DIFFERENCES IN THE LIFE HISTORIES OF XEROLENTA OBVIA
(MENKE, 1828) (HYGROMIIDAE) IN A COASTAL AND A
MOUNTAINOUS AREA OF NORTHERN GREECE
M. LAZARIDOU AND M. CHATZIIOANNOU
School of Biology, Faculty of Sciences, Aristotle University, 54124 Thessaloniki, Greece
(Received 23 July 2004; accepted 30 December 2004)
ABSTRACT
The life cycle of Xerolenta obvia (Menke, 1828) was studied in two areas, Paleokastro (Chalkidiki), an
inland mountainous area, and Nea Karvali (Kavala), a coastal area in northern Greece. At Paleokastro
snails hatch in autumn, become adult the following July, but do not lay eggs until October, after which
they die. Clutch sizes are small, but eggs and hatchlings are large compared with those at Nea Karvali.
Growth is fast in spring, and continues until the end of July. The young hatchlings have dark shellbands, but by July a quarter of snails appear unbanded. At Nea Karvali, eggs are also laid in
October, and young snails emerge from hibernation in March. Here, however, they do not mature
until April of the following year. They thus have a 2-year life cycle, with adults dying in their second
autumn. Clutches are about three times the size of those at Paleokastro, but eggs and hatchlings are
significantly smaller. A little growth occurs in winter, but the rate of growth is generally much
slower than at Paleokastro. Only 1 – 2% of this population has banded shells; the bands are less
obvious and they become invisible in some individuals as they mature. At both sites population
density fluctuated during the two study years, but it was always higher at Nea Karvali. These results
are discussed in relation to the differing climates of the sites, and comparisons made with studies on
related species in the region.
INTRODUCTION
Land snail activity, growth and reproduction are highly dependent on appropriate climatic conditions. Lazaridou-Dimitriadou
& Sgardelis (1997) have shown that discontinuities in growth
rates and population dynamics between seasons may be attributed to environmental thresholds. Responses to the same climate
may, however, differ between species and, in some groups, the
basic life history pattern may be unaffected by differences in
climate, as in the rock-dwelling Albinaria species in Greece
(Giokas & Mylonas, 2002).
The relatively large species in the Family Hygromiidae show a
variety of life-history patterns. Only three species in this family
have been studied thoroughly in Greece: Cernuella virgata (Da
Costa, 1778) by Lazaridou-Dimitriadou (1981), Monacha cartusiana
(Müller, 1774) by Staikou & Lazaridou-Dimitriadou (1990)
and Xeropicta arenosa Ziegler, 1836 by Lazaridou-Dimitriadou
(1981) and Staikou & Lazaridou-Dimitriadou (1991). These
species live in coastal, semi-coastal or more inland areas.
The hygromiid snail Xerolenta obvia (Menke, 1828) ranges
from Asia Minor to the Balkans, the Carpathians, and along
the Baltic coast and, in the Mediterranean region, to the southeast of France (Fechter & Falkner, 1993). It thus has wide ecological amplitude in terms of macroclimate. The climate of
northern Greece ranges from Mediterranean (mostly coastal
areas) to temperate (inland areas) or continental (mountainous
areas). The coastal areas have milder winters and longer and
hotter dry periods than the inland and mountainous areas.
This study reports on investigations into the life cycle of
X. obvia at two sites, an inland mountainous area at Paleokastro
(Chalkidiki) and a coastal area at Nea Karvali (Kavala), presenting striking differences in climatic regime.
Correspondence: M. Lazaridou; e-mail: [email protected]
MATERIAL AND METHODS
Study areas
Paleokastro lies about 50 km northeast of Thessaloniki in a
mountainous area 600 m above sea level. The vegetation in
the study area is dominated by grasses, nettles (Urtica dioica ),
dandelions (Taraxacum spp.) and thistles (Carduus spp.). The
climate of the region is temperate. The substratum is mostly
limestone. Nea Karvali lies 160 km northeast of Thessaloniki,
in a semi-coastal area at the foot of Neas Komis mountain.
The habitat of Xerolenta obvia is limestone covered with rather
uniformly distributed clumps of Taraxacum spp. and grasses.
Figure 1 shows the temperature and precipitation regimes at
each site during the study period.
Sampling and analyses
From October 1987 to November 1990 at Paleokastro and from
May 1989 to November 1990 at Nea Karvali, stratified random
samples were taken in a 500 m2 area every month, except
between December and February when the snails were hibernating under vegetation. A quadrat sample size of 1 m2 was chosen
as appropriate using Healy’s method (Cansela da Fonceca,
1969). Taylor’s method (1961) was used to determine the total
number of sampling units necessary for a sampling error less
than 20%. Sampling was carried out in the mornings in the
absence of rain. All snails found in a quadrat were collected,
measured and then returned to their initial place. The length
of their greatest shell diameter (D) was measured with vernier
calipers to 0.1 mm. For size frequency histograms, D was used
with a 1-mm class interval (Cansela da Fonseca, 1965).
Additional, qualitative observations were made at Nea
Karvali during the winter months. From these repeated observations, we are sure that all snails are hibernating between
December and the end of February. Hence, growth occurring
Journal of Molluscan Studies (2005) 71: 247– 252. Advance Access Publication: 28 June 2005
# The Author 2005. Published by Oxford University Studies on behalf of The Malacological Society of London, all rights reserved.
doi:10.1093/mollus/eyi032
M. LAZARIDOU AND M. CHATZIIOANNOU
Table 1. Xerolenta obvia population density, at Paleokastro and at Nea
Karvali.
Date
n
N
x
s.d.
E%
Paleokastro
25-10-1987
15
106
7.06
4.15
28-11-1987
39
103
2.64
2.61
15.15
15.82
26-03-1988
5
150
30
10.07
15.01
26-04-1988
3
238
79.33
17.9
13.02
25-05-1988
3
138
46
7.55
9.47
01-07-1988
3
189
63
44.67
40.94
31-07-1988
17
302
17.76
15.36
20.98
27-08-1988
8
121
15.12
7.53
17.6
29-09-1988
6
161
26.83
11.16
16.98
29-10-1988
14
178
12.71
9.13
19.2
31-03-1989
26
229
8.8
9.33
20.7
09-05-1989
13
98
7.38
4.8
17.68
01-06-1989
12
102
8.5
5.28
17.9
30-06-1989
21
111
5.28
4.74
19.6
31-07-1989
22
206
11.44
9.63
19.84
21-08-1989
12
196
16.3
12.15
21.47
26-09-1989
12
114
9.5
5.82
17.69
26-10-1989
19
163
8.58
6.002
16.05
16-11-1989
38
98
2.58
2.43
15.31
31-03-1990
25
63
2.52
2.69
21.38
30-04-1990
4
279
69.75
37.64
26.98
31-05-1990
7
429
61.28
39.32
22.45
01-07-1990
17
457
26.88
24.8
22.38
01-08-1990
17
363
21.35
15.5
17.6
09-09-1990
21
443
21.09
19.65
20.33
11-10-1990
15
168
11.2
8.24
19
04-11-1990
29
106
3.65
2.48
12.61
31-05-1989
8
288
39.63
50.82
45
29-06-1989
4
430
107.5
47.86
22.26
31-07-1989
4
583
145.75
57.17
19.61
22-08-1989
3
365
121.6
32.39
15.37
28-09-1989
2
231
115.5
28.99
17.74
25-10-1989
4
446
111.5
42.22
18.93
17-11-1989
9
710
78.9
60.17
25
02-04-1990
23
88
4.27
23
06-06-1990
11
349
31.73
26.5
25
05-07-1990
8
496
62
28.45
16
01-08-1990
8
686
28-08-1990
8
1056
03-10-1990
6
364
04-11-1990
6
510
Nea Karvali
Figure 1. Mean monthly temperatures (8C) and total precipitation
(mm) at Paleokastro (A) and Nea Karvali (B) from October 1987 to
November 1990.
between November and the following April is thought to occur
very rapidly during March.
The cohorts were distinguished using probability paper
(Harding, 1949). This method was valid because the modes of
the age-classes were separated by at least 2.5 standard deviations
(Grant, 1989), except in April 1990 at Nea Karvali. Although
many age classes had less than 50 individuals, the modal values
were consistent from month to month, confirming that the
modes were real and not the result of sampling variation. This
method has also been used for demographic analyses of other populations of molluscs (Lazaridou-Dimitriadou & Kattoulas, 1991;
Lazaridou-Dimitriadou, 1995). During the reproductive period,
10 clutches from each site were collected and taken to the laboratory, where the diameter of each egg and each hatchling snail were
measured, and the percentage of hatching was recorded.
3.83
85.8
27.23
11
93.42
25.02
60.66
34.94
23.51
85
10.04
4.8
132
Where: n ¼ number of samples, N ¼ number of animals (sample
size), x ¼ mean number of animals/m2, s.d. ¼ standard deviation,
E% ¼ sampling error.
1989 and 1990 showed that the densities differed (F ¼ 5.297,
P ¼ 0.0132, N ¼ 25) and this difference was due to 1989
(Fischer PLSD ¼ 0.372 at 95% significance level). Within
years, significant increases in density in the springs of 1988 and
1990 were probably sampling effects due to snails emerging progressively as temperatures increase. The density declined after
July because of sampling effects since the highest temperatures
appeared in July (Fig. 1) and the snails were hidden and aestivating under plants. A real decline appeared in October, when
the adult snails died after laying eggs.
RESULTS
Population density
Because the availability of snails for sampling varied with season,
estimates of density are prone to errors. Nevertheless, there are
evident differences between the two sites (Table 1). At Paleokastro,
the mean population density during the study period was
22.5 + 4.8 (SE) snails/m2. The density was low throughout
1989 (Fig. 2A). An ANOVA test among the densities of 1988,
248
LIFE HISTORY OF XEROLENTA OBVIA IN GREECE
Figure 2. Density of Xerolenta obvia (number of snails/m2, mean + SD) at Paleokastro (A) and Nea Karvali (B) from October 1987 to November 1990.
At Paleokastro, snails hatched in November and were visible
on vegetation but did not grow rapidly until spring. Growth
between April and July was very rapid. Achieved adult size
was considerably greater in 1989 than in 1988; rainfall in
spring and early summer was higher in 1989. Most grew to
sexual maturity before July, 7 months after hatching, when
their D reached 8 mm, but an identifiable minority grew more
slowly (Fig. 4A: G88b, G89b, G90b). By June or July every
year, 5 – 10 % of the population showed a slower growth so
that the cohort becomes split. In 1989, these snails also reproduced in October, although they were smaller (D 8 mm). In
the other years, they remained smaller, even at the end of
summer. The population aestivated (forming epiphragms)
through the summer dry period for 2– 4 months (Table 2),
before the mating period started in October, lasting only a few
days. Egg-laying was at a peak at the end of October.
At Nea Karvali, the mean population density during the study
period was 84.4 + SE 6.4 snails/m2, almost four times that at
Paleokastro. Population density fluctuated during the study
period (Table 1), but there was no statistical difference between
the densities of 1989 and 1990 (t-test ¼ 1.552, df ¼ 12,
P ¼ 0.147). Significant increases in apparent density occurred
in July 1989 and August 1990. The low values of densities
during March reflect the incomplete emergence from hibernation.
Life history and growth
All data are based on monthly samples taken on the dates shown
in Table 1, and on observations and measurements taken during
the reproductive period. Figure 3 shows the changes in size distribution over the study period at both sites, and Figure 4 shows
the changes in mean shell diameter by cohort.
249
M. LAZARIDOU AND M. CHATZIIOANNOU
Figure 3. Size-frequency histograms of the populations of Xerolenta obvia at Paleokastro (A) and Nea Karvali (B) from October 1987 to November 1990.
DISCUSSION
Laboratory observations confirmed that X. obvia lays a single
clutch. Mean clutch size was 18.3 eggs + 9.03 SD (range 7 –
30); they were laid at a depth of about 2 cm. Mean egg diameter
was 1.46 + 0.18 mm and that of hatchlings was 1.58 + 0.18
(range 1.45– 1.7 mm).
At Nea Karvali, young snails first appeared in November, and
reappeared from hibernation in March, but did not become
sexually mature until April of the following year, when their D
reached a mean of 12 mm. As at Paleokastro, growth was most
rapid in spring and, again, a proportion of them grew more
slowly than the rest, at least in 1990 (Fig. 4B). In general,
growth was much slower than at Paleokastro, especially in the
later stages of life. Judging by the observations on epiphragms
(Table 2), aestivation here is less continuous and consistent
than at Paleokastro. As at Paleokastro, the mating period
started in October and lasted only a few days, and egg-laying
was at its peak at the end of October. Mean clutch size was
57 + 32.9 eggs (range 17 to 95), laid again at a depth of
about 2 cm. Mean egg diameter was 1.00 + 0.14 mm (range
0.9– 1.1) and that of hatchlings was 1.1 + 0.27 mm (range
1.0– 1.2).
At Paleokastro, one generation appears per year. At Nea
Karvali, two generations are present throughout the year since
these snails live 2 years and mature in their second year. As at
Paleokastro, the size-class distribution is bimodal for both
cohorts (G89, G90) and the slower growing sections (approximately 10%) (G89b, G90b) form a recognizable split cohort
in April and August 1990, respectively (Fig. 4).
At Paleokastro, all snails hatch with dark bands, and these
persist throughout life in about 75% of the population
(Table 2). At Nea Karvali, however, only 1 or 2% of the
snails hatched with bands on their shells; these eventually
stopped appearing in some of them as the shell grew (Table 2).
Environmental variables are strongly seasonal in northern
Greece and so snails exhibit predictable oscillations in their
activity pattern. Summer drought and high temperatures
inhibit activity, as do low temperatures in winter. In both
sites, the breeding period of X. obvia is from late October to
mid-November, which is the favourable period for the rapid
development of juveniles. They stay buried in the soil during
winter. The low apparent densities at both places at the end of
autumn are due to the fact that at Nea Karvali some snails
entered dormancy so they could not be found, whereas at Paleokastro they started dying in October after reproduction. Growth
and activity did not occur during the adverse periods of winter
and of summer drought. Increased growth took place during
spring because temperatures were not exceedingly high
(around 108C) and total monthly precipitation did not fall
below 30 mm.
In Paleokastro, growth stops during the summer dry spell and
the genitalia and gonads mature, so that the snails are ready to
lay eggs before their death in autumn. In a good year, such as
1989, they can achieve in a few months an adult size not much
less than that achieved at Nea Karvali. The short period available for growth and development means that the achieved
adult size is more modest in less favourable years, leading to a
low mean clutch size. Eggs and hatchlings, however, are large.
Xeropicta obvia at Paleokastro is thus an annual, like Xeropicta
arenosa Ziegler (Lazaridou-Dimitriadou, 1981; Staikou &
Lazaridou-Dimitriadou, 1991).
At Nea Karvali, however, X. obvia matures in 2 years and
remains active (or at least visible) for longer periods during
summer hot periods. Hence at Nea Karvali, seasonality in
activity is not so pronounced, despite its apparently more
extreme summer climate. The extended period of growth
250
LIFE HISTORY OF XEROLENTA OBVIA IN GREECE
Figure 4. Modal distribution of Xerolenta obvia at Paleokastro (A) and Nea Karvali (B) from October 1987 to November 1990. G denotes the generations. The % figures denote the proportions of the different generations coexisting at Paleokastro or Nea Karvali.
Carter, 1977). There are, however, substantial differences in
life-cycle strategies between the two populations. At Paleokastro,
there is a short but very favourable season for growth. Laying
larger eggs increases the chances of juveniles reaching adult
size before that season ends. Aestivation while waiting for the
autumn rains is then the safest strategy. At Nea Karvali,
growth is slower because there are fewer days on which activity
is possible, and they are possibly spread over a greater part of the
year. Laying many, smaller eggs may be an appropriate
response to more favourable winter conditions. Taking
account of the different times taken to reach reproductive
usually results in larger adult size and hence substantially larger
clutches. Eggs and hatchlings are, however, small. This life cycle
pattern is the same as that of Monacha cartusiana at Edessa
(Staikou & Lazaridou-Dimitriadou, 1990).
Despite the higher rainfall at Paleokastro, it is clear that both
populations retain an essentially Mediterranean breeding
season: the summer is not a suitable time for egg and hatchling
survival and growth. In this respect, both populations differ from
those of other helicoid species in temperate climates further
north, where mating, egg-laying and hatching occur over the
late spring and early summer (Williamson, Cameron &
251
M. LAZARIDOU AND M. CHATZIIOANNOU
Table 2. Percentage of Xerenta obvia snails in aestivation (with an epiphragm), and the percentage with dark bands on the shell, at Paleokastro and Nea
Karvali in 1989.
With epiphragm (%)
Date
Paleokastro
Without bands (%)
Nea Karvali
Paleokastro
Nea Karvali
31/3/1989
0
0
0
98.4
9/5/1989
99.8
0
0
98
1/6/1989
54.9
0
0
98.1
0
25
99.2
30/6/1989
31/7/1989
21/8/1989
100
86.9
100
52.5
30.6
99
50.4
24.5
99.1
29/9/1989
99.4
25.2
99.1
29/10/1989
0
71.9
1.12
22
99.3
29/11/1989
0
0
22
99
maturity, actual fecundity per adult does not differ between
populations as much as clutch size alone would indicate.
Thermal properties of differently coloured snails may be related
to the fitness of different phenotypes in particular climatic conditions (Jones, Leith & Rawlings, 1977). The faintly or unbanded
snails at Nea Karvali probably heat up less than the darker ones
from Paleokastro when exposed to the sun. This would be an
advantage in the longer periods of dryness prevailing at Nea
Karvali, a semi-coastal habitat. The extended activity periods
may be assisted because their shell is not covered with dark
bands, as at Paleokastro, so they may be able to remain active
or above ground for periods in the summer months. Conversely,
the possession of dark bands in many snails at Paleokastro may
enable them to maintain activity at lower temperatures. Differences in thermal physiology can lead to different behavioural or
life cycle traits (growth rate, fecundity, mortality rates, etc)
(Abdel-Rehim, 1983, 1986, 1988; Cowie & Jones, 1985; Burla
& Costelli, 1993; Staikou, 1999).
While some of these conclusions are necessarily speculative,
the results show that the species can adopt quite distinctive
life-history patterns in populations relatively close to one
another, as a response to local climate.
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ACKNOWLEDGEMENTS
We would like to thank Dr E. Gittenberger of the Natural
Museum of Leiden for information on the systematic position of
Xerolenta obvia, as well as Dr V. Flari and Dr N. Eleutheriadis for
their technical help in the field. Finally we would like to thank
the referees and Dr R. A. D. Cameron for their valuable comments and corrections.
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