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LOCOMOTOR ACTIVITY PATTERNS OF THE MANGROVE
LITTORINIDS, LITTORARIA ARDOUINIANA AND
L. MELANOSTOMA, IN HONG KONG
OLIVE H. K. LEE AND GRAY A. WILLIAMS
Department of Ecology & Biodiversity, University of Hong Kong, Pokfulam Road, Hong Kong
(Received 12 November 2001; accepted 21 January 2002)
ABSTRACT
Littoraria ardouiniana and L. melanostoma are common in Hong Kong mangrove forests. The locomotion of these snails is constrained to their host trees and, therefore, affected by physical factors
experienced in the tree canopy. To investigate factors that affected the activity of these Littoraria species,
in situ observations and experiments were conducted. Observations suggested that the littorinids were
inactive in daytime, except when it rained, and active at night, even without stimulation by rain. All
littorinids crawled downwards when they started moving in the evening and returned close to their
initial height after their activity period. Spraying with freshwater to simulate rain initiated movement.
Since most individuals were located above the high water mark and subject to terrestrial conditions,
the littorinids were not influenced by tidal change on a daily basis, but were activated by rain. It
appears that physical factors, most likely desiccation stress, strongly influence the activity patterns of
these two littorinid species within the mangrove tree canopy.
INTRODUCTION
The activity patterns of intertidal gastropods are controlled
by biological and physical factors, and are often triggered by
environmental cues (proximate stimuli), such as photoperiod,
light intensity, tidal change, lunar cycle, water movement,
wave action, and gravity (Newell, 1979; Underwood, 1979;
Hawkins & Hartnoll, 1983; Chelazzi, Focardi & Deneubourg,
1988; Little, 1989; Chapman & Underwood, 1992). Most intertidal molluscs on rocky shores are active when they are submerged by the tide, both by day and at night (see reviews by
Branch, 1971; Hawkins & Hartnoll, 1983; Little, 1989). Some
species, especially on tropical shores, however, are active when
washed by waves, and are inactive during emergence and submergence (Hawkins & Hartnoll, 1983; Garrity, 1984; Williams
& Morritt, 1995; Hodgson, 1999), while rain may inhibit activity
(Little, Morritt, Paterson, Stirling & Williams, 1990; but see
Fretter & Graham, 1962). The behaviour of some intertidal
animals is, however, related to both tidal and diel cycles (e.g.
Little & Stirling, 1985).
Many intertidal animals tend to become active and feed only
at night (Underwood, 1979; Branch & Cherry, 1985). Some
species may feed both by day and night, although their activity
is often greater at night (Hawkins & Hartnoll, 1983; Hodgson,
1999). Light is a cue for movement in Littorina obtusata (L.),
L. saxatilis (Olivi), and Melaraphe neritoides (L.) (Evans, 1965;
Underwood, 1979). Some species are restricted to daytime foraging as their activity may be limited by their orientation to
light during homing and/or by the nocturnal activity of predators (reviewed by Hawkins & Hartnoll, 1983).
The activity patterns of intertidal organisms are also limited
by environmental stresses. Desiccation, for example, is thought
to be an important factor in the evolution of the timing of
foraging patterns (Little, 1989). Since the drying effects of the
wind and sun can terminate foraging (Newell, 1979), inactivity
during daytime low tides protects against desiccation (Chapman & Underwood, 1992). On sunny days, littorinids withdraw
Correspondence: G. A. Williams; e-mail: [email protected]
J. Moll. Stud. (2002) 68: 235–241
into their shells, close their opercula and attach their shells to
the rock with mucus, limiting contact with the hot substrate,
and thus reducing heat and desiccation stresses (Newell, 1979;
Garrity, 1984). Since desiccation stress is minimal during the
night, gastropods often feed while the tide is out at night
(Newell, 1976). Most siphonarian and lottiid limpets, as well
as littorinids, have been suggested to forage only when awash
during the rising and falling tide to avoid the risks of desiccation and predation (Newell, Pye & Ahsanullah, 1971; Hawkins
& Hartnoll, 1983).
The activity of intertidal animals is also affected by biological
factors, such as predation. Littoraria irrorata (Say), for example,
climbs Spartina stems to avoid predation by crabs (Warren,
1985). On rocky shores, Nerita funiculata (Menke) is inactive
during nocturnal low tides to prevent predation by crabs
(Levings & Garrity, 1983), while many limpets forage only when
awash at the edge of the rising and falling tide supposedly to
reduce the risk of attack by terrestrial and marine predators
(Hawkins & Hartnoll, 1983).
In mangrove forests, animals may exhibit different activity
patterns compared to rocky shore species as the physical conditions, such as substratum, wave action, tidal change, physical
stress, and also biotic interactions, differ greatly between these
two habitats. In mangroves, snails often enter a resting stage
when trees are dry and feed only during wet periods, i.e. after
rainfall or high tide (Gallagher & Reid, 1979; Kohlmeyer &
Bebout, 1986), and rain and dew are major environmental cues
that stimulate activity (Little & Stirling, 1984; Jensen, 2000).
Unlike rocky shore gastropods, most mangrove species are
inactive when submerged because feeding may be more efficient out of water (Hartnoll, 1988). Some mangrove snails and,
indeed, most Littoraria species, migrate with the tide to remain
above the water surface and only feed above the high water
mark (Kohlmeyer & Bebout, 1986; Ohgaki, 1992; Duncan &
Szelistowski, 1998; Jensen, 2000).
Littoraria ardouiniana (Heude) and L. melanostoma (Gray) are
common in Hong Kong mangroves (Morton & Morton, 1983;
Walthew, 1995; Lee, 2001), where they occur on various mangrove tree species (Reid, 1986, 1992a). The activity of these
© The Malacological Society of London 2002
O. H. K. LEE & G. A. WILLIAMS
littorinids is likely to be affected by physical factors, especially
wetting by water that may play a role in triggering the activities
of these littorinids. The present study aims to investigate the
activity patterns and the physical factors that affect these
patterns in L. ardouiniana and L. melanostoma in Hong Kong
mangroves.
Are littorinids stimulated to become active by rain?
An experiment to investigate the impact of rain on littorinid
activity was performed at Sheung Pak Nai on 15 June 1998 from
14:30 to 18:30, when there was no natural rain and the tide did
not immerse the mangrove trees. Sixty Littoraria ardouiniana
and L. melanostoma were haphazardly chosen on both Kandelia
candel and Aegiceras corniculatum (n 2 littorinid species 2
tree species 60 individuals 240). The littorinids were
divided into four groups (each with 30 L. ardouiniana, and 30
L. melanostoma on K. candel and A. corniculatum). The first group
was sprayed with distilled water (water temperature 32°C)
five times using a spray bottle; the second group was sprayed
with seawater collected from the site (temperature 31°C,
salinity 2‰); the third group was blown with dry air using a
dust remover; and the fourth group received no treatment.
After each treatment all littorinid groups were monitored for
3 min, which was sufficient time for the littorinids to react and
the number of moving littorinids was recorded. Nominal logistic models were used to test the null hypothesis that the littorinids were not activated by water and/or air movement, and
Likelihood ratio tests (Edwards, 1992) were performed. The
factors tested included the two littorinid species, the two different tree species and the responses (percentage of littorinids
starting to move) to the four treatments.
MATERIALS AND METHODS
When are mangrove littorinids active?
Activity patterns of Littoraria ardouiniana and L. melanostoma on
the most common Hong Kong mangrove species; Kandelia
candel and Aegiceras corniculatum, were monitored in a mangrove of about 1 ha at Sheung Pak Nai (22° 27 N, 113° 58 E),
New Territories, Hong Kong. Forty-five mature (shell length
12 mm) L. ardouiniana (20 on K. candel and 25 on A. corniculatum) and 43 mature (shell length 11 mm) L. melanostoma (20
on K. candel and 23 on A. corniculatum) were lightly marked
with Tipp-Ex (Tipp-Ex GmbH & Co. KG, Germany). As the
animals were not numbered, individuals were located on different trees to avoid confusion. The locations of the animals were
marked by brightly coloured tags attached to convenient
branches, which aided relocation of the littorinids.
Activity of the littorinids was recorded hourly from 11:00 to
21:00 on 20 April 1998, then every 1.5 h after this, due to the
longer time needed to locate the animals at night. Observations at night were made with white light, but shining the light
directly on the littorinids was avoided. The percentages of
moving littorinids on the two mangrove species were calculated
at each time interval. As the same individuals were recorded
throughout the observation period, no statistical analysis was
attempted.
Only the vertical positions of the littorinids were measured,
in terms of height above ground (1 cm); no attempt was
made to score horizontal movement within the canopy. Variation in the elevation of the littorinids before and after foraging
was analysed with a three-factor ANOVA, with time (at the
beginning or end of the study; 10 random individuals chosen
for each time), snail (the two littorinid species), and tree (the
two mangrove species) as fixed, orthogonal factors (n 2
times 2 snail species 2 tree species 10 individuals 80).
Air temperature and relative humidity were recorded under
the canopy at the edge of the mangrove forest every hour.
Times of sunset and sunrise, high tide and low tide, tidal levels,
and the time of rainfall were also recorded. At the end of the
study, shell lengths of the marked snails were measured using
Vernier calipers (0.1 mm).
Does the timing of littorinid activity correspond to high
tide?
Littorinid behaviour at high tide was investigated at Sheung
Pak Nai in the daytime on 22 March 2000. Thirty individuals of
Littoraria ardouiniana and L. melanostoma located above and
below the high water mark (HWM approximately 10–24 cm
above the ground), were haphazardly located before, during,
and after the high tide. The number of littorinids moving was
recorded about 2 h before the time of the highest tidal level,
during the high tide (2.1 m above CD), and about 1 h after the
high tide. Since it was difficult to observe the littorinids located
below HWM during the high tide survey, these data were not
recorded [n (30 individuals 2 species) 3 observations
above HWM and two observations below HWM 300]. A nominal logistic model was used to test the null hypothesis that the
behaviour of the littorinids was not influenced by the time of
high water and likelihood ratio tests were performed. The
factors tested were the two littorinid species, the two locations
and the three different times.
RESULTS
Are mangrove littorinids active at night when there is
no rain?
When are mangrove littorinids active?
Daytime air temperature ranged from 23 to 32°C, while the
relative humidity (RH) was 50–80%. At night, air temperature
remained at about 22°C, while RH ranged from 88 to 94%.
Periods of rain (30 min) occurred at night and in the early
morning (Fig. 1). High tides were at 15:00 on 20 April (2.2 m
above CD) and at 8:00 on 21 April (1.7 m above CD). The mean
shell length of Littoraria ardouiniana (SE) was 17.14 0.46
mm, and that of L. melanostoma 16.04 0.48 mm. The shell
lengths of the two littorinid species on the two mangrove
species were not significantly different (2-factor ANOVA; snail
tree; P 0.05).
Only a few littorinids moved during daytime (i.e. 7:00–18:00),
but activity increased greatly at night after rain (Fig. 1). There
were two main peaks of activity. The first at 19:00 occurred in
both species, whereas the second was at 3:00 in L. ardouiniana
and 4:00 in L. melanostoma (Fig. 1). The percentages of moving
During the 24-h watch rainfall occurred at night. To attempt to
separate the influence of darkness and rainfall on the activity
patterns of littorinids, additional observations were made at
Sheung Pak Nai just after sunset, from 17:30 to 21:30 on 29
June 1998. No rainfall occurred during this period. Fifty individuals of Littoraria ardouiniana and L. melanostoma, half on
Kandelia candel and half on Aegiceras corniculatum, were haphazardly chosen, and the number of moving littorinids, air temperature, and relative humidity were recorded every hour. Air
temperature and relative humidity were also recorded every
hour. The variation in activity of the two littorinid species on
the two mangrove species over the entire watch period was
analysed with a two-factor ANOVA, with littorinid (snail) and
tree species (tree) as fixed, orthogonal factors (n 2
littorinid species 2 tree species 5 observation times 20).
236
LOCOMOTOR ACTIVITY OF MANGROVE LITTORINIDS
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littorinids were similar in the two littorinid species and on the
two mangrove species (Fig. 1).
All littorinids moved downwards when they started moving in
the evening at 19:00 (Figs 2 and 3). Some L. melanostoma
descended to the tree bases and onto the mudflat, although
they did not touch the water since the tide level was low.
Littoraria ardouiniana also moved downwards but most remained
at a higher vertical position than L. melanostoma on the tree
trunks and in the canopy. Littoraria melanostoma on Kandelia
candel and L. ardouiniana on Aegiceras corniculatum started
moving upwards after 21:00 (Figs 2 and 3), while the other
combination of species started moving upwards after midnight
(Figs 2 and 3). In general, most littorinids moved upwards
before 6:30 and stopped moving after 9:30. The mean elevation
of the littorinids was not significantly different before and after
activity (Table 1, mean net vertical displacement (SE) of
L. ardouiniana on K. candel and A. corniculatum was –1.53 0.64 cm and 0.47 0.66 cm, respectively, while that of L.
melanostoma on K. candel and A. corniculatum was –0.68 0.65
cm and –0.78 0.48 cm, respectively).
Are mangrove littorinids active at night when there is no rain?
During the observation period the air temperature decreased
from 32°C at 17:30 to 26°C at 21:30, while the relative humidity
increased from 60 to 75%. The tidal height was about 0.4 m
above CD at 21:30 and did not immerse either the littorinids
or the trees. Many L. ardouiniana and L. melanostoma became
active after sunset (at about 18:30; Fig. 4). More than half of the
L. melanostoma had started to move by 21:30 (Fig. 4), while less
than 30% of L. ardouiniana had moved by this time (Fig. 4).
The overall percentages of littorinids moving over the entire
sampling period were not, however, significantly different
between the two littorinid species nor on the two tree species
(two-factor ANOVA; tree, snail, and tree snail; P 0.05).
Are littorinids stimulated to become active by rain?
Air temperature ranged from 32 to 34°C and relative humidity
between 60 and 65% during the study. The littorinids responded
differently towards the three treatments and the control
(Fig. 5), significantly more moving after being sprayed with
freshwater than after the other treatments and in the control,
which were similar to each other (liikelihood ratio test, df 3,
2 32.76, P 0.001; Fig. 5). The number of moving littorinids did not vary significantly between different mangrove
trees (Likelihood ratio test, df 1, 2 0.27, P 0.603); however, more L. melanostoma moved than L. ardouiniana (Likelihood ratio test, df 1, 2 9.80, P 0.002).
Does the timing of littorinid activity correspond to high tide?
Most littorinids did not generally move during daytime (Table
2). Before the high tide less than 20% of L. ardouiniana and less
than 7% of L. melanostoma located above the high water mark
(HWM) were moving, while 50% of L. melanostoma located below
the HWM were moving as the substrata were wet. The numbers
of moving littorinids below HWM was significantly higher
than above HWM (likelihood ratio test, df 1, 2 29.97,
P 0.001) and significantly more L. melanostoma were moving
than L. ardouiniana (likelihood ratio test, df 1, 2 9.21,
P 0.002). The numbers of moving littorinids before, during
and after the high tide were also significantly different
(Likelihood ratio test, df 1, 2 25.14, P 0.001), and the
littorinids were most active before the high tide.
DISCUSSION
Observations in the mangrove revealed that the littorinids were
inactive during daytime, but were active at night, especially in
rain (as also recorded for land snails; Staikou, 1999). There
were two peaks of activity at night, one in the evening and one
at midnight. These peaks may have been triggered by rain.
Previous studies (e.g. McMahon & Britton, 1985) have shown
mangrove littorinids to be inactive during daytime and to
attach their shells to the trees with mucus during prolonged
exposure to air. This behaviour is thought to reduce desiccation (Newell, 1958a; Mayes, 1962; Hawkins & Hartnoll, 1983;
Garrity, 1984) and heat stress (Vermeij, 1971). In the mangrove
canopy, littorinids may be limited by water availability, but they
require much water for physiological needs (e.g. mucus production; Lee & Davies, 2000). In some Malaysian mangroves,
seawater only reaches littorinids at bi-weekly intervals and these
littorinids are, therefore, subjected to terrestrial conditions
for long periods with only rainfall as a source of water (Berry
& Chew, 1973; also see Ohgaki, 1992 for an example from
Japanese mangroves). In many Hong Kong mangroves, seawater may only reach the bases of mangrove trees during high
tide (personal observation). Rain, therefore, appears to be an
important source of water for mangrove littorinids.
Figure 1. Percentage of moving Littoraria ardouiniana and L. melanostoma
during an observation in Sheung Pak Nai mangrove. Arrows onset of
rainfall; white bar daytime; black bar night time; black dots and solid
lines littorinids on Kandelia candel; white dots and dashed lines littorinids on Aegiceras corniculatum.
237
O. H. K. LEE & G. A. WILLIAMS
The activity patterns of Hong Kong mangrove littorinids are
similar to mangrove littorinids in Australia, where foraging
occurred mainly at night (Reid, 1992b). In the mangrove habitat in Hong Kong, air temperature decreases and relative
humidity increases in the evening, and the littorinids become
active after sunset, even without stimulation from rain or the
tide. On a rainless night, intensity of activity did not differ
between the two littorinid species, but both species were more
active on Aegiceras corniculatum than Kandelia candel. This difference in activity may be because the leaves of A. corniculatum were
more wet than those of K. candel (personal observation), since
the leaves of A. corniculatum excrete salt water (Hodgkiss, 1986).
When active, the littorinids moved down the trees in the
evening, and later moved up and stopped moving in the morning, thereby maintaining their overall vertical distribution (see
Newell, 1958b; Hawkins & Hartnoll, 1983). It has been suggested that most littorinids initiate activity by moving downwards (i.e. showing a positive geotaxis) to carry out feeding
excursions after periods of desiccation, i.e. under non-stressful
conditions (Newell, 1958b), while the upward movement (i.e.
positive phototaxis) after feeding was influenced by light
(Bingham, 1972). The littorinids may move downwards at
night to forage from the lower tree levels, because the nutritional value of leaves is relatively low and these animals are
known to feed on a mixed diet of mangrove plant tissues and
epiphytic microflora (Lee, Williams & Hyde, 2001).
Simulation of rain showed that both L. ardouiniana and L.
melanostoma, like other mangrove littorinids (Little & Stirling,
1984; Kohlmeyer & Bebout, 1986; Jensen, 2000), are stimulated
to become active by rain. More littorinids moved after spraying
with fresh water than with low salinity seawater, further supporting the idea that tidal inundation does not play a role in
littorinid activity. Agitation caused by blowing with air did not
produce an obvious effect, suggesting that wind action was
not an important environmental cue for activity. More L.
melanostoma initiated movement during the experiment, suggesting that this species responded more vigorously to rain
than L. ardouiniana.
Figure 2. Mean vertical elevation of Littoraria ardouiniana (n 11–24,
SE) and L. melanostoma (n 10–20, SE) on Kandelia candel during an
observation in Sheung Pak Nai mangrove. Numbers varied because during
some night time periods relocation of snails proved difficult. Arrows onset of rainfall; white bar daytime; black bar night time.
Figure 3. Mean vertical elevation of Littoraria ardouiniana (n 3–20, SE)
and L. melanostoma (n 10–23, SE) on Aegiceras corniculatum during an
observation in Sheung Pak Nai mangrove. Numbers varied because during
some night-time periods relocation of snails proved difficult. Arrows onset
of rainfall; white bar daytime; black bar night-time.
238
LOCOMOTOR ACTIVITY OF MANGROVE LITTORINIDS
Since the littorinids do not feed on dry substrata, daytime
provides limited opportunities for feeding. As the mangroves
become more cool and moist at night, dew on the leaf surfaces
may enhance littorinid activity. Temperature appears to have a
minor influence on the activity of mangrove littorinids (Jensen,
2000; although sometimes this is not the case, see Henry,
McBride & Williams, 1993), and activity is enhanced by rain,
since littorinids appear to prefer to forage on wet substrata.
Immersion by the incoming tide did not, however, influence
overall activity of the population, as most littorinids were
located above the high tide. Individuals located below HWM
showed no movement, even when immersed (OHKL, personal
observation).
Most littorinids were inactive during daytime, even during
high tide periods. More L. melanostoma moved than L. ardouiniana in daytime, although L. melanostoma located above the
HWM were inactive. The high activity of L. melanostoma might
be because this species is always located at lower levels on the
trees (Lee, 2001) and they crawl on the wet surfaces of the
trunks after high tide. More littorinids moved before the high
tide, although this may be an artefact as observations were
made in the early morning, when the leaves were still wet
because of dew, which might stimulate activity. As the leaves
dried, the littorinids became inactive, regardless of the state of
the tide and attached themselves to the leaves with mucus. This
suggests that mangrove littorinids in Hong Kong do not
Table 1. Three-factor ANOVA to investigate variation in vertical position of
the two littorinid species, Littoraria ardouiniana and L. melanostoma (snail),
on the two mangrove species (tree) at the beginning and the end of the 24-h
watch (time) (n 10). Significant P-values (P 0.05) are indicated in bold.
The variances were homogeneous (C 0.25, P 0.05). SNK multiple comparison tests were conducted where appropriate.
Source of variation
Figure 4. Percentage of moving Littoraria ardouiniana and Littoraria melanostoma during an evening observation in Sheung Pak Nai mangrove. Black
dots and solid lines littorinids on Kandelia candel; white dots and dashed
lines littorinids on Aegiceras corniculatum.
df
SS
MS
F
P
Time
1
0.11
0.11
1.48
0.228
Snail
1
2.43
2.43
32.04
0.000
Tree
1
0.59
0.59
7.84
0.007
Time snail
1
0.01
0.01
0.00
0.971
Time tree
1
0.01
0.01
0.10
0.755
Snail tree
1
0.75
0.75
9.92
0.002
Time snail tree
1
0.02
0.02
0.27
0.607
0.08
RES
72
5.45
TOT
79
0.36
SNK tests
Tree species
x Snail species
Aegiceras corniculatum
Littoraria ardouiniana L. melanostoma
Kandelia candel
Littoraria ardouiniana L. melanostoma
Snail species
x Tree species
Littoraria ardouiniana
Kandelia candel Aegiceras corniculatum
Littoraria melanostoma
Kandelia candel Aegiceras corniculatum
Table 2. Number of moving Littoraria, located below or above the high
water mark (HWM), before, during, and after high tide.
Below HWM
Figure 5. Percentage of littorinids moving (n 60): C Control; AIR blown with air; FW sprayed with freshwater; SW sprayed with seawater;
KC Kandelia candel; AC Aegiceras corniculatum; LM Littoraria melanostoma; LA L. ardouiniana.
239
Above HWM
L. ardouiniana
L. melanostoma
L. ardouiniana
L. melanostoma
n 30
n 30
n 30
n 30
Before
4
15
5
2
During
No record
No record
0
0
After
1
10
0
0
O. H. K. LEE & G. A. WILLIAMS
respond to high tide, because most are not touched by seawater
and only those located below HWM might respond to high
tides in the daytime. Since few individuals are found below
HWM at any time, littorinids in Hong Kong mangroves may not
be threatened by marine predators. In salt marshes, Littoraria
irrorata feeds during low tide and ascends plant stems to avoid
inundation by the high tide to escape predation, since the risk
of predation by fish and crabs is greater under water than in the
air (Hamilton, 1976; Warren, 1985). The Australian mangrove
littorinids Littoraria articulata (Philippi, 1846), L. intermedia
(Philippi, 1846) and L. scabra (Linnaeus, 1758), which are
located low on mangrove trees, perform daily migrations to
avoid submersion, whereas L. filosa (Sowerby) and L. philippiana (Reeve, 1851), which were found higher on the trees, only
made occasional journeys down to the water level (Reid,
1992b). The mangrove littorinids in Hong Kong did not, however, perform migrations with the tidal cycle.
In summary, Littoraria species in Hong Kong spend the
majority of their benthic stage on the mangroves, their habitats
effectively being their hosts. Activity was stimulated by water,
especially rain, and also occurred at night, both at times with
and without rain. These littorinids did not respond to tidal
change unless the substratum became wet, for they mostly
occur above HWM. It can be concluded that the locomotory
behaviour of the mangrove littorinids was mostly controlled by
physical factors related to desiccation stress.
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ACKNOWLEDGEMENTS
Dr Kevin Hyde and colleagues of the Hard Rock Ecology
Group, Department of Ecology & Biodiversity, University of
Hong Kong, are thanked for assisting in fieldwork and commenting on the manuscript. Special thanks to Carol Lau,
Cecilia Szeto and the Lee family for assisting in the 24-h watch.
Miss Kelly Lau is thanked for technical support. O. H. K. Lee
acknowledges a HKU Postgraduate Studentship.
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