383 MARTINS.cdr

Journal of Coastal Research
1814 - 1818
SI 39
ICS 2004 (Proceedings)
Brazil
ISSN 0749-0208
Effect of a Storm Event on Lysosomes of Haemocytes in Donax Hanleyanus
(Mollusca: Bivalvia) on Exposed Sandy Beaches of Santa Catarina State, Brazil
L. K. P. Martins†; V. R. Bellotto‡; E. S. Alves ¥ and P. C. de Brito‡
†1Instituto Brasileiro de Meio Ambiente,
IBAMA, R. Marechal Rondon s/n,
68181-010, Itaituba, Pará, Brazil,
[email protected]
‡ Centro de Ciências Tecnológicas da
Terra e do Mar, CTTMar, Universidade
do Vale do Itajaí, PO Box 360, 88302202, Itajaí, Santa Catarina, Brazil;
[email protected]
[email protected]
¥ Instituto de Biociências,
Pós-graduação em Ecologia,
Universidade de São Paulo, Rua do
Matão, Travessa 14, no 321, 05508-900,
São Paulo, Brazil, [email protected]
ABSTRACT
MARTINS, L. K. P.; BELLOTTO, V. R. ; ALVES, E. S. and BRITO, P. C., 2006. Effect of a storm event on
lysosomes of haemocytes in Donax hanleyanus (Mollusca: Bivalvia) on exposed Sandy Beaches of Santa Catarina
State, Brazil. Journal of Coastal Research, SI 39 (Proceedings of the 8th International Coastal Symposium), 1814 1818. Itajaí, SC Brazil, ISSN 0749-0208.
Lysosomal destabilization assays have been used as valuable biomarkers of pollutant exposures in a variety of
marine organisms. It is accepted by water quality monitoring programs (UNESCO) as useful in environmental
quality assessment. However, for the correct use of a stress index, it is necessary to know whether the investigated
response exhibits natural fluctuations related, for example, to seasonal cycle, short-term natural environmental
changes associated to tidal cycle or episodic events. The aim of this study, carried out on two different beaches, in the
Santa Catarina, Brazil, was to evaluate the effects of a storm event upon the populations of Donax hanleyanus, using
lysosomal destabilization assay. The selected beaches are exposed to wave action and represent different
morphodynamic types. Samples were taken before, during and after the storm event. At theses times, the beach
profiles, water temperature and salinity were monitored. Lysosomal stability was measured using the Neutral Red
dye retention time assay (NRR) in which stress-induced pathological alteration of the lysosomal compartment was
viewed by microscopy in live haemocytes exposed to neutral red. Both beaches showed a reduction in the lysosomal
retention capacity during the storm period, indicating cells injury. However, significant differences between the
control and the storm periods were observed only in the Taquara beach, which showed the highest sediment erosion
rate. There weren't significant changes on temperature or salinity during the studied period. These results suggest
that D. hanleyanus can be stressed by storm condition, but with different magnitudes conditioned by intensity of
environmental alteration.
ADITIONAL INDEX WORDS: Beach erosion, biomarker, neutral red assay.
INTRODUCTION
Due to the variety of human activities that potentially affect
ecological systems, it also is imperative to discriminate among
effects of specific types of disturbances. This requires
approaches that can isolate effects of particular activities from
nonhuman sources of natural variation (OSENBERG and
SCHIMITT, 1996).
Nowadays, environmental agencies and international
organizations have implemented methods for identification,
quantification and ecotoxicological evaluation of chemical
pollutants in monitoring program of marine environmental
quality. The available techniques includes biomarkers and sublethal biological responses to environmental chemicals, that
have been applied as sensitive “early warning” tools for
biological effect measurement. In this context, the effect
biomarker, the lysosomal membrane destabilization, has
proved to be one of the most suitable and sensitive procedures to
monitor risk areas (CARAJAVILLE et al., 2000).
The neutral-red retention assay makes use of the fact that
lysosomes in unstressed cells retain the neutral red dye for a
long time after uptake. In contrast, following uptake in stressed
cells, the dye will leak the lysosomes into the cytoplasm more
quickly, as indication of cell-membrane damage (LOWE et al.,
1992). The presence of high levels of organic pollutants (e.g.:
PAHs, PCBs) or heavy metals into these lysosomes can cause
the breakdown of their membrane and efflux of their acid
hydrolases and toxic contents to the citosol, resulting in cell
injury or even death, implied by the impairment of the ATPdependent proton pump (LOWE et al., 1992; RINGWOOD et al.,
2002).
The greatest part of studies have been developed with
organism that live in rocky intertidal habitats, or other suitable
hard substrate, while few studies considers organisms from
sandy beaches. However, sandy beaches have played an
important role as locations for recreation and as attractions upon
which tourism development has been based (ORAMS, 2000).
This uses of beaches for recreational and tourism purposes have
had significant environmental impacts (KLEIN et al., 2002b). In
addition, sandy beaches comprise three-quarters of the world's
coast line (WENNER, 1987 in SOULE and KLEPPEL, 1987). So,
the development and implementation of appropriate techniques
to assess environmental quality are imperative to promote
effective management on this system.
Nevertheless, sandy beaches are amongst the most dynamic
physical systems on the earth's surface (SHORT, 1999) and it can
be more difficult to distinguish human impacts from natural
process. Storms, with their high levels of wave action, present
one of the greatest hazards to sandy beaches and may
dramatically alter their physical and biological characteristics.
Vertical elevation changes of 2.5 m, mean shoreline
transgressions on the order of 50 m, and volume changes on the
2
3
order of 10 m /m of beach length can occur on time scales of
hours during storms (AUBREY, 1983).
Mussels, mainly from the family Mytilidae have gained
recognition as biomonitor organisms, serving to detect any
environmental disturbance (VIARENGO and CANESI, 1991) . For
tropical and subtropical sandy beaches, however, various
species of Donax seem to have the most potential as indicator
species (WENNER, 1987 in SOULE and KLEPPEL, 1987).
Lysosomal enlargement in mollusk hemocytes can be
induced by several natural environmental stressors, like
temperature, salinity, food available, tides and reproductive
cycles, besides organic and metallic pollutants (CARAJAVILLE
et al., 2000; RINGWOOD et al., 2002). Therefore, up to our
knowledge, there is no information about the effects on the
lysosomal membrane stability of bivalves haemocytes, when
exposed to a storm event and it's high wave energy.
So, the aim of this study was to assess the effects of a storm
disturbance upon the bivalve D. hanleyanus, using the stress
Journal of Coastal Research, Special Issue 39, 2006
Environmental Risk and Monitoring
biomarker lysosomal destabilization, on exposed sandy
beaches subjected to different sediment mobility, in order to
evaluate the usefulness of this specie on the environmental
quality monitoring. There are number of reasons to select D.
hanleyanus, as follow : a) it's a filter feeder (BROWN and
MCLACHLAN, 1990), being susceptible to accumulate
contaminants within its tissues; b) it's a common species in
Santa Catarina and other Brazilian sandy beaches, occurring
along all the morphodynamic spectrum (GIANUCA, 1987;
BARROS et al., 1994; SOUZA and GIANUCA, 1995; BORZONE
and SOUZA, 1997; ALVES and RODRIGUES, 2000; BARROS et al.,
2001); c) live in the intertidal zone (BROWN and MCLACHLAN,
1990), been easy to collect; d) it's one of the fastest burrower
bivalves of sandy beaches (MCLACHLAN et al., 1995), been
very adapted to this dynamic environment.
METHODS
StudyArea
Two beaches located in the central-north coast of the Santa
'
Catarina State (26o30'S and 27o20S)
were selected to this study
(Figure 1). These beaches are exposed to wave action and
represent different morphodynamic types.
Taquaras is a reflective beach with well selected coarse
sands (0.72 to 0.92 mm) and accentuated slope (10o) (MENEZES,
1999). It has a parabolic plan form, a N-S orientation (KLEIN et
al., 2002a) and its shoreline is 920 m long (MENEZES, 1999). It
is subject to high sediment mobility along the year and can
presents scarps of 2 m height during storm events (KLEIN and
MENEZES, 2001).
In contrast, Navegantes is a dissipative beach with well
selected fine sands (0.15 to 0.19 mm) and gentle slope (2.5 to
3.5o), subjected to low to moderated sediment mobility during
1815
the year (MENEZES, 1999). It has a very well developed frontal
dunes and a surf zone width between 54 and 83 m with a
multiple-bar system (KLEIN and MENEZES, 2001). It presents a
N-S orientation and its shoreline is 10,030 m long (MENEZES,
1999). Itajaí-açu River opens to the sea in northern extremity of
this beach, influencing coastal water quality up to 20 km north
of its mouth (SCHETTINI et al., 1999; SCHETTINI, 2002).
The local tides are semidiurnal with a maximum range of 1.2
m, but storm surges can raise at least on meter above the
astronomical tide (CARVALHO et al., 1996; TRUCCOLO, 1998).
Northeasterly winds are predominant along the year, but
southwesterly winds occur in winter and spring associated to
the arrival of cold fronts (NOBRE et al., 1986).
Sampling and DataAnalysis
Three sites were distributed along the two beaches (Figure
1). Samples were taken before (Jul 26, 2002 - control), during
(Aug 20, 2002) and after (22 and 25 Aug, 2002) a storm event,
occurred between 17th and 20th August 2002, on low tide.
During these samples, beach profiles were monitored with a
leveling instrument, as proposed by BIRKEMEYER (1981). In
order to compare consecutive beach profiles a fixed reference
point was adopted and the Interactive Survey Reduction
Program (ISRP) was used to analyze profile changes and to
compare sub aerial beach volume of sediments (BIRKEMEIER,
1986).
Wave break height (Hb) was visually estimated by two
different observers (one for each beach) and therefore it is not
comparable between sites. Sand samples were taken with a
plastic corer of 5cm diameter to a depth of 10cm for grain size
analysis (one sample) and determination of water content of
sediments (three samples). Samples were dried (at 60oC for 12
hours) and sieved through graded screens (0,5 intervals) to
compute mean grain size according to FOLK and WARD (1957).
The water content of sediments was estimated as the loss in
weight of wet sands after drying (at 50oC for 72 hours). Water
temperature and salinity was obtained by a thermometer (0.1oC
of precision) and a refratometer (precision of an unity),
respectively. These environmental data were obtained only for
the central site (1 and 3) of each beach.
Living specimens of D. hanleyanus were collected by hand
from each site and immediately transported to laboratory.
Animals were measured for shell length (mm) and acclimated in
aquarium contend filtrated sea water with the same salinity of
each sampling site and used for assays.
About 20 individuals from each site were analyzed. The
haemolymph was withdrawn (0.1 0.3 ml) by small needle
aspiration from the anterior adductor muscle (MARTINS, 2001)
into a 0.1 ml of saline solution (filtrated seawater pH 7.36 and
salinity 31). The stock solution was diluted to 0.2% in the same
seawater. The use of seawater corrected for the ideal pH
becomes the protocol more cheap and practical. Lysosomal
stability was measured using the Neutral Red dye Retention
time assay (NRR) in which stress-induced pathological
alteration of the lysosomal compartment was viewed by
microscopy in live granular haemocytes exposed to neutral red
solution, an acidotropic weak base (RASHID et al., 1991). The
time was registered when the cells showed abnormal shapes,
intense enlarged red lysosomes and leakage of membrane
(LOWE et al., 1992).
Storm effect on D. hanleyanus was tested for each site by one
way Analysis of Variance (ANOVA) and significant differences
between times was assessed by the use of a posteriori Tukey's
test (ZAR, 1996).
RESULTS AND DISCUSSION
Figure 1. Study area and sample sites illustrative figure.
On both beaches, the height of incident waves peaked during
the storm event (20th August), and decreased afterwards (Table
1). The increasing in wave energy had different effects on
sediment remobilization of beaches studied (Figure 2). It results
in a high beach profile change on Taquaras (Figure 2B), where a
Journal of Coastal Research, Special Issue 39, 2006
1816
Martins et al.
total of 8.8 m3/m of sediment was removed from sub aerial
beach (Table 1), and in lower changes on Navegantes (Figure
2A), where only 1.2m3/m of sediment was eroded (Table 1).
After storm, Taquaras presented a fast profile restoration
besides Navegantes showed slight but progressive profile
erosion (Figure 2 and Table 1).
In fact, the wave energy required to induce beach cut are
dependent on beach state (WRIGHT and SHORT, 1984).
Dissipative beaches accommodate higher waves by causing
them to break further seaward on the gentle nearshore slope
thereby dissipating their energy over a wider surf zone. So, this
beach state is suited to high storm waves, and consequently
experiences little erosion during storm events (SHORT, 1999).
For other hand, reflective beaches are most susceptible to
increment in waves conditions, and experiences intense and fast
erosion. However, erosion is usually followed by rapid beach
accretion on this morphodynamic state (SHORT, 1980, 1999).
Temporal variation induced by storm event was not
observed on other environmental factors (Table 1). However, a
progressive decrease of salinity was recorded on Navegantes
along the study period. Salinity was slight lower on this beach
(Table 1).
Differences in animals size were observed between beaches.
The biggest bivalves always were collected on Taquaras beach
where shell length varied between 13 and 38mm. In
Navegantes, shell length varied between 15-24mm and
1728mm on sites 1 and 2, respectively. Both beaches showed a
reduction lysosomal retention capacity during storm event
(Figure 3). However, significant differences between control
period (before storm) and storm periods (p<0.05) were only
observed on Taquaras (Table 2) that showed the highest
sediment erosion rate (Table 1 and Figure 2B).
On this beach, a restoration of neutral red retention capacity
was recorded with the transition from storm to calm conditions
(Figure 3A) but this trend was not significant different (Table
2).
Lysosomal responses on molluscs can be induced by a wide
range of factors like food availability, low temperatures
(CAMUS et al., 2000) and seasonality during the annual cycle
(ETXEBERRIA et al., 1995), suggesting that this group is
susceptible to stress when natural changes occur. Results
obtained in this study corroborate this observations.
D. hanleyanus is an intertidal burrower that needs to
maintain their position (or to regain it once lost) on the shore to
survive (BROWN and MCLACHLAN, 1990). So, it suggest that a
higher energy expenditure is necessary under intense sediment
erosion, because animals need to burrow very fast to avoid be
displaced from the beach with sediment. This fact would
explain the reduction lysosomal retention capacity observed
during storm event on Taquaras beach (Figure 3A), where an
intense erosion rate was recorded (Figure 2B). These results
3,5
control
storm
two days after
one week after
3,0
2,5
Height (m)
2,0
1,5
1,0
0,5
0,0
-0,5
A
-1,0
0
5
10
15
20
25
30
35
40
45
50
55
60
65
70
75
Distance (m)
3,5
control
storm
two days after
one week after
3,0
2,5
Height (m)
2,0
1,5
1,0
0,5
0,0
0,5
B
-1,0
0
5
10
15
20
25
30
35
40
Distance (m)
Figure 2. Beach profiles of Navegantes (A) and Taquaras (B).
X-axis indicates distance of the dunes.
suggest that D. hanleyanus can be affected by this natural
physical process, but with different magnitudes conditioned by
the intensity of alterations that storm can exert on
environmental conditions.
There are only a few field studies, which have shown that
biological indicators may reflect just a successful homeostatic
response of bivalves to drastic natural events, demonstrating the
important role that the lysosomal system plays in this individual
homeostasis (WEDDERBURN et al., 2000). Nevertheless, each
organism varies with respect the degrees of support capability
of environmental changes on the metabolic processes.
Therefore, the variability of responses between individuals is
Table 1. Environmental factors recorded on Taquaras and Navegantes beaches along study period. S: salinity in the surf zone; T: water
temperature in the surf zone; Hb: wave height.
Taquaras
Data
Control
Storm
Two days after
One week after
26-Jul
20-Aug
22-Aug
27-Aug
S
T( C)
o
Hb
(cm)
Mean Grain Size
(mm)
Water Content of
Sediments (%)
Sediment
3
Volume (m /m)
Sediment
3
Exchange (m /m)
33
32
32
29
19
19
19
22
86
144
115
97
0.72
0.75
0.72
0.66
16.7
17.0
16.1
16.2
58.8
50.0
50.9
54.8
---8.8
0.9
3.9
S
T( C)
o
Hb
(cm)
Mean Grain Size
(mm)
Water Content of
Sediments (%)
Sediment
3
Volume (m /m)
Sediment
3
Exchange (m /m)
33
29
28
24
19
20
20
23
63
117
107
63
0.16
0.18
0.17
0.18
Navegantes
Data
Control
Storm
Two days after
One week after
26-Jul
20-Aug
22-Aug
27-Aug
19.2
18.7
19.2
19.4
Journal of Coastal Research, Special Issue 39, 2006
42.6
41.4
39.8
38.7
----1.2
-1.6
-1.1
1817
NRR time (min)
Navegantes beach -site2
NRR time (min)
Navegantes beach -site1
NRR time (min)
Taquaras beach
Environmental Risk and Monitoring
100
90
80
70
60
50
40
30
20 A
10
100
90
80
70
60
50
40
30
20 B
10
100
90
80
70
60
50
40
30
20 C
10
organisms with biggest frequency can reduce this possibility
and minimizes the influence of a wide diversity of natural
changes; as such, this can lead to a better understanding of the
mechanism of adaptation of D. hanleyanus during the natural
modifications on the sandy beaches.
The results of these studies illustrate once again that
lysosomes can undergoing the influence of the natural changes,
as strong wave action, being necessary include this observation
on the interpretation of results.
LITERATURE CITED
control
two days after
storm
one week after
date
Mean
±SE
±SD
control
two days after
storm
one week after
date
control
two days after
storm
one week after
date
Figure 3. Mean neutral red retention time ( standard deviation)
in haemocytes lysosomes of D. hanleyanus collect from the
Taquaras (A) and Navegantes (B and C) beaches during the field
experiment.
very high (DEPLEDGE and RAINBOW, 1990).
The integrated approach, including use of biomarkers and
chemicals analysis, on the assessing the environmental quality,
have been conducted in tropical or subtropical environments for
better interpretation of contaminant impact on marine
organisms (NASCI et al., 2000). However, natural variables, like
temperature and salinity, can interfere on the elucidation of any
biological responses to toxic substances, complicating the
interpretation of results (NASCI et al., 2000).
Probably, the individuals that experiment a storm event, with
intense sediment remobilization as on Taquaras beach, are more
vulnerable to pollutant-induced stress because these organisms
already be living near their stress tolerance limits. So, the toxic
effects of contaminants, on naturally stressed individuals yet,
possibly occur with more frequency and severity.
Although these natural factors could interfere in the
interpretation of results of NRR assay, a monitoring of
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Journal of Coastal Research, Special Issue 39, 2006