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Environmental impact of razor clam harvesting using salt in Ria Formosa lagoon (Southern Portugal) and subsequent recovery of associated benthic communities.

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AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009)
Published online 10 December 2008 in Wiley InterScience
(www.interscience.wiley.com). DOI: 10.1002/aqc.995
Environmental impact of razor clam harvesting using salt in Ria
Formosa lagoon (Southern Portugal) and subsequent recovery of
associated benthic communities
RITA CONSTANTINO, MIGUEL B. GASPAR, FÁBIO PEREIRA, SUSANA CARVALHO, JOÃO CÚRDIA,
DOMITÍLIA MATIAS and CARLOS C. MONTEIRO
Instituto Nacional de Recursos Biológicos, I. P./L-IPIMAR, Av. 5 de Outubro, s/n, 8700-305 Olhão, Portugal
ABSTRACT
1. Razor clams are found in different habitats ranging from sheltered systems (e.g. lagoons and estuaries) to
open coasts. They are distributed worldwide and comprise a small number of species of high economic value.
Depending on the specific habitat and species exploited, different mechanical and hand-harvesting techniques are
employed. While the environmental effects resulting from mechanized methods have been described by several
authors, the impacts caused by traditional hand-harvesting methods remain unknown. Therefore, a study was
undertaken in Ria Formosa lagoon (South of Portugal) addressing the environmental effects resulting from
harvesting Solen marginatus with salt.
2. No significant impact on the sediment was found; the main effect was an increase in salinity after covering
the area with salt, which decreased rapidly with the flood tide and after a few hours had returned to preharvesting levels.
3. No effects on benthic communities were observed, with similar fluctuation patterns recorded in control and
experimental areas, the observed differences being attributed to the natural variability of benthic populations.
4. Based on the results obtained in the present study, a razor clam fishery using salt in intertidal areas can be
considered environmentally ‘friendly’.
Copyright r 2008 John Wiley & Sons, Ltd.
Received 4 June 2007; Revised 25 May 2008; Accepted 2 June 2008
KEY WORDS:
razor clams; benthic communities; harvesting impacts; Solen marginatus; salt fishery
INTRODUCTION
Razor clams are distributed throughout the world, in Pacific,
Atlantic and Mediterranean waters. Razor clams are found in
habitats ranging from sheltered systems (e.g. lagoons
and estuaries) to open coasts. Depending on the species, they
can also be found from intertidal to subtidal areas at water
depths up to 70 m, and on sandy, sandy-mud or muddy
bottoms. In Europe, the important commercial razor clam
species are Ensis siliqua, E. minor, E. arcuatus and Solen
marginatus. These species live burrowed in the sediment
with the long axis of the shell orientated in the
vertical position, extending their siphons out of the
sediment to feed on suspended particles (Tebble, 1966;
Poppe and Goto, 1993; Tuck et al., 2000).
Worldwide, several mechanical and hand-harvesting
techniques are employed according to the habitat and species
exploited. In intertidal and shallow-subtidal areas, harvesting
is generally done by hand or using rudimentary tools; in
greater water depths, razor clams are usually captured either
by mechanical (Gaspar et al., 1994, 1998) or hydraulic dredges
(Robinson and Richardson, 1998; Tuck et al., 2000; Fahy and
Gaffney, 2001; Hauton et al., 2003a, 2003b).
In intertidal and shallow-subtidal areas of estuaries and
coastal lagoons of Europe, several harvesting methods are
used; namely salting (Fahy and Gaffney, 2001; Patiño, 2002;
Pyke, 2002; Gaspar and Constantino, 2006), using a stabbing
metallic rod (Lassuy and Simons, 1989; Sebe and Guerra,
1997; Gaspar and Constantino, 2006) or rakes, shovels and
grubber hoes (Sebe and Guerra, 1997). In shallow-subtidal
*Correspondence to: M.B. Gaspar, Instituto Nacional de Recursos Biológicos, I. P./L-IPIMAR, Av. 5 de Outubro, s/n, 8700-305 Olhão, Portugal.
E-mail: mbgaspar@cripsul.ipimar.pt
Copyright r 2008 John Wiley & Sons, Ltd.
ENVIRONMENTAL IMPACT OF RAZOR CLAM HARVESTING USING SALT IN A LAGOON
areas razor clam harvesting is also undertaken by divers, using
salting or hand-picking methods (Sebe and Guerra, 1997;
Pyke, 2002; Barón et al., 2004; Gaspar and Constantino,
2006).
Historically, fisheries management has focused on the
conservation of sustainable stocks of the harvested target
species. However, over the last two decades, the ecological
impacts of fishing activities on marine ecosystems have
received increasing attention. Concern about the secondary
environmental effects induced by fisheries in sublittoral areas
has become increasingly important (Dayton et al., 1995;
Jennings and Kaiser, 1998; Kaiser and De Groot, 2000;
Kaiser et al., 2001; Fulton et al., 2005). Minimization of the
negative secondary effects of fishing activities has become an
important component of fishery management plans and one of
the major purposes of management policies (Kaiser et al.,
2001; Badino et al., 2004). Consequently, managers of coastal
areas are sometimes required to assess the environmental
effects of a variety of disturbing activities on benthic
communities. This requires a good understanding of the
damage and the subsequent recovery processes of the
communities involved (Dernie et al., 2003). As a
consequence, over the past decade, the subsequent negative
environmental effects of several mechanical techniques have
been highlighted with many studies undertaken worldwide
(Hall et al., 1990; Kaiser et al., 1996; Hall and Harding, 1997;
Spencer et al., 1998; Thrush and Dayton, 2002; Badino et al.,
2004). Indeed, it is known that mechanical harvesting activities
modify or destroy benthic habitats, promoting sediment
changes, reducing biomass and diversity of communities
(Hall and Harding, 1997; Kaiser et al., 1998; Spencer et al.,
1998; Collie et al., 2000). However, the magnitude of these
impacts depends on the community, area disturbed, fishing
pressure, type of fishery and habitat itself (Brown and Wilson,
1997). Even though some of the environmental effects of the
previously mentioned activities seem to be known, the
potential effects resulting from some traditional harvesting
procedures are still unidentified.
The Ria Formosa lagoon is located in the south of
Portugal, where the razor clam S. marginatus has been
traditionally harvested with salt, both in intertidal and
shallow-subtidal areas. When the individuals burrow into the
sediment, they form galleries that are open to the sediment
surface by a hole called the ‘eye’. When the fishermen find an
543
eye they pour salt into it; the salinity inside the gallery rises,
ultimately reaching intolerable levels forcing the animal to
move towards the sediment surface, where the fishermen pick
them up easily by hand. In subtidal habitats, the harvesting
process is similar but is carried out by divers, using a bottle
containing a highly concentrated solution of salt and water.
When divers find a bed of razor clams, they spread the brine
solution over it, with the same effect.
Salting for razor clams is also carried out in other European
countries, such as Spain (Patiño, 2002), Ireland (Fahy and
Gaffney, 2001) and the UK (Pyke, 2002). However, to the
authors’ knowledge, the environmental consequences of this
activity are unknown making sustainable stock management
difficult.
The aim of the present work was to investigate the
immediate environmental effects of razor clam harvesting
with salt in an intertidal area, and to monitor the subsequent
recovery of the associated benthic community.
METHODS
Site description and sampling strategy
Ria Formosa lagoon (Figure 1) is a 55 km long mesotidal
lagoon located on the southern coast of Portugal (Algarve)
with a surface area of approximately 16 300 ha (Gamito and
Erzini, 2005). It is a barrier island system comprising
mainland, barrier islands, barrier platforms, inlet deltas and
shoreface (Gamito, 2006). The experiments were carried out
between August and November 2005, in an intertidal razor
clam fishing ground following a BACI (Before-After-ControlImpact) experimental design (Underwood, 1992; Smith, 1993),
aiming to investigate if the disturbance of the impacted area
caused a different pattern of change, from before to after
fishing, compared with the natural change in a control area.
The experimental design included three control plots and
three experimental plots with an area of 6 m2 (2 m 3 m) each
free from any perturbation, mostly fishing, during the study
period. Each plot was subdivided into 24 quadrats of 0.25 m2
each. To minimize interactions between plots, each of them
was located 6 m from the edge of any other plot. In the
experimental plots, razor clam harvesting was simulated by
covering the area with salt during low tide, but target species
Figure 1. Ria Formosa lagoon (southern Portugal) and the location of the study area (clam ground plot).
Copyright r 2008 John Wiley & Sons, Ltd.
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009);
DOI: 10.1002/aqc
544
R. CONSTANTINO ET AL.
were not removed from the experimental plot. It is worth
stating that in the present study the simulation of harvesting
with salt was exaggerated, since generally the fishermen only
pour salt into the sediment gallery excavated by the razor
clam, instead of covering all the area with salt. To assess the
effects of razor clam harvesting and the subsequent recovery of
benthic habitat, seven sampling surveys were undertaken:
before harvesting (B); 1; 2; 7; 14; 30 and 90 days after
harvesting. Environmental factors, namely temperature and
salinity were recorded in the interstitial water with a multiparameter sounder (YSI 556 MPS). Measurements were taken
at sampling times mentioned above and also 1 and 2 h after
salting. In both treatment and control plots, three quadrats
were randomly chosen and sampled. Within each quadrat,
three macrobenthic (0.006 m2 per corer) and two meiobenthic
(0.002 m2 per corer) samples were collected using corers. Each
quadrat was sampled only once. The macrobenthic and
meiobenthic material were sieved in situ through 500 mm and
63 mm mesh sieves, respectively, and samples were preserved in
a 4% solution of buffered formalin. In the laboratory, the
biological material was sorted and individuals were identified
to the lowest possible taxonomic level and counted. Species
identification was made according to Fauvel (1923, 1927);
Laubier and Ramos (1973); Katzman et al. (1974); Fauchald
(1977); Strelzov (1979); Campoy (1982); San Martin (1984);
Chambers (1985); George and Hartmann-Schröeder (1985);
Holthe (1986); O’Connor (1987); Fitzhugh (1989); Rainer
(1989); Pleijel and Dales (1991); Chambers and Garwood
(1992); Sigvaldadóttir and Mackie (1993), for annelids;
Tattersall and Tattersall, (1951); Tebble (1966); Naylor
(1972); Jones (1976); Lincoln (1979); Bellan-Santini et al.
(1982); Smaldon et al. (1993), for arthropods; Parenzan (1974,
1976); Macedo et al. (1999), for molluscs; and Nobre (1938),
for echinoderms. The individuals in the meiofauna
samples, were classified into major taxonomic groups and
counted.
Data analysis
Mean and standard deviation were calculated for all the
environmental factors, analysed for both control and
experimental areas and for each sampling period. The data
from each of the three macrofauna corers collected within a
quadrat were pooled prior to data analysis. The same
procedure was followed for meiofauna samples. Data were
analysed using both multivariate and univariate methods.
Macrobenthic and meiobenthic community structure was
analysed with respect to abundance (N), total number of
taxa (S), Margalef’s taxa richness (d), diversity (ShannonWiener index H0 ) and evenness (Pielou’s J0 ) indices (Krebs,
1994). These variables were calculated for both areas and for
each sampling date. The mean and standard deviation for the
most abundant taxonomic groups (Polychaeta, Bivalvia and
Gastropoda) in macrofauna samples were also calculated, for
both areas and for each sampling survey.
GLM ANOVA was performed only for macrofauna
samples, using STATISTICA v6.0, in order to detect
differences between control and treatment samples, during
the sampling period. These analyses were performed for the
number of taxa, number of individuals and for Polychaeta,
Bivalvia and Gastropoda abundance. Whenever significant
differences were observed (Po0.05), Tukey multiple
comparison tests were carried out.
Multivariate methods were used to assess for changes
in community structure. Ordination by non-metric
multidimensional scaling (MDS) using the Bray–Curtis
similarity index (group-average linkage method) calculated
from square-root transformed abundance data was used to
assess different patterns in the macrobenthic and meiobenthic
community structure. For both macro and meiofauna, significant
differences between control and experimental plots for each
sampling date were determined using a priori one-way analysis of
similarities (ANOSIM). MDS and ANOSIM analyses were
Figure 2. Temperature and salinity values (mean and standard deviation) measured in interstitial water, from control and experimental areas, during
the study period (B -before; I.A - immediately after; h - hours; d - days; control - grey; experimental - black).
Copyright r 2008 John Wiley & Sons, Ltd.
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009);
DOI: 10.1002/aqc
ENVIRONMENTAL IMPACT OF RAZOR CLAM HARVESTING USING SALT IN A LAGOON
performed using the PRIMER v5.0 software package (Clarke
and Gorley, 2001).
In order to relate the species composition of macrofauna
samples, a principal components analysis (PCA) was also
performed. The linear model (PCA) was chosen instead of the
unimodal model because the length of the gradient (maximum
1.372) was less than 3.0 (Lepš and Šmilauer, 2003). This
ordination technique reduces the variance of the data along
ordination axes. A diagram with the two ordination axes with
highest eigenvalues was produced with the samples and species
displayed. The distance between the sample points in the
545
ordination diagram is the Euclidean distance. The PCA
analysis was performed using the software CANOCO for
Windows V4.5 (ter Braak and Šmilauer, 2002).
RESULTS
Environmental parameters
Sea water temperature and salinity showed low variability
during the study period (Figure 2). Generally, the water
Figure 3. Mean and standard deviation of macrobenthic abundance (N, ind 0.018 m2), number of taxa (S, taxa 0.018 m2), diversity (H0 ), taxa
richness (d) and evenness (J’) (B - before; d - days; control - grey; experimental - black).
Copyright r 2008 John Wiley & Sons, Ltd.
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009);
DOI: 10.1002/aqc
546
R. CONSTANTINO ET AL.
Figure 4. Mean abundance (ind. 0.018 m2) and standard deviation for the most abundant macrofauna taxonomic groups. Data concerning control
and experimental plots, and all sampling surveys (B - before; d - days).
Table 1. Summary of the results of GLM ANOVA
No. Taxa (S) Abundance
(N)
P
Time
Treatment
Interaction 0.26
F
P
17.1
16.5 0.69
1.27 F
42.8
0.15
2.1
Polychaeta Bivalvia
P
F
P
F
Gastropoda
P
27.6 0.07 1.94 9.04 5
0.1
1.76 0.7
0.63 0.06
F
47.3
9.01
2
Po0.001; Po0.01; Po0.05.
temperature varied between 20 and 301C, except 90 days after
the beginning of the experiment, when lower values were
observed (161C). Salinity increased considerably in the
experimental plot after covering the area with salt, followed
by a decrease after 1 and 2 h with the flood-tide. After 24 h, the
salinity in experimental plots was similar to that in the control
plots and remained almost constant (36) during the study
(Figure 2).
Macrofauna
A total of 35894 macrofaunal individuals distributed among 82
taxa were collected and identified. Both control and
Copyright r 2008 John Wiley & Sons, Ltd.
experimental areas were dominated by Gastropoda followed
by Polychaeta, Oligochaeta, Bivalvia and Phoronida.
The majority of groups presented higher abundance values
in the control area. The control area also presented higher
values for total number of individuals and taxa.
During the study period, both control and experimental
areas showed a similar pattern of variation for mean
abundance (N) (Figure 3). Values decreased 1 and 2 days
after salting, increasing afterwards, reaching the highest values
90 days after (Figure 3). The number of taxa also fluctuated
similarly in both control and experimental plots. Values
decreased 1 day after the beginning of the experiment
followed by small fluctuations during the remaining study
period. In both areas, the highest number of taxa was observed
after 90 days (Figure 3). During the study period, all diversity
indices showed similar patterns of variation. Generally,
diversity (H0 ), taxa richness (d) and evenness (J0 ) were
slightly higher in the control area. All indices presented the
lowest values 1 day after salting (Figure 3).
Polychaeta abundance fluctuated during the study period
with abundances generally higher in the experimental plots
(Figure 4). Low values were observed in both areas 1 day after
salting, while the highest values were recorded in the
experimental plot after 7 days for experimental and after 90
days in the control plot (Figure 4). Bivalves were more
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009);
DOI: 10.1002/aqc
ENVIRONMENTAL IMPACT OF RAZOR CLAM HARVESTING USING SALT IN A LAGOON
547
Figure 5. Multidimensional scaling ordination (top) and cluster analysis (bottom) diagrams for macrobenthic data (black symbols–control area;
white symbols–experimental area; CB - control before; EB - experimental before; C - control; E - experimental; d - days).
abundant in the experimental area from the beginning of the
study until 7 days after salting but by 14 days higher numbers
were found in the control area than in the experimental plots
(Figure 4). Gastropods showed a similar pattern of variation
in both areas, but with higher values in control plots. The
number of gastropods decreased dramatically within the first 2
days after the beginning of the study before increasing during
the remainder of the study period (Figure 4) although at a
much greater rate in the control plots.
The results of the GLM ANOVA (Table 1) showed
significant differences for treatment and time factors for
most biological variables tested. The only exceptions were
abundance of bivalves and total abundance that presented
significant differences for treatment and time, respectively. The
number of taxa showed significant differences between
treatment and sampling periods (Table 1). However, the
Tukey test showed that those differences were not observed for
control and experimental areas when the same period of time
was considered (Table 2). Significant differences in abundance
were only observed for factor time (Table 1), but the
interaction between the two factors was also significant, not
allowing for further conclusions (Table 1). Polychaeta and
Gastropoda also presented significant differences between
treatment and sampling periods (Table 1). With respect to
Polychaeta, the Tukey test detected significant differences
between 2 and 7 days sampling periods and in relation to
Gastropoda significant differences were found between 1, 2, 7,
14 and 30 days (Table 2). For bivalves the Tukey test did not
Copyright r 2008 John Wiley & Sons, Ltd.
detect significant differences between control and experimental
areas for the same sampling period.
With respect to macrofauna samples, multidimensional
scaling (MDS) and cluster diagrams (Figure 5), showed two
main groups: Group A contained samples from control and
experimental areas collected 2, 7 and 14 days after salting.
Group B comprised samples collected before and 1, 30 and 90
days after the start of the experiment, in both control and
experimental areas. Concerning all sampling surveys, the
results of the ANOSIM test did not show significant
differences between control and experimental areas (Table 3).
Macrobenthic
assemblages
between
control
and
experimental areas were similar for each sampling date, the
samples formed small clusters with small differences between
them (Figure 6). The samples from the day after impact (1 day)
are closer to the samples before harvesting, meaning that
immediate effects of salting are not noticeable. The horizontal
axis accounted for 57.6% of the total variance and
discriminated three major groups of samples: before and 1
day without correlation, 2, 7 and 14 days with negative
correlation and 30 and 90 days, which are positively
correlated. The vertical axis accounted for 18.1% of the
variance, discriminating the first sampling dates after impact (1
and 2 days) from the remaining sampling dates (7, 14, 30 and
90 days). Ecologically, these differences are probably due to
small temporal fluctuations in the populations. As the most
important information regarding the present work concerns
the effects of salting and as the interpretation of the ordination
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009);
DOI: 10.1002/aqc
548
ns
ns
ns
ns
ns
ns ns
ns ns
ns
ns ns
ns ns
ns ns
ns
ns
ns ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns ns
ns ns ns
ns
ns
ns ns ns
ns ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
A total of 67961 individuals distributed among seven
taxonomic groups were identified and counted, for both
control and experimental areas. The most representative
groups were Nematoda, Copepoda, Ostracoda and
Polychaeta. Gastropods had the lowest abundance in both
areas.
During the study period, abundance values varied similarly
in control and experimental areas (Figure 7). Nevertheless,
abundance increased sharply within both areas 7 days after the
beginning of the study (Figure 7). Similarly, the number of
taxa (S) followed an identical pattern in both areas despite the
small fluctuations observed among areas and sampling
surveys. The lowest values, in both areas, were observed at
day 14 (Figure 7). All diversity indices varied similarly in both
areas, although higher values were recorded in the control area
(Figure 7). In both areas, diversity (H0 ) and taxa richness (d)
were lowest 14 days after salting. In relation to evenness (J0 )
the minimum value was registered 1 day after the beginning of
the experiment (Figure 7).
The MDS and cluster diagram (Figure 8) showed no
discernible groups, with no separation between control and
experimental areas and between sampling surveys. The results
of the ANOSIM tests did not show significant differences
between control and experimental areas (Table 3).
ns
ns
ns
ns
ns
14
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns ns
13
12
11
10
ns 9
8
7
6
5
4
3
ns ns
ns
ns
ns
2
14 1
13
12
11
10
9
8
7
6
5
4
3
Meiofauna
ns
ns
ns ns ns ns
ns ns ns ns ns ns ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
DISCUSSION
Copyright r 2008 John Wiley & Sons, Ltd.
Po0.001; Po0.01; Po0.05.
ns
ns
ns
ns
ns ns ns ns
ns
ns
ns
ns
ns
ns
ns
ns
ns ns ns ns
ns ns ns
ns ns
ns
B
1d
2d
7d
14d
30d
90d
B
1d
2d
7d
14d
30d
90d
C
C
C
C
C
C
C
E
E
E
E
E
E
E
1
2
3
4
5
6
7
8
9
10
11
12
13
14
14
13
12
11
10
9
8
7
6
5
4
3
2
Treat. Time 1
No. Taxa (S)
Table 2. Tukey test results of GLM ANOVA
1
2
diagram is straightforward, the differences between control
and impacted areas are small, and to facilitate the
interpretation of the species along the time gradient, only the
species present in 30 or more samples are presented (20 out of
87). The PCA ordination diagram (Figure 6) shows that
Bittium reticulatum, Hydrobia ulvae and Philine aperta
abundance differ along the time period (along the horizontal
axis). In fact, these taxa showed a decrease in abundance 2, 7
and 14 days after the beginning of the experiment, but after 30
and 90 days abundance was even higher than on the first two
sampling dates. Some taxa, such as Oligochaeta, Exogone sp.,
Heteromastus sp., Cirratulidae spp., Paridoneis lyra,
Phoronida, Tanais dulongii and Glycera, also increased in
abundance from the first sampling dates (before and 1 day) to
the remaining dates (along the vertical axis). Nevertheless, in
both cases, these trends were observed in both control and
experimental areas showing that they were not due to salting
but to other factors.
ns ns ns
ns ns
ns
Gastropoda
Polychaeta
R. CONSTANTINO ET AL.
Intertidal habitats are under huge human pressure and the
study of the structure of macrobenthic communities has been
widely used for detecting human-related impacts, becoming
one of the most common indicators (Baldó et al., 1999; Ellis et
al., 2000). It is known that a variation of environmental
factors, even if not for a prolonged period, may affect the
structure of benthic communities (Prescott, 2006). Thus, it was
expected that the drastic increase of salinity in sediment pore
water would cause the mortality of some individuals that were
exposed to high concentrations of salt, leading to changes in
the benthic community composition. However, results revealed
that salting does not have a detrimental effect on benthic
communities, as control and experimental areas showed
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009);
DOI: 10.1002/aqc
ENVIRONMENTAL IMPACT OF RAZOR CLAM HARVESTING USING SALT IN A LAGOON
549
Figure 6. PCA for macrofauna samples, for both control and experimental area, for all sampling surveys (CB - control before; EB - experiment
before; C - control; E - experiment; black symbols - control area; white symbols - experimental area; Nass pfe- Nassarius pfeifferi; Hydr ulv- Hydrobia
ulvae; Chon sp.- Chone sp.; Phil ape- Philine aperta; Bitt ret- Bittium reticulatum; Lori luc- Loripes lucinalis; Cera edu- Cerastoderma edule; Abra tenAbra tenuis; Rud dec- Ruditapes decussatus; Glyc tri- Glycera tridactyla; Para lyr- Paradoneis lyra; Cirr- Cirratulidae; Hete sp- Heteromastus sp.;
Exog sp.- Exogone sp., OLIG- Oligochaeta; PHOR- Phoronida; Tana dul- Tanais dulongii; Noto sp.- Notomastus sp.; Aon oxy- Aonides oxycephala).
Table 3. Results of ANOSIM test for macrofauna and meiofauna
data, comparing control and experimental areas for all sampling
surveys
Control-Experimental
Macrofauna
R
Before
1 day
2 days
7 days
14 days
30 days
90 days
0.37
0.52
0.07
0.35
0.04
0.11
0.63
Meiofauna
P
0.2
0.1
0.5
0.1
0.6
0.4
0.1
R
P
0.30
0.26
0.07
0.15
0.67
0.07
0.18
0.1
0.2
0.6
0.8
0.1
0.6
0.1
similar fluctuation patterns. Thus, the differences obtained
during the study period seem to result only from natural
variability of benthic population. This result probably
indicates that benthic communities in intertidal soft bottoms
areas are extremely resilient to episodes of environmental
stress, namely salinity changes. Many benthic invertebrates
have developed mechanical adaptations and are able to survive
within salinities of 70 to 80 (Berger and Kharazova, 1997).
Moreover, intertidal species are used to daily environment
changes between low and ebb tides (Vernberg and Vernberg,
1972; Widdows and Brinsley, 2002; Prescott, 2006), especially
during the summer when the temperatures are very high (in the
Algarve they may reach 431C).
Several hand tools are used to harvest razor clams in
intertidal areas, even though they either cause the immediate
death of the individual (metallic rod) or disturb the sediment
and the associated benthic organisms (rake, grubber hoe and
shovel) but the effects from the use of other rudimentary hand
tools in razor clam fisheries have never been studied. Sebe and
Guerra (1997) reported that the use of rakes, shovels and hoes
provokes slight morphological sediment changes, such as the
Copyright r 2008 John Wiley & Sons, Ltd.
formation of small humps and depressions. However,
according to these authors, these changes were no longer
visible a few hours after the impact. Although sediment is left
in situ, it is disturbed and its cohesive nature can be disrupted
and therefore finer particles can be washed away during
flooding (Kaiser et al., 2001; Hiddink, 2003) which may lead to
changes in sediment grain-size composition. On the other
hand, the use of hand-harvesting tools promotes sediment
aeration and oxygenation, which may lead to the release of
nutrients to the water column. Falcão et al. (2006) also showed
that sediment reworking through harvesting induced changes
in HPO2
4 pore water concentration during tidal inundation.
These authors found that phosphate released to the water
column in reworked sediments decreased up to two orders of
magnitude in sediments of muddy flats, whereas no major
differences were observed in sandy bottoms. This may be
problematic in eutrophication-sensitive sheltered areas.
Moreover, because coastal areas may be highly urbanized,
sediments from these areas can also be contaminated with
xenobiotics. Therefore, the disturbance of the sediment may
ultimately remobilize contaminants that can be incorporated
into species of commercial interest with potential consequences
for human health. The environmental impacts described before
are potentially higher when more mechanized fishing
techniques such as dredges and hydraulic dredges are used.
Several studies reported the deleterious effects of mobile gears
on ecosystems. These effects included changes in physical
characteristics of sediment (loss of the fines fraction and
change of seabed topography), water column (release of
nutrients and contaminants), associated benthic communities
(reduction of abundance and diversity) and target populations
(see review by Gaspar and Chı́charo, 2007 and references
therein)
Intertidal zones are high productive systems characterized
by high diversity. Moreover, very important ecological
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009);
DOI: 10.1002/aqc
550
R. CONSTANTINO ET AL.
Figure 7. Mean and standard deviation of meiobenthic abundance (N, ind 0.004 m2), number of taxa (S, taxa 0.004 m2), diversity (H0 ), taxa
richness (d) and evenness (J’) (B - before; d - days; control - grey; experimental - black).
communities can be found in these areas, emphasizing the
environmental importance of intertidal areas as habitat
(Prescott, 2006). Thus, based on these assumptions it is
worth mentioning that harvesting razor clams with
mechanical fishing techniques should be avoided in these
particularly sensitive habitats.
In subtidal habitats, the harvesting of razor clams is carried
out by apnea and scuba diving, even though the latter method
is prohibited. The present study did not evaluate the impact of
salting for razor clams in subtidal areas, but it is unlikely for
Copyright r 2008 John Wiley & Sons, Ltd.
there to be any negative effects, since the local increase of
salinity resulting from spreading a brine solution will be
immediately diluted or within a short period of time by
currents (M.B. Gaspar, pers. obs.). However, Muir (2003) in a
study carried out in the Clyde Sea, stated that adding salt to
the sea bed produced a high, localized increase in salinity at the
point of salting that persisted for much longer than expected.
The key to the rate at which dilution takes place depends on
the relative strengths of the brine solution, or size of the rock
salt crystals used by the fishers, and the tidal and current
Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 542–553 (2009);
DOI: 10.1002/aqc
ENVIRONMENTAL IMPACT OF RAZOR CLAM HARVESTING USING SALT IN A LAGOON
551
Figure 8. Multidimensional scaling ordination (top) and cluster analysis (bottom) diagrams for meiobenthic data (CB - control before; EB experiment before; C - control; E - experimental; d - days; black symbols - control area; white symbols - experimental area).
regime in the fishing area. Nevertheless, even if rock salt
crystals persist for long periods it is to be expected that the
environmental impacts would be much greater if mobile fishing
gear is used.
Despite the fact that direct effects caused by the salt fishery
on the target species were not a component of the present
work, some considerations should be made. Fishing razor
clams with salt does not appear to have negative consequences
for the target species, both in intertidal and subtidal areas, as
individuals are picked up by hand and no physical damage is
caused to the animals. In contrast, several methods, namely
hand tools and mechanized methods, potentially damage
individuals by cutting their siphons, ripping pedal muscles
and breaking their shells (Gaspar et al., 1994; Sebe and
Guerra, 1997; Robinson and Richardson, 1998). The fact that
the salt fishery does not damage or kill the target species is
extremely important, as some areas where the fishery takes
place are classified as B areas and therefore individuals must be
subjected to depuration before human consumption, which is
impossible if individuals are severely damaged during
harvesting.
Laboratory experiments showed that salting seems to affect
the physiological condition of razor clams, more specifically
their ingestion rate, excretion rate and re-burrowing capacity
(Diniz, 2004). In fact, the major problem associated with a salt
fishery in intertidal areas relates to the undersized individuals
discarded by fishermen on the sediment surface. These
individuals are removed from their galleries and do not reburrow immediately, therefore increasing the risk of predation
by wading birds feeding in intertidal areas, however, this is
Copyright r 2008 John Wiley & Sons, Ltd.
also a problem when hand tools are employed. By contrast in
shallow-subtidal areas undersized individuals removed from
galleries during salt fishery re-burrow almost immediately
(M.B. Gaspar, pers. obs.).
Based on the information gathered and the results obtained
in the present study, the razor clam fishery with salt can be
considered environmentally ‘friendly’, both in intertidal and
subtidal habitats, and therefore should be encouraged,
especially when the fishery is undertaken in sensitive
ecosystems like coastal lagoons and estuaries.
ACKNOWLEDGEMENTS
The authors would like to thank José Luı́s Sofia for technical
support during sampling surveys. The present study was
carried out within the framework of the SHARE project
‘Sustainable Harvesting of Ensis (Razor Shellfish)’ under the
INTERREG IIIB Programme–Atlantic Area and European
Union (FEDER programme).
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