SPECIAL FEATURE: EXTREME COLD SPELLS
Chilling damage to mangrove mollusk species
by the 2008 cold event in Southern China
Yi Liu,1 Mao Wang,1,† Wenqing Wang,1 Haifeng Fu,1 and Changyi Lu1,2
1Key
Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment & Ecology, Xiamen University, Xiamen 361102 China
2State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361102 China
Citation: Liu, Y., M. Wang, W. Wang, H. Fu, and C. Lu. 2016. Chilling damage to mangrove mollusk species by the 2008
cold event in southern China. Ecosphere 7(6):e01312. 10.1002/ecs2.1312
Abstract. The frequency, duration, and intensity of extreme cold events are widely regarded as primary
constraints on the upper latitudinal limits of mangroves. Little data are available on the consequences of
recovery (or lack thereof) of non-­floristic components of mangrove ecosystems after a disturbance caused
by cold weather. An unusually severe cold wave occurred in southern China in January 2008. The impact of
this cold event and the subsequent recovery of mollusks in a Rhizophora stylosa mangrove forest in southern
China were evaluated over a 3-­yr study from April 2007 to January 2010. The cold event caused significant
mortality of mollusks, which was rapidly followed by an increase in the populations of opportunistic species, and then their subsequent collapse within 6 months. Comparison with data collected in April 2007
(before the cold event) revealed that the density, biomass, and species richness of mollusks decreased by
87.5%, 80.6%, and 56.3%, respectively, except for a transient and compensatory increase in the numbers of
benthic mollusks (by 47.5%). Arboreal mollusks were more sensitive to the cold event than benthic species,
but both groups showed similar recovery trajectories. After 21 months, the density, biomass, and richness of
mollusk species still remained 9.4%, 13.2%, and 26.2% lower than pre-­event. Full recovery took more than
24 months. In comparison to mangrove vegetation, mollusks inhabiting mangroves appeared to be more
vulnerable to cold events, but also recovered faster. In conclusion, it took more than 2 yr for the species richness of mollusks to recover from the cold event, and the rate of recovery was slower for the arboreal type.
Key words: arboreal; benthic; cold event; mangrove; mollusks; Rhizophora stylosa; southern China; Special Feature:
Extreme Cold Spells.
Received 14 April 2015; revised 22 November 2015; accepted 5 December 2015. Corresponding Editor: J. Rehage.
Copyright: © 2016 Liu et al. This is an open access article under the terms of the Creative Commons Attribution
­License, which permits use, distribution and reproduction in any medium, provided the original work is properly
cited.
† E-mail: [email protected]
Introduction
its of mangroves (Stuart et al. 2007, Gilman et al.
2008, Krauss et al. 2008, Ross et al. 2009, Cavanaugh et al. 2014). Low temperature not only affects
the growth and reproduction of mangrove plants
(Stuart et al. 2007, Pickens and Hester 2011, Wang
et al. 2011) but also has an impact on the structure
and composition of mangrove communities over
Temperature is one of the most important environmental factors affecting mangrove distribution
worldwide. The frequency, duration, and intensity of extreme cold events are widely regarded as
primary constraints on the upper latitudinal lim v www.esajournals.org
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SPECIAL FEATURE: EXTREME COLD SPELLS LIU ET AL.
the long term (Stevens et al. 2006, Gilman et al.
2008, Ross et al. 2009, Mitra 2013). Much attention
has been focused on the physiological responses
of mangrove plants to low temperatures (Norman
et al. 1984, Yang et al. 1999, Stuart et al. 2007) and
on the damage to mangrove vegetation caused by
cold events in certain areas (Stevens et al. 2006,
Chen et al. 2010, Wang et al. 2011).
Mangrove vegetation contributes to habitat
complexity and diversity in the fauna associated with mangrove ecosystems (Hutchings and
Saenger 1987, Lee 1998). Leaf scorch and widespread defoliation are the predominant symptoms of low-­temperature damage to mangroves
(Chen et al. 2010, Wang et al. 2011). Vegetation
damage caused by low temperature will inevitably influence associated fauna, especially those
relying on detritus, as defoliation greatly alters
temporal detritus supply. Furthermore, ­extremely
low temperatures directly affect the early development, juvenile growth, reproduction, physiological metabolism, mortality, and distribution
of intertidal mangrove organisms, particularly
mollusks (Golikov and Scarlato 1973, Forsythe
et al. 2001, Galbraith and Vaughn 2009). As most
intertidal mollusks are sedentary or sessile, they
cannot easily escape environmental stress (Danulat et al. 2002) and thus are considered a sensitive indicator of environmental change. Chilling
damage affects the structure and composition
of mangrove plant communities (Stevens et al.
2006, Ross et al. 2009, Chen et al. 2010), but few
studies exist on the effects of cold events on the
fauna inhabiting mangrove systems.
Mollusks represent one of the most important
groups of mangrove macrobenthos in terms of
abundance and species richness (Macintosh et al.
2002) and play a critical ecological role in the
structure and function of mangrove ecosystems
(Macintosh et al. 2002, Ashton et al. 2003). Variation in the diversity and abundance of mangrove
mollusks has significant ecosystem consequences
(Li et al. 1998, Carlén and Ólafsson 2002, Fratini
et al. 2004), such as changes in waterfowl populations and communities (Mercier and McNeil
1994, Moreira 1997). Mollusk macrofauna biodiversity is regarded as an important indicator of
the resilience of mangrove ecosystems following
a disturbance (Macintosh et al. 2002).
The mechanisms of cold tolerance have been
well documented in intertidal mollusks (Aarset
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1982, Murphy 1983, Waller et al. 2006). However,
the focus has been on species in the supralittoral
or eulittoral zones of temperate or arctic regions,
and thus, almost all studies on the effects of low
temperature on intertidal mollusks have been
conducted at near freezing temperatures (Ansart and Vernon 2003, Sinclair et al. 2004, Waller
et al. 2006). All intertidal mollusks that have been
studied are freeze tolerant (Ansart and Vernon
2003). However, little emphasis has been placed
on the effects of chilling temperatures (>0°C) on
intertidal mollusks in subtropical areas (McLachlan and Young 1982), and there has been no research on the recovery processes of subtropical
mollusk species after a chilling event.
Additionally, although most studies have
shown that the frequency of cold events may
decrease with global climate change (Ross et al.
2009), the impact of cold damage in a warming
world will increase (Gu et al. 2008). The Intergovernmental Panel on Climate Change (IPCC
2007) documented that extreme weather events
have become more common globally. During
January 2008, an unusually persistent episode
of severe weather occurred in southern China.
This event was characterized by low temperatures and the occurrence of frozen precipitation
(Wang et al. 2008, Yin 2008). The number of continuous days with abnormally low and/or freezing temperatures broke records, dating back to
the winter of 1954/1955, in the lower reaches of
the Yangtze River Basin and in Guizhou Province
(Wang et al. 2008). The 2008 cold event caused
significant damage to mangroves in China (Jiang and Huang 2008, Li et al. 2009, Chen et al.
2010), including to the Rhizophora stylosa forests
at Gaoqiao, Lianjiang, Guangdong Province,
China (Chen et al. 2008, 2010). During this event
(from January 14th to February 4th), the lowest
recorded air temperature was 5.2°C (Fig. 1), and
the lowest surface seawater temperature was
11.0–12.0°C near Lianjiang. Therefore, we expected that the macrobenthos in the R. stylosa forests
would experience significant negative effects
from the cold episode.
To quantify the impacts of environmental
­disturbances, such as oil spills, topography changes, extreme temperatures, and cyclones on mangroves, and their subsequent recovery (Jackson
et al. 1989, Duke et al. 1997, Lewis 2005, Aung et al.
2013), research must track focal species after any
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SPECIAL FEATURE: EXTREME COLD SPELLS LIU ET AL.
Fig. 1. Daily mean air temperatures in Lianjiang, Guangdong, China, during the winters of 2008 (from
December 2007 to February 2008), 2009 (from December 2008 to February 2009), and 2010 (from December 2009
to February 2010). The shaded area indicates the duration of the 2008 cold event.
initial damage has occurred, and maintain records
of baseline ecological data prior to such events. If
these data are lacking, studies may be unable to
quantify the actual impacts and recovery trajectory
(Forde 2002). In April 2007, we initiated a study on
mangrove mollusks along the eastern coast of the
Beibu Gulf. Mangrove forests there experienced the
2008 cold event (Chen et al. 2010), which provided
the opportunity to evaluate the consequences of this
event in terms of variation in the mollusk community before (from April 2007 to January 2008) and
after the event (from April 2008 to January 2010).
Methods
Study area
The study was conducted at Gaoqiao, located
in the southern part of Yingluo Bay near Lianji­
ang, Guangdong Province, China (21°32.837′ N,
109°46.132′ E; Fig. 2), which is part of the
Zhanjiang National Nature Reserve since 1997,
and was designated as a Ramsar site in 2002.
Yingluo Bay is endowed with the largest single
block of mangrove forest in mainland China,
with a total area of 1200 ha. The bay experiences
Fig. 2. Location of the research site at Gaoqiao in southern Yingluo Bay in Lianjiang, Guangdong, China.
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Table 1. Plant community parameters of the studied Rhizophora stylosa forest and damage caused by the cold
event in 2008 at Gaoqiao, Lianjiang, Guangdong, China.
Parameters
Mean ± S.D.
(ind./m2)
0.2 ± 0.0
9.3 ± 1.1
4.1 ± 0.3
98.0 ± 1.6
20.5
19.2
45.0
Tree density
Diameter at breast height (DBH) (cm)
Canopy height (m)
Percent cover (%)
Percentage of dead individuals (%) †
Defoliation percentage (%) †
Leaf scorch percentage (%) †
† Data from Chen et al. 2010.
a maritime climate and constitutes a transition
region between the northern subtropical zone
and southern tropical zone. The annual average
rainfall is 1535 mm and annual average temperature is 23.0°C. The mean air temperature is
16.0°C in the coldest month (January), and the
lowest recorded temperature is 2.8°C. The bay
is subject to anomalous diurnal tides, with an
average tidal range of 2.5 m, with the highest
tidal range being 6.3 m. Mangrove forests in
this zone are dominated by Aegiceras corniculatum,
R. stylosa, and Avicennia marina, with varying
dominance at different locations. Previous research indicated that R. stylosa is more sensitive
to low temperatures than the other two species
(Chen et al. 2010), and thus, we selected a R.
stylosa forest for assessment in this study (Table 1).
The cold episode of 2008 was characterized
by daily minima below 10°C for 21 d, with the
lowest minimum air temperature being 5°C at a
station near the mangrove study site. The mean
temperature for the entire month of January was
12.9°C, significantly lower than the average January temperatures in the two preceding years
(15.8°C and 17.0°C in 2006 and 2007, respectively) and the two subsequent years (16.9°C and
16.8°C in 2009 and 2010, respectively, Fig. 1).
After the cold event, evident damage was observed in the R. stylosa trees. A study conducted in
March 2008 (2 months after the cold event) revealed
that 20.5% of mature trees died, while the surviving
trees lost 19.2% of their foliage, on average. Furthermore, 45.0% of the surviving foliage displayed
leaf scorch (Table 1). No mature propagules (hypocotyls) were observed in 2008. Although most
remaining R. stylosa trees flowered and produced
mature hypocotyls in 2009, the number of mature
hypocotyls of each terminal shoot was 70% less
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than in normal years. This pattern did not recover
until 2013 (unpublished data). This suggests that
the mangrove trees at Gaoqiao require at least 5 yr
to recover from a cold event of this magnitude.
Sample collection
From April 2007 to January 2010, 12 seasonal
samples were collected (in April, July, October,
and January, corresponding to spring, summer,
autumn, and winter, respectively) from arboreal
and benthic mollusk communities in the R.
stylosa forest. The sample collection in January
2008 was conducted during the cold event (15–17
January 2008). For arboreal mollusks, five quadrats (5 × 5 m, 100 m apart from one another)
were set randomly inside the forest and sampled
in every season and year (5 quadrats × 12
sampling events = 60 arboreal samples). All
specimens attached on trunks, stilt roots, and
other parts of trees were collected by hand
(Sasekumar 1974). Mussels and oysters were
harvested with knives. For benthic mollusks,
12 quadrats (25 cm × 25 cm, set as three quadrats along four transects 100 m apart from one
another) were randomly designated inside the
forest and sampled during each sampling event
(12 quadrats × 12 sampling events = 144 benthic
samples). Mollusks were collected by placing
a 25 × 25 cm wooden frame on the sediment
surface (Lu 2003, SOAC 2007) and sieving the
upper 30 cm of sediment through a 1-­mm mesh
(Alfred et al. 1997). The benthic sampling process was separate from the arboreal sampling
process. All the specimens were cleaned, identified to the species level, and then counted
and weighed using a portable electronic balance
(precision 0.01 g; BT124S, Sartorius, Germany)
to obtain wet weights. Unidentified specimens
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were preserved in 70% alcohol for further identification and classification in the laboratory.
To assess if benthic vs. arboreal fauna were exposed to differential temperature stresses during
a cold event, we collected air and surface soil temperature data in 2009–2010 (no recording instruments were deployed at the time of occurrence of
the 2008 cold event). From June 2009 to ­January
2010, daily average air temperatures were recorded by an Eddy tower for monitoring water
and CO2 exchange in mangrove wetlands. The
tower was established in 2009 near the assessed
R. stylosa forest. Air temperatures were recorded
at a height of 5 m (1 m above the canopy) by a
thermometer-­hygrometer (Model 107 temperature probe, Campbell Scientific Inc., USA), while
soil temperature (20 cm depth) was recorded by
a TCAV probe (Model 109 temperature probe,
Campbell Scientific Inc., USA).
s­ eparately to the benthic and arboreal faunas. The
data were log-­transformed or square-­root transformed when necessary to meet normality (Kolmogorov–Smirnov test) and homogeneity of variances assumptions prior to statistical analyses.
Analyses were carried out with SPSS version 17.0.
Results
Mollusk species and composition
In total, 18 mollusk species, comprising 14
gastropods and four bivalves, were identified
in the R. stylosa forest. The benthic fauna comprised five gastropods and one bivalve, while
the arboreal fauna comprised nine gastropods
and three bivalves. The dominant arboreal species
was Littoraria melanostoma, with the highest biomass (9.5 g/m2) and density (16.2 ind./m2) among
all observed species (October 2008). Benthic
species were dominated by Assiminea brevicula,
with a maximum biomass of 19.0 g/m2 and
density of 336.0 ind./m2 (April 2008). The total
range in density and biomass of the arboreal
type (1.3–12.9 ind./m2 and 1.1–8.2 g/m2, respectively) were much lower than those of the benthic
type (48.0–314.7 ind./m2 and 2.0–103.0 g/m2), but
the richness of the arboreal type (2–12 species)
was higher than that of the benthic type (1–4
species) (Fig. 3, Appendix S1).
Statistical analyses
Two models were constructed to assess cold
damage and recovery. In the first model, three
study periods (before the cold event and 1 and
2 yr after the event) were compared. The period
before the cold event comprised three sampling
events (from April 2007 to October 2007). The
periods 1 and 2 yr after the cold event comprised
four (from January 2008 to October 2008) and
five (from January 2009 to January 2010) sampling events, respectively. Variation in biomass,
density, and species richness between the period
before the cold event and the period 1 yr after
was evaluated to assess cold damage, and the
same parameters were evaluated between 1 and
2 yr after the cold event to gauge recovery.
In the second model, we examined finer temporal scale responses to the cold event to better
account for seasonality and better understand
the effects of the cold event on both faunas. We
compared biomass, density, and species richness in April 2007 (first sample in the study and
spring) to January 2008 (3 months after the cold
event) to evaluate the more immediate effects of
cold damage. To evaluate recovery in the same
season, the same parameters were evaluated between autumn pre-­cold event (October 2007) and
October 2009 (21 months after the cold event).
Variation in mangrove faunal parameters was
evaluated using one-­way ANOVAs, followed
by Tukey’s post hoc tests. Models were fitted
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The impact of the 2008 cold event on the density,
biomass, and species richness of mollusks
The 2008 cold event cause major reductions
in both the arboreal and benthic mollusk faunas.
The density, biomass, and species richness of
benthic mollusk species declined by 19.5%
(P = 0.018), 66.3% (P = 0.0001), and 45.3%
(P = 0.001), respectively, in the year following
the cold event. During the second year, no
recovery occurred. Instead, the density, biomass,
and species richness remained at levels that
were 43.2% (P = 0.0001), 49.1% (P = 0.0001),
and 35.3% (P = 0.001) lower relative to pre-­
event. For the arboreal mollusks, density, biomass, and species richness decreased by 78.6%
(P = 0.0001), 67.8% (P = 0.001), and 43.9%
(P = 0.0001), respectively, in the year following
the cold event. In the second year, this arboreal
fauna also remained at levels that were 53.2%
(P = 0.0001), 38.2% (P = 0.005), and 43.2%
(P = 0.0001) lower than pre-­event (Fig. 3). This
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Fig. 3. Variation in mollusk density, biomass, and species richness in a Rhizophora stylosa forest at Gaoqiao,
Lianjiang, Guangdong, China, during the study period. “Before Cold Event” denotes three sampling events
(from April 2007 to October 2007) before the cold event (January 2008). One and two years after the cold event,
mollusk parameters were again recorded (four dates from January 2008 to October 2008 and five dates from
January 2009 to January 2010).
suggests that chilling damage was extensive
on both benthic and arboreal mollusk populations. Further, these faunas failed to fully recover
by the end of the second year.
A finer examination of the declines in mangrove
mollusks revealed that the density of arboreal
species, dominated by L. melanostoma, decreased
by 87.5% (P = 0.0001) in April 2008 immediately after the event, relative to densities in April
2007. In contrast, the density of benthic mollusk
species, dominated by A. brevicula, increased by
47.5% (P = 0.003) during this period, with similar values to pre-­event levels by July 2008, yet
this increase was short-­lived (Fig. 4). In comparison with baseline values measured in October
2007 (144.0 ± 13.1 ind./m2), the mean density of
the benthic type increased to 154.7 ± 7.5 ind./
m2 (P = 0.374) 2 yr later (October 2009), while
the arboreal type showed a decrease of 26.3%
(P = 0.0001) (Fig. 4). Similarly, in comparison
with baseline values measured in April 2007,
the biomass of the arboreal and benthic types,
measured in April 2008, indicated a decrease of
85.1% (P = 0.0001) and 76.2% (P = 0.0001), respectively. In October 2009, these values were 8.4%
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(P = 0.365) and 17.9% (P = 0.032) lower, respectively, relative to April 2007.
Relative to baseline levels (April 2007), the richness of mollusks in April 2008 of the arboreal and
benthic types were lower by 50.0% (P = 0.011)
and 62.5% (P = 0.007), respectively. In comparison with the other baseline levels in October
2007, the species richness measured in October
2009 displayed decreases of 32.4% (P = 0.008) and
20.0% (P = 0.230) for the arboreal and benthic
types, respectively (Fig. 4). Some species, such
as Xenostrobus atratus and Laternula nanhaiensis,
were observed before the cold event, but then declined to undetectable levels at 2 yr after the cold
event (Appendix S1). In conclusion, it took more
than 2 yr for the species richness of mollusks to
recover from the cold event, and the rate of recovery was slower for the arboreal type.
Discussion
There are few studies on the influence of
e­ xtremely low temperatures caused by climate
change on mangroves and on their responses to
such events (Ross et al. 2009). The cold event in
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Fig. 4. Seasonal variation in mollusk density, biomass, and species richness in a Rhizophora stylosa forest at
Gaoqiao, Lianjiang, Guangdong, China, during the study period. The shaded area indicates the duration of the
cold event (2008).
January 2008 in China caused extensive damage
to R. stylosa trees at Gaoqiao. Chen et al. (2010)
estimated that at least 2 yr is required for the
recovery of reproductive output of these mangroves. Observations from our study suggest that
a time period of up to 5 yr or longer may be
necessary for mangrove trees in this region to
recover fully from the cold event. However, in
comparison with the severe mortality of mangrove
trees in the southern U.S. after a series of cold
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winters in the 1980s (Stevens et al. 2006), the
event assessed in this study was relatively minor.
Stevens et al. (2006) estimated that it would take
30 yr for Avicennia germinans forests to recover
from chilling damage recorded in the 1980s.
Generally, mangrove forests are highly resilient
to such environmental disturbances (Lugo 1998,
Ellison 2000, Lewis 2005, McLeod and Salm 2006).
They have a variety of key features that contribute
to their resilience, including self-­design and simple
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Fig. 5. Daily variation in air and soil (20 cm depth) temperatures in the studied Rhizophora stylosa forest at
Gaoqiao, Lianjiang, Guangdong, China, in January 2010.
architecture that enable rapid regrowth and
­rehabilitation post-­disturbance (Alongi 2008).
Therefore, in the absence of major mortality of
mangrove trees, mangrove vegetation may recover
relatively quickly after disturbances.
Extremely low temperatures affect the early development, juvenile growth, reproduction, physiological metabolism, mortality, and distribution
of intertidal mollusks (Golikov and Scarlato 1973,
Forsythe et al. 2001, Galbraith and Vaughn 2009).
A few mollusk species can migrate vertically (Williams 1970, Vannini et al. 2008) or dig deeply into
sediment (Murphy 1979, Ansart and Vernon 2003)
to escape extreme temperatures. However, most
species are unable to avoid such events. Although
all intertidal mollusk species that have been studied are freeze-­tolerant (Ansart and Vernon 2003),
freezing events lasting for more than a few weeks
can severely threaten population survival (French
and Schloesser 1996, Werner and Rothhaupt 2008).
Except for the dominant species L. melanostoma
that can resist chilling temperatures by switching to a dormant mode, most arboreal mollusks
are highly susceptible to cold weather, evidenced
through fluctuations in their density. Our results
suggest that the arboreal mollusk species are more
sensitive to cold events than the benthic ones.
Mangroves vary in their recovery rates, especially with respect to large-­scale disturbances.
Recovery periods can last from years to decades,
depending on the scale of the disturbance (Alongi 2008). Previous research has shown that most
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invertebrate communities display substantial recovery only a few years after major disturbances (Suchanek 1993). In the case of oil spills, it can
take 2–15 yr for intertidal invertebrates to recover
(Suchanek 1993). Our study indicated that it took
more than 2 yr for mollusks to recover from chilling damage. Combining our data with that from a
previous study on the impact of cold weather on
mangrove plants, Chen et al. (2010) suggest that although the mollusk species inhabiting mangroves
are more vulnerable to cold weather events than
mangrove plants are, the former recover more rapidly. Following a small-­scale disturbance (artificial
experimental clearance of mollusks) in southern
Brazil, mollusk assemblages displayed rapid recovery (Sandrini-­Neto and Lana 2014). Mollusk
reproduction is characterized by high reproductive
capability and a high level of reproductive redundancy (Galtsoff 1961, Bishop and Hackney 1987).
High fecundity, continuous reproduction, and fast
growth underpin their ability to rapidly recover.
Cold damage to intertidal mollusks has been
shown to be related to the intensity and ­duration
of exposure to low temperatures (Roland and
Ring 1977, Aarset 1982, Ansart and Vernon 2003).
We did not monitor air and soil temperatures
during the cold event. However, temperature
data collected in January 2010 provide some insight into a potential difference in vulnerability
between benthic and arboreal fauna. The soil
temperature varied between 13.9°C and 19.9°C,
while the air temperature varied between 10.6°C
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and 21.8°C (Fig. 5). The average soil temperature was 0.6°C higher than the air temperature
(16.8°C vs. 16.2°C) and tended to be more stable. This is because the saturated soils of mangrove forests have a large capacity to retain heat.
Therefore, it is likely that, during the cold event
in 2008, arboreal mollusks experienced lower
temperatures than the benthic mollusks. Except
for the dominant species L. melanostoma, most
arboreal mollusks were likely directly exposed
to the cold event, and accordingly displayed
the observed higher fluctuations in their density
(Fig. 4). Among the mollusk species, littorinids
are generally better adapted to temperature extremes and desiccation, via either behavioral or
physiological regulation, relative to most other
intertidal taxa (Murphy 1979, Clarke et al. 2000,
McMahon 2001, Sinclair et al. 2004). This includes
L. melanostoma, which can resist chilling temperatures by switching to a dormant mode, and thus,
exhibits high cold resistance and high fecundity.
After the cold event, the arboreal species were
collectively more sensitive than the benthic species, particularly in terms of density.
Although the populations of most benthic mollusk species decreased significantly following the
cold event, their density increased exponentially to an abundance of over 300 ind./m2 in April
2008. However, a population crash was observed
in July 2008 (Fig. 4). This may be explained by the
behavior of the opportunistic species A. brevicula. Severe mortality resulting from the cold event
created a niche vacancy, which in turn resulted in
compensatory growth of opportunistic species.
The species A. brevicula is a common mollusk in
mangroves and can tolerate freezing temperatures (Li et al. 2007). In addition, it is characterized by a low body weight (0.05 g/ind.), short
life-­span (Fortuin et al. 1981, Kurata and Kikuchi
1999), strong fecundity (Sada 2001, Suzuki et al.
2002), and ease of dispersal by currents (Abbott
1958). These traits may have allowed it to exhibit
a rapid increase in population size after a competitive release. Such large fluctuations in the
density of opportunistic species have also been
reported following other disturbances, such as
oil spills (Suchanek 1993).
In conclusion, chilling damage not only affected
the structure and composition of mangrove forests but also appeared to affect the sessile faunas
they support. Both arboreal and benthic mollusk
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species were significantly affected by the cold
event, and our findings indicated that recovery
was incomplete even 2 yr after the event. Variation
in the diversity and abundance of mollusk species,
particularly benthic mollusks, has remarkable
ecosystem consequences (Li et al. 1998, Carlén
and Ólafsson 2002, Fratini et al. 2004). These include changes to populations and communities of
high consumers such as waterfowl (Mercier and
McNeil 1994, Moreira 1997) and impacts on detrital food webs (Wells 1984, Proffitt and Devlin
2005). With respect to arboreal mollusks, sessile
species may affect the survival rate and growth
of mangrove seedlings (Fan et al. 1993), but little
information exists regarding their relationship
with mature mangrove forests. No significant
interactions between these two were observed
in our study. For example, certain boring organisms, such as Teredinidae species, drill holes and
live in mangrove trunks and may therefore influence mature mangrove trees (Zhou and Li 1986,
Huang et al. 1996). However, no significant effects
in this regard were detected in this study. Due to
the importance of mangrove management and
rehabilitation, further studies on chilling damage
to mollusk species with longer timeframes and simultaneous observations of other faunal groups
are necessary.
Acknowledgments
We gratefully appreciate the support of the staff
members at the Zhanjiang Mangrove National Nature
Reserve. We also thank Xueqin Gao, Zhiguang Geng,
Zhigang Tu, and Yanjun Liu for their assistance with
field work. Our special appreciation goes to Wenman
Liu and Xiaoli Mao for editing the final draft of
the article. This research was jointly supported by
the National Natural Science Foundation of China
(41276075) and the Natural Science Foundation of
Fujian Province, China (2013J01164).
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