
and moisture were limiting resources in field experiments 1 and 2 (Table 1). I compared growth rates of
single juvenile Mesodon thyroidus in one m2 cages
having zero or two conspecific adults under two treatments: ambient or augmented food and moisture conditions. Due to time limitations, I did not perform
these field tests for resource competition in Neohelix
albolabris and Anguispira altemata.
Experiment 2 allows comparing the possibility of
intraspecific interference for Mesodon thyroidus in
the field with that in laboratory experiment 1 (in
which food and moisture were not limiting, described
below). To test this possibility with Neohelix albolabris, I performed field experiment 3 (Table 1),
examining growth rates of pairs of juvenile N. albolabris in field cages having zero or two conspecific
adults under augmented food and moisture conditions. I used the mean growth of the two juvenile
snails in statistical analyses.
I collected snails locally and marked them individually. I collected adult and juvenile snails for field
experiments from unpaved roads at night after rain.
391
The most useful features for discriminating juvenile
Mesodon thyroidus and Neohelix albolabris were
presence of black pigment granules on the tentacles
and less pronounced shell rib sculpture in A', albolabris (Pearce, in prep.). Conspecific snails were probably somewhat related because they were mostly
from an area of forest less than 200 m diameter. I
used juvenile snails that were greater than 10 mm
diameter so they could not escape from the cages, so I
could easily mark their shells, and so I could more
easily find them again among the leaf litter in the
experimental cages. So I could identify individuals on
recapture, I marked shells with a spot of white correction fluid, a number in permanent ink, then painted
over that with clear fingernail polish (modified from
Hazlett, 1984). I marked juvenile snails on their upper
shell surface where subsequent shell growth would
not overgrow the mark.
The 24 cages in upland hardwood forest served to
retain snails and to exclude vertebrate predators.
Cages enclosed natural vegetation that was present
on the site. The cages were 6 mm mesh galvanized
wire screen on the sides and top (dimensions: 122 X
82 cm with sides 30 cm high, with the lower 10 cm
buried in the soil) and enclosed 1 m2 of forestfloor.In
these cages experimental snails were at densities
somewhat greater than but near natural field densities.
For field experiments with augmented food and
moisture, I added enough chicken food pellets to the
cages so that food remained between feedings and I
added water with a sprinkler system when natural
rain had not fallen for 48 hours. Chicken food has
been reported to give good growth of snails
(Stephanou, 1986b).
Finding snails in cages so that I could measure their
size sometimes proved challenging because snails
usually rest out of sight under leaves during the day.
To disturb the leaf litter in the cage as little as possible, I sought actively crawling snails at night using a
lantern when the ground was moist. If natural rain
had not moistened the ground, I moistened cages a
few hours before seeking snails. To locate snails that I
could not find at night, or when time constraints
Table 1. Details of methods used in field and laboratory experiments testing the effect of adult snails
on growth rates of conspecific juvenile Mesodon thyroidus, Neohelix albolabris, and Anguispira
altemata. Field cages enclose 1 m2 of forest floor, laboratory cages contain 0.04 m2 surface area.
Juv. start
Diam. (mm)
Snail numbers
Experiment
Species
Juvenile Adult
field 1
field 2
field 3
lab 1
lab 2
lab 3
lab 4
1
1
2
1
1
1
1
M. thyroidus
M. thyroidus
N. albolabris
M. thyroidus
N. albolabris
A. altemata
A. altemata
moisture
0or2
ambient
0or2
added
0or2
added
0, 1 or 3 ad lib.
0, 1 or 3 ad lib.
0, 1 or 3 ad lib.
0 or 3
ad lib.
(days)
Replicates
Start
date
Mean
s.d.
72
44
57
24
24
24
16
12
12
12
5
5
5
5
19 May '92
29Jul.'93
23 May '93
12 Nov.'90
12 Nov. '90
12 Nov. '90
27 May'91
15.51
12.69
15.47
6.59
5.44
4.67
3.96
0.79
1.72
1.52
0.45
0.18
0.34
0.32
392
TIMOTHY A. PEARCE
necessitated a daytime search, I shuffled through the
leaf Utter tofindestivating snails.
Laboratory experiments
To determine whether interference competition
occurs under laboratory conditions in which food and
moisture resources were not limiting, I examined the
effect of conspecific adults on the growth rates of
juveniles. In laboratory experiments 1 through 3
(Table 1) I compared growth rates of Mcsodon thyroidus, Neohelix albolabris, and Anguispira altemata,
respectively. Each experiment had a single juvenile
alone, a single juvenile with one adult, and a single
juvenile with three adults, with five replicates of each
treatment for each species. To further explore a trend
seen in laboratory experiment 3,1 conducted laboratory experiment 4 on A. altemata using two treatments: a single juvenile alone or with three adults.
In laboratory experiments I used young juvenile
snails that hatched from eggs laid by adults. Consequently, juveniles in laboratory experiments were
smaller than those in field experiments. Juveniles in
any one experiment started as similar size individuals.
I was unable to control for possible kin effects when I
combined adults and juveniles in treatments because
I could not identify which adults were parents of
which juveniles.
Laboratory cages were polyethylene containers
(610 ml, internal surface area 390 cm2) with snap-top
lids having about 125 holes 2 mm in diameter for
ventilation. Snail population densities in the cages
were several orders of magnitude greater than natural
population densities. During experiments I kept cages
in glass terraria with lids of wire mesh covered by a
moist cloth towel to maintain humidity.
Because a number of researchers have speculated
that presence of mucus might influence snail growth
rates (Cain, 1983; Goodfriend, 1986; Baur, 1988b), I
eliminated mucus when I washed cages and terraria
by including a 3 minute soak in 0.5% sodium
hypochlorite (bleach).
To avoid the possibility that snails might compete
for food or water resources, I provided an excess of
food and moist absorbent paper (ca 860 cm2) in laboratory experiments. In laboratory experiments 1
through 3, I replaced moist absorbent paper every 4
days, and offered excess lettuce every 2 days and fish
food (TetraMin brand) every 4 days. During laboratory experiment 4, I replaced moist absorbent paper
and offered lettuce and fish food every 2 days. To
avoid the possibility of competition for calcium, in
experiments where calcium was present in treatments
(e.g., in the feces of adults who had eaten ground
shell), I added calcium to the control cages as well as
to the treatment cages. Calcium seems to influence
snail distributions (Coney, Tarpley, Warden & Nagel,
1982; Burch & Pearce, 1990) and mortality (Cain,
1983), and may affect snail growth (Mead, 1961;
Gomotefa/., 1986).
Statistical analyses
To determine if snails in different treatments differed
in growth rates over the duration of the experiments,
I performed one way analysis of variance (ANOVA)
on the total growth change at the end of the experiment using Systat version 5.2.1 (Wilkinson, 1990). For
experiments having a significant difference in growth
rate among three treatments, I used the Tukey posthoc multiple comparison test to determine which
treatments differed significantly.
RESULTS
Field experiment results
In field experiment 1 under ambient food and
moisture conditions (without added food or
water), juvenile Mesodon thyroidus in 1 m2 field
cages grew significantly more slowly when living with two adults than when alone (Fig. 1) (df
= 1, F = 6.497 p = 0.018). Furthermore, more
juveniles reached maturity in the absence of
adults (Fisher exact test, p = .035); six of the
twelve juveniles growing alone reached adult
shell morphology (forming a reflected lip) while
only one of the twelve juveniles that had been
living with two adults did so.
In contrast, when I added food and water to
the field cages neither Mesodon thyroidus in
field experiment 2, nor Neohelix albolabris
in field experiment 3 differed significantly in
growth whether they were living alone or with
adults (Figs. 2, 3) (for M. thyroidus, df = 1, F =
0.115, p = .738; for N. albolabris, df = 1, F =
1.404,p = .249).
Laboratory results
Mesodon thyroidus juveniles in laboratory
experiment 1 grew significantly more slowly in
the presence of more conspecific adults (Fig. 4).
Juveniles living in cages with one or three
adults for 24 days increased shell diameter
more slowly than those living alone (df = 2, F =
10.021, p = .003; Tukey between alone and one
adult, p = .013, between alone and three adults,
p = .003). Growth rates of juveniles exposed to
one or three adults did not differ significantly
(Tukey, p = .708).
Neohelix albolabris juveniles in laboratory
experiment 2 also grew significantly more
slowly in the presence of conspecific adults (Fig.
5). Juveniles living in cages with three adults for
24 days increased shell diameter more slowly
than those living alone or with one adult (df =
2, F = 16.474, p = .0004; Tukey between alone
and three adults, p = .0006, between one and
three adults, p = .002). Growth rates of
juveniles living alone or with one adult did not
differ significantly (Tukey, p = .720).
ADULTS INHIBIT JUVENILE LAND SNAIL GROWTH
393
O
Figure L Change in shell diameter of juvenile Mesodon thyroidus in 1 m2 field cages without added food or
water. Treatments were one juvenile alone and one juvenile with two conspecific adults. Error bar is standard
deviation. Sample size is 12 for each data point.
—n—alone
o
co
ro
lange in diameter (
E 4- —-o—with 2 adults
J
/
V
0-c
t
0
i
i
i
20
i
40
day
Figure 2. Change in shell diameter of juvenile Mesodon thyroidus in 1 m2 field cages with added food and
water. Treatments were one juvenile alone and one juvenile with two conspecific adults. Error bar is standard
deviation. Sample size is 9-12 (depending on mortality) for each data point.
In contrast, growth rate of Anguispira alternata in laboratory experiments 3 and 4 showed
no response to number of conspecific adults
(Figs. 6, 7). Anguispira alternate juveniles did
not show significantly different changes in shell
diameter when living alone, with one, or with
three adults for 24 days in laboratory experi-
ment 3 (df = 2, F = 2.711, p = .145) or when living alone or with three adults for 16 days in laboratory experiment 4 (df = 1, F = 1.054, p =
335). Survival rates of A. alternate, on the other
hand, were lower in the presence of adults
(Fisher exact test, p = .022); all five juveniles
living alone survived the 24 days of laboratory
394
TIMOTHY A. PEARCE
£
E
CO
CO
JZ
o
(
day
Figure 3. Change in shell diameter of juvenile Neohelix albolabris in 1 m2 field cages with added food and
water. Treatments were one juvenile alone and one juvenile with two conspecific adults. Error bar is standard
deviation. Sample size is 11—12 (depending on mortality) for each data point.
alone
E 4- -—o-—with 1 adult
o—- with 3 adults
Figure 4. Change in shell diameter from day zero of a juvenile Mesodon thyroidus living in laboratory cages
alone or with one or with three conspecific adults. Error bar is standard deviation. Sample size is 5 for each
data point.
experiment 3, while only four of the ten
juveniles living with either one or three adults
survived that long.
DISCUSSION
Resource competition with conspecific adults
appeared to limit growth rates of juvenile
ADULTS INHIBIT JUVENILE LAND SNAIL GROWTH
395
•alone
o—with 1 adult
a>
E
-o—-with 3 adults
CO
-a
o
Figure S. Change in shell diameter from day zero of juvenile Neohelix albolabris living in laboratory cages
alone or with one or with three conspecific adults. Error bar is standard deviation. Sample size is 5 for each
data point.
E
alone
a> 2 CD
~o—with 1 adult
-o— with 3 adults
E
CO
=5 H
c
CD
O)
C
CO
o
Figure 6. Change in shell diameter from day zero of juvenile Anguispira altemata living in laboratory cages
alone or with one or with three conspecific adults. Error bar is standard deviation. Sample size is 2-5 (depending on mortality) for each data point.
-
E 2E
CD
c5
CD
1-
CO
•v
00
Figure 7. Change in shell diameter from day zero of juvenile Anguispira altemata living in laboratory cages
alone or with three conspecific adults. Error bar is standard deviation. Sample size is 5 for each data point.
396
TIMOTHY A. PEARCE
Mesodon thyroidus in the field under ambient
food and water conditions. Under augmented
food and water conditions, conspecific adults
did not affect growth rates of M. thyroidus in
field cages.
Interference competition with conspecific
adults appears to be responsible for limiting
growth rates of juvenile Mesodon thyroidus at
relatively high population densities in the laboratory. Juvenile M. thyroidus in the laboratory
received abundant food and water, so competition for those resources seems unable to
explain their slower growth. Their slower
growth in the presence of adults is apparently
due to interference competition.
Interference competition with conspecific
adults also appears to be responsible for limiting growth rates of juvenile Neohelix albolabris
in the laboratory. Resource competition for
food and water, which were non-limiting, cannot explain their slower growth, so apparently
interference competition occurred. However,
in field cages at lower population densities, as
was the case for Mesodon thyroidus, growth
rates of N. albolabris juveniles having
augmented food and water were unaffected by
conspecific adults. I did not test whether N.
albolabris competed for resources in thefieldat
ambient food and moisture conditions. I predict
that N. albolabris would compete for resources
under natural conditions in the field as did M.
thyroidus.
In contrast to laboratory results for Mesodon
thyroidus and Neohelix albolabris, growth rates
of Anguispira alternata were unaffected by the
densities of conspecific adults at which the
other species experienced growth inhibition.
Anguispira alternata experienced neither
resource competition nor interference competition at these population densities. Possibly its
growth rate may be affected at levels of crowding greater than those I tested. The effective 26
to 78 snails per m2 density I used in the laboratory experiments were considerably less than
the mean of 807 A. alternata snails per m2 found
in one habitat by Douglas (1963). The possibility that this species may be able to tolerate
great population densities could account for the
apparent lack of growth inhibition at the densities I tested.
Competition for the resources food, water, or
both appears to explain reduced growth rates of
juvenile Mesodon thyroidus living with conspecific adults in field experiments under ambient
food and moisture conditions. I have not conducted experiments to determine whether the
limiting resource was food or moisture. In field
cages with added food and water, little of the
added food appeared to have been eaten, so
food may not have been a limiting resource. I
speculate that of those two potentially limiting
resources, moist sites rather than food may
have been more limiting. Maintaining sufficient
moisture is very important for land snail activity, growth, and survival (Solem, 1974; Boag,
1985; Imevbore, 1990). Oosterhoff (1977)
added water to some field cages of Cepaea
nemoralis (Linnaeus, 1798) and found the proportion of snails becoming adults increased in
the moister cages, although growth rates did
not differ. Mechanisms by which insufficient
moisture could affect snail growth include (a)
direct physiological stress or (b) moisture limitation, which would reduce the amount of time
available for movement and feeding activity.
Snails could plausibly compete for limited
moisture, for example, by excluding each other
from moist resting sites.
Even if moisture were limiting in my experiments, food could also be limiting. Although
many workers report that food does not seem
to limit land snails in the field (Williamson et al.,
1976; Hunter, 1978; Peake, 1978; Cain, 1983),
other workers do report food limitation in land
snails. For example, Pomeroy (1969) and Butler
(1976), studying Cernuella virgata (da Costa,
1778) infieldcages gave evidence of food shortage in more crowded cages. In these studies,
crowded snails growing more slowly in the field
are consistent with the hypothesis that food or
other resources were limiting. In freshwater
snails, food often seems to be limiting (Eisenberg, 1966). Future experiments could separate
the importance of competition for food and
moisture infieldsituations.
In my laboratory experiments, resource limitation did not appear to be responsible for the
slower growth of Mesodon thyroidus and Neohelix albolabris juveniles living with conspecific
adults. I added enough food and water to laboratory cages so food and moisture remained
between cage cleanings and feedings, so those
resources are not likely to have been limiting as
they had been in some previous laboratory
experiments (Cowie & Cain, 1983; Daguzan &
Verly, 1989). Competition for another unidentified resource might explain the reduced
growth of juveniles living with adults. However,
evidence from further experiments on the
nature of the growth inhibition (Pearce, in
prep.) shows that juvenile M. thyroidus and N.
albolabris may grow more slowly in cages simply soiled by conspecific adults, from which the
adults were absent. These results obviate the
ADULTS INHIBIT JUVENILE LAND SNAIL GROWTH
possibility of direct competition with adults for
resources. Consequently, slower growth of M.
thyroidus and N. albolabris in laboratory experiments appears to be due to interference, not
resource competition.
Interestingly, adult Mesodon thyroidus and
Neohelix albolabris interfered with juvenile
growth in laboratory experiments but not in
field experiments although I provided abundant food and water in both. The main condition differing between field and laboratory
experiments that could explain this result is
population density, i.e., number of snails per
area. Population densities in field experiments
were one or three M. thyroidus, or two or four
N. albolabris in cages enclosing 1 m2 of forest
floor. In laboratory experiments, snail densities
were one, two or four in cages containing 0.04
m2 surface area. Actual available surface area
in both field and laboratory cages was somewhat greater due to presence of plants and dead
leaves in the forest, and crumpled absorbent
paper in the laboratory. Interactions that did
not noticeably interfere with growth at field
experiment densities may have increased dramatically to interfere with growth at the considerably greater population density in laboratory
experiments.
In laboratory experiments, different juvenile
growth rates in the presence of different numbers of adults could be due either to population
densities or to absolute numbers of conspecifics
regardless of area. Because all of my laboratory
cages were the same size, I cannot distinguish
whether differences in juvenile responses were
due to number of interactions with any snail, or
number of interactions with different individuals, both of which increased in the denser cages.
If subsequent interactions with the same individual have little affect on juveniles, then total
number of individuals a snail meets (absolute
number) would be more important than the
number of times a juvenile interacts with any
snail (population density). On the other hand, if
any snail interaction affected juveniles equally
whether with a previously met or novel individual, then population density would be the more
important influence.
To test whether differences in response were
due to population density or to number of
snails, an experiment would need, besides treatments with different numbers of snails in the
same size cages, additional treatments having
the same number of snails in different size
cages. An experiment testing the effects of population density versus number of individuals in
Cepaea nemoralis found that single individuals
2
397
in boxes of 125 cm surface area grew more
rapidly than eight individuals in 1000 cm2 boxes
(Cameron & Carter, 1979). This result with
snails at the same density but different absolute
numbers of snails, is consistent with three
hypotheses: (1) number of other snails, not
simply population density, can influence snail
growth rate (Cameron & Carter, 1979) (2)
number of individuals per surface area may not
be the important variable, instead some other
measure of population density such as snails
per volume or snails per number of corners that
could be used as resting sites (Dan & Bailey,
1982) may be more important, and (3) social
interactions may regulate snail growth. For
example, in the freshwater snail Biomphalaria
glabrata (Say, 1818), Thomas & Benjamin
(1974) found that in the same volume of water,
paired individuals grew more rapidly than
either single individuals or more crowded individuals, indicating that other snails exert an
important influence. We need further research
to distinguish among these hypotheses.
Because Mesodon thyroidus and Neohelix
albolabris do not naturally occur in high densities in the field, interference interactions would
seem unlikely to ever exert a greater influence
than resource competition in real-worldfieldsituations of those species. Crowding effects in the
field can occur in other snail species living in relatively great field densities, leaving open the
possibility that interference interactions may
affect natural populations of some snails. For
example, crowding effects were found for dense
field populations of Cemuella virgata (Pomeroy,
1969; Butler, 1976; Smallridge & Kirby, 1988;
Bull, Baker, Lawson & Steed, 1992), Cepaea
nemoralis (Oosterhoff, 1977; Williamson et al.,
1977; Cameron & Carter, 1979), Helix aspersa
Muller, 1774 (Dan & Bailey, 1982; Lucarz &
Gomot, 1985; Stephanou, 1986a) and Theba
pisana (MUller, 1774) (Moran, 1989; Smallridge
& Kirby, 1988; Bull et al., 1992). Further investigations need to examine whether intraspecific
interference or resource competition has a
greater influence on the crowding effects in field
populations of those species.
The interference competition responsible for
slower growth of juveniles living with adults in
laboratory experiments in this study could
be due to behavioral interactions or to allelochemical interactions. If the growth-inhibitor is
allelochemical, the nature of the substance
needs study. I have conducted further investigations on the nature of the interference, e.g.,
whether behavioral interactions account for the
slower growth, and whether growth-inhibiting
TIMOTHY A. PEARCE
398
substances are present in the feces or mucus
(Pearce, in prep.).
In summary, resource competition for food
or moisture best explains how Mesodon thyroidus adults slowed growth rates of conspecific
juveniles under natural conditions in the field,
and interference competition seems to be
responsible for slower growth of M. thyroidus
and Neohelix albolabris in laboratory experiments.
ACKNOWLEDGMENTS
I am grateful to J.B. Burch, BJ. Rathcke, B.A.
Hazlett, and G.R. Smith for encouragement and guidance during this study. Funds from the University of
Michigan Biological Station and the University of
Michigan Department of Biology made this research
possible. Anonymous reviewers made helpful comments.
BURCH, J.B. & JUNG, Y. 1988. Land snails of the Uni-
versity of Michigan Biological Station area. Walkerana,y. 1-177.
BURCH, J.B. & PEARCE, T.A. 1990. Terrestrial Gas-
tropoda. In: Soil Biology Guide (D.L. Dindal, ed.),
201-309. John Wiley & Sons, New York.
BUTLER, A J. 1976. A shortage of food for the terrestrial snail Helicella virgata in South Australia.
Oecologia, 25:349-371.
CAIN, A.J. 1983. Ecology and ecogenetics of terrestrial molluscan populations. In: The Mollusca, 6:
Ecology (W.D. Russel-Hunter, ed.), 597-647.
Academic Press, London.
CAMERON, R.A.D. & CARTER, M.A. 1979. Intra- and
interspecific effects of population density on
growth and activity of some helicid land snails
(Gastropoda: Pulmonata). Journal of Animal Ecology, 48:237-246.
CARTER, M.A. & ASHDOWN, M. 1984. Experimental
studies on the effects of density, size, and shell
color and banding phenotypes on the fecundity of
Cepaea nemoralis. Malacologia, 25: 291-302.
CHARRIER, M. 1981. Contribution a l'etude des effets
du groupement sur la croissance de Pescargot
'petit-gris' Helix aspersa MUller (Gast6ropode pulREFERENCES
mon£ stylommatophore). Archives de Zoologie
experimental et gtnerale, V22: 29-38.
ARCHER, A.F. 1939. The ecology of the Mollusca of
the Edwin S. George Reserve, Livingston County,
CHEVALLIER, H. 1982. Facteurs de croissance chez
Michigan. Occasional Papers of the University of
des gaste'ropodes pulmones terrestres pal£arcMichigan, 398:1-24.
tiques en 61evage. Haliotis, 12:29-46.
ASAMI, T. 1988. Temporal segregation of two sym- CONEY, C.C., TARPLEY, W.A., WARDEN, J.C. &
patric species of land snails. Venus, 47:278-297.
NAGEL, J.W. 1982. Ecological studies of land snails
in the Hiwassee River basin of Tennessee, U.S.A.
BAILEY, S.E.R. 1989. Daily cycles of feeding and
Malacological Review, 15: 69-106.
locomotion in Helix aspersa, Haliotis, 19: 23-31.
BAUR, A. 1990. Intra- and interspecific influences on COOK, A. 1989. Crowding effects on the growth of
juvenile slugs (Limax pseudoflavus). In: Slugs and
age at first reproduction and fecundity in the land
Snails in World Agriculture. (I.F. Henderson, ed.),
snail Balea perversa. Oikos, 57: 333-337.
193-200. The British Crop Protection Council,
BAUR, A. & BAUR, B. 1992. Responses in growth,
Monograph No. 41. Thornton Heath, U.K.
reproduction and life span to reduced competition
pressure in the land snail Balea perversa. Oikos, 63: COOK, L.M. & CAIN, A.J. 1980. Population dynamics,
298-304.
shell size and morph frequency in experimental
populations of the snail Cepaea nemoralis (L.).
BAUR, B. 1988a. Microgeographical variation in shell
Biological Journal of the Linnean Society, 14, 259size of the land snail Chondrina clienla. Biological
292.
Journal of the Linnean Society, 35: 247-259.
BAUR, B. 1988b. Population regulation in the land
COWIE, R.H. 1984. The life-cycle and productivity of
snail Arianta arbustorum: density effects on adult
the land snail Theba pisana (Mollusca: Helicidae).
size, clutch size and incidence of egg cannibalism.
Journal of Animal Ecology, 53: 311-325.
Oecologia, 77: 390-394.
COWIE, R.H. & CAIN, AJ. 1983. Laboratory maintenance and breeding of land snails, with an example
BAUR, B. & BAUR, A. 1990. Experimental evidence
from Helix aspersa. Journal of Molluscan Studies,
for intra- and interspecific competition in two
49:176-177.
species of rock-dwelling land snails. Journal of Animal Ecology, 59: 301-315.
DAGUZAN, J. & VERLY, D. 1989. Etude experimentale de l'effet de la densite sur la reproduction de
BLINN, W.C. 1963. Ecology of the land snails
l'escargot petit-gris (Helix aspersa Muller). HalioMesodon thyroidus and AUogona profunda. Ecoltis, 19:105-115.
ogy, 44:498-505.
BOAG, D.A. 1985. Microdistribution of three genera
DAN, N. & BAILEY, S.E.R. 1982. Growth, mortality,
of small terrestrial snails (Stylommatophora: Puland feeding rates of the snail Helix aspersa at difmonata). Canadian Journal of Zoology, 63: 1089ferent population densities in the laboratory and
1095.
the depression of activity of helicoid snails by other
individuals or their mucus. Journal of Molluscan
BULL, CM., BAKER, G.H., LAWSON, L.M. & STEED,
Studies, 48:257-265.
M. A. 1992. Investigations of the role of mucus and
faeces in interspecific interactions of two land
DOUGLAS, C.L. 1963. Population analyses, variation,
snails. Journal of Molluscan Studies, 58: 433-442.
and behavior of Anguispira aliemata altemata.
ADULTS INHIBIT JUVENILE LAND SNAIL GROWTH
399
Transactions of the Kansas Academy of Sciences, REICHARDT, A., RABOUD, C, BURLA, H. & BAUR, B.
66:186-194.
1995. Causes of death and possible regulatory processes in Arianla arbustorum (L,, 1758) (PulEISENBERG, R.M. 1966. The regulation of density in a
monata, Helicidae). Basteria, 49:37-46.
natural population of the pond snail, Lymnaea
elodes. Ecology, 47:889-906.
RIDDLE, W.A. 1983. Physiological ecology of land
GOMOT, A., BRUCKERT, S., GOMOT, L. & COMBE, J.C.
snails and slugs. In: The Mollusca, 6: Ecology
1986. A contribution to the study of the beneficial
(W.D. Russel-Hunter, ed.), 431-461. Academic
effects of soil on the growth of Helix aspersa. Snail
Press, London.
Farming Research, 1: 76-83.
SMALLRIDGE, M.A. & KIRBY, G.C. 1988. Competitive
GOODFRIEND, G.A. 1986. Variation in land-snail shell
interactions between the land snails Theba pisana
form and size and its causes: a review. Systematic
(Muller) and Cernuella virgata (DaCosta) from
Zoology, 35:204-233.
South Australia. Journal of Molluscan Studies, 54:
251-258.
HAZLETT, B.A. 1984. Daily movements of some tropical marine gastropods. Marine Behaviour and STAJKOU, A. & LAZARIDOU-DIMITRIADOU, M. 1989.
Physiology, 11,35-48.
Effect of crowding on growth and mortality in the
HUBRICHT, L. 1985. The distributions of the native
edible snail Helix lucorum (Gastropoda: Pulland mollusks of the eastern United States. Fieldmonata) in Greece. Israel Journal of Zoology, 36:
iana, Zoology, n.s., 24:1-191.
1-9.
HUNTER, P.J. 1978. Slugs—a study in applied ecology.
STEPHANOU, D. 1986a. Contribution to the study of
In: Pulmonates, (V. Fretter & J. Peake, eds.), 2A:
the effect of stocking density in the culture of Helix
271-286. Academic Press, London.
aspersa (Muller). Snail Farming Research, 1: 27-33.
IMEVBORE, E.A. 1990. Observations on the responses
STEPHANOU, D. 1986b. Experiments on the nutrition
of the African giant snail, Archachatina marginata
of Helix cincta (Kobelt) and Helix aspersa (MUUer).
to varying moisture conditions in captivity. Snail
Snail Farming Research, 1: 42-49.
Farming Research, 3:15-20.
TATTERSFIELD, P. 1981. Density and environmental
effects on shell size in some sand dune snail populaKREBS, CJ. 1994. Ecology, fourth edition. Harpertions. Biological Journal of the Linnean Society, 16:
Collins, New York.
71-81.
LAZARIDOU-DIMITRIADOU, M. & DAGUZAN, J. 1981.
Etude de l'effet du 'groupement' des individus chez
THOMAS, J.D. & BENIAMIN, M. 1974. Effects of numTheba pisana (Mollusque Gasteropode Pulmone
bers, biomass, and conditioning time on the growth
Stylommatophore). MaJacologia, 20:195-204.
and natality rates of Biomphalaria glabrata (Say)
the snail host of Schistosoma mansoni Sambon.
LUCARZ, A. 1982. Effet du groupement sur la croisJournal of Applied Ecology, 11: 823-840.
sance pondeYale d'escargots Helix aspersa Muller.
Comptes Rendus de l'academie des sciences serie
TILLING, S.M. 1985. The effects of density and interIII. Sciences de la Vie, 294: 753-756.
specific interactions on mortality in experimental
populations of adult Cepaea (Held). Biological
LUCARZ, A. 1984. Experimental study of the effect of
Journal of the Linnean Society, 24:61-70.
population density on egg laying by the snail Helix
aspersa Muller. International Journal of Inverte- WILKINSON, L. 1990. SYSTAT: the system for
brate Reproduction, 7:185-192.
statistics. SYSTAT, Inc., Evanston, Illinois.
LUCARZ, A. & GOMOT, L. 1985. Influence de la denWILLIAMSON, P. 1976. Size-weight relationships and
site de population sur la croissance diametrale et
field growth rates of the landsnail Cepaea
ponderale de Pescargot Helix aspersa Muller dans
nemoralis L. Journal of Animal Ecology, 45: 875differentes conditions d'elevage. Journal of Mol885.
luscan Studies, 51:105-115.
WlLLLIAMSON, P., CAMERON, R . A . D . & CARTER,
MEAD, A.R. 1961. The giant African snail. University
M.A. 1976. Population density affecting adult shell
of Chicago Press, Chicago.
size of snail Cepaea nemoralis L. Nature, London,
263:496-497.
MORAN, S. 1989. Weather- and population densityinduced infantilism in the landsnail Theba pisana WILLIAMSON, P., CAMERON, R.A.D. & CARTER, M.A.
in a semi-arid climate. International Journal of
1977. Population dynamics of the landsnail Cepaea
Biometeorology, 33:101 -108.
nemoralis L. A six-year study. Journal of Animal
Ecology, 46:181-194.
OOSTERHOFF, L.M. 1977. Variation in growth rate as an
ecological factor in the landsnail Cepaea nemoralis WOLDA, H. & KREULEN, D. 1973. Ecology of some
(L.). Netherlands Journal of Zoology,Tl: 1-132.
experimental populations of the land snail Cepaea
nemoralis (L.). II. Production and survival of eggs
PEAKE, J. 1978. Distribution and ecology of the Styand juveniles. Netherlands Journal of Zoology, 23:
lommatophora. In: Pulmonates, 2A: Systematics,
168-188.
evolution and ecology (V. Fretter & J. Peake, eds.),
429-526. Academic Press, London.
YOM-TOV, Y. 1972. Field experiments on the effect of
population density and slope direction on the reproPEARCE, T.A. 1992. Spool and line technique for
duction of the desert snail Trochoidea (Xerocrassa)
tracing field movements of terrestrial snails.
seetzenL Journal of Animal Ecology, 41:17-22.
Walkerana, 4: 307-316.
POMEROY, D.E. 1969. Some aspects of the ecology of
ZAR, J.H. 1984. Biostatistical Analysis, Second Edithe land snail, Helicella virgata, in South Australia.
tion. Prentice-Hall, Inc. Englewood Cliffs, New
Australian Journal of Zoology, 17:495-514.
Jersey.