Download Some effects of marine reserve protection on the population

AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 1 – 9 (2001)
Some effects of marine reser7e protection on the
population structure of two spearfishing target-fish species,
Dicentrarchus labrax (Moronidae) and Sparus aurata
(Sparidae), in shallow inshore waters, along a rocky coast
in the northwestern Mediterranean Sea
J.-Y. JOUVENELa,* and D.A. POLLARDb,1
a
Laboratoire d’Ichtyoécologie Tropicale et Méditerranéenne, Ecole Pratique des Hautes Etudes,
Uni6ersité de Perpignan, France
b
Centre d’Océanologie de Marseille, Uni6ersité de la Méditerranée, Station Marine d’Endoume, Marseille, France
ABSTRACT
1. The relative abundances of two highly sought after spearfishing target-fish species,
Dicentrarchus labrax (Linnaeus 1758) and Sparus aurata Linnaeus 1758, were compared using
underwater visual censuses in shallow ( B5 m) inshore waters along rocky shores inside and outside
a marine reserve area in the northwestern Mediterranean Sea (Banyuls-sur-Mer region, France).
2. The relative abundances of these two species were consistently lower outside the reserve area,
which comprised around 40% of the 25.6 km of inshore coastal waters surveyed.
3. The demographic structure of D. labrax was also different inside and outside the protected
area, the proportion of larger fish being significantly higher in the marine reserve.
4. The direct and indirect impacts of spearfishing are postulated to explain the distributional and
population structural characteristics of these two species in the shallow waters off this rocky coast.
5. Prohibition of spearfishing has favoured the persistence of these species during summer (the
main spearfishing season) in the shallower inshore waters inside the area of the
Cerbère/Banyuls-sur-Mer marine reserve.
6. These preliminary results indicate the need for additional work in this area and further
surveys to ascertain spearfishing impacts on target-fish species in the vicinity of other marine
protected areas.
Copyright © 2001 John Wiley & Sons, Ltd.
KEY WORDS:
marine reserve protection; spearfishing; target species
INTRODUCTION
The population enhancement role of marine reserves is now well established for fish assemblages in
warm-temperate Northern Hemisphere waters. Several studies have shown that this ‘reserve effect’
* Correspondence to: Dr Yves-Jean Jouvenel, Laboratoire d’Ichtyoécologie Tropicale et Méditerranéenne, Ecole Pratique des
Hautes Etudes, CNRS URA 1453, Université de Perpignan, 66860 Perpignan Cedex, France. E-mail: [email protected]
1
Present address: New South Wales Fisheries Research Institute, Cronulla, New South Wales, Australia.
Copyright © 2001 John Wiley & Sons, Ltd.
Received 30 August 1999
Accepted 25 July 2000
2
J.-Y. JOUVENEL AND D.A. POLLARD
influences the population dynamics of commercially and recreationally important target-fish species.
Densities are generally higher in protected areas (e.g. Bell, 1983; Garcia-Rubies and Zabala, 1990), and
demographic structure differs significantly in the relative abundance of larger individuals (e.g. Bell, 1983;
Bayle-Sempere and Ramos-Espla, 1993; Dufour et al., 1995), both of which in turn result in greater
biomass (Francour, 1991). Seasonal variations in abundance and size structure are also reduced in
protected areas, resulting in the presence of a relatively more stable and permanent fish fauna (Francour,
1994). Some authors, however, have argued that species diversity (or total number of species, i.e. species
richness) is only weakly correlated with reserve protection. Nevertheless, at small spatial scales the species
composition of fish assemblages can be affected by human pressures while overall species richness may
remain stable (see Roberts and Polunin, 1991 for discussion of community effects). Some species which
are particularly targeted by spearfishers may tend to avoid the more heavily fished areas, which
commonly lie at shallower depths. The behaviour of larger and more mobile target-fish species thus seems
to be significantly altered by spearfishing, one consequence being that they move to deeper waters
(Harmelin, 1987). Total protection against fishing, and particularly spearfishing, seems to restore a
broader and more natural depth range for these species (Harmelin et al., 1995). The broad question of the
usefulness of marine protected areas in fisheries management is most recently reviewed by Sumaila et al.
(1999).
In France, the specific impacts of spearfishing on coastal fish assemblages have not yet been assessed,
though a few case-studies are available from warm-temperate waters in Australia (Hill, 1985; Johnson,
1985; Lincoln Smith et al., 1989) and elsewhere.
Spearfishing is a largely recreational activity, occurring mostly during the warm season (June to
September) in shallow inshore waters in the northwestern Mediterranean Sea. However, since 1989 two
spearfishing competitions have also been held annually in the Banyuls-sur-Mer area, in March and
October. These competitions have each involved about 180 competitors and many spearfishers train all
year round for this event.
In order to determine the possible impacts of spearfishing, we censused populations of two important
target-fish species (Dicentrarchus labrax and Sparus aurata) in the shallower inshore waters along the 25.6
km of rocky coast in the Banyuls-sur-Mer region, to the south of cape Bear, France, during mid-summer.
We used underwater visual censuses to assess the effects of the Cerbère/Banyuls-sur-Mer marine reserve
on the densities, demographic structures and spatial distributions of these two species.
THE SPECIES, STUDY AREAS AND METHODS USED
The main aim of the study was thus to investigate the apparent impact of spearfishing on two target-fish
species of high economic and recreational importance in the Mediterranean coastal fisheries, the moronid
D. labrax (European seabass) and the sparid S. aurata (gilthead seabream). These two species are
particularly targeted by spearfishers because of their excellent eating qualities and their high score values
in competitions. D. labrax and S. aurata are both sporadic in their occurrence, and their relative
abundance varies seasonally in this area: i.e. they are more abundant in shallow waters in winter, outside
the main spearfishing season (Chauvet et al., 1992). The feeding behaviour of the two species differs in
that D. labrax feeds essentially on fishes and crustaceans together with some cephalopods (Whitehead et
al., 1986), while the diet of S. aurata comprises mainly bivalve molluscs together with some crustaceans
and fishes.
The inshore coastal waters study area was surveyed over 25.6 km of shoreline from Cape Bear to
Terrimbau Bay (Figure 1). This area contains several different shallow water (i.e. B 5 m depth) habitats
variably distributed along the coastline. The overall percentage lengths of each habitat type in this region
were 35% flagstones (smooth rocky slopes), 45% blocks, and 20% pebbles and sands, the latter occurring
Copyright © 2001 John Wiley & Sons, Ltd.
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 1 – 9 (2001)
EFFECTS OF MARINE RESERVE PROTECTION ON SPEARFISHING TARGET SPECIES
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Figure 1. Spatial distribution of abundances of D. labrax and S. aurata off the study area shoreline between Cape Bear and
Terrimbau Bay, southwestern France.
Copyright © 2001 John Wiley & Sons, Ltd.
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 1 – 9 (2001)
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J.-Y. JOUVENEL AND D.A. POLLARD
mainly in small bays (Jouvenel, 1997). Underwater visibility in the area over the study period averaged
greater than 5 m. The marine reserve area extends along 40% of the shoreline, i.e. for about 10 km (see
Figure 1). Spearfishing is prohibited throughout the marine reserve, although other fishing practices are
allowed along 70% of the marine reserve coastline. We investigated the presence of the two target-fish
species in shallow (i.e. between 0 and 5 m depth) inshore coastal habitats, generally within 5 m of the
shoreline, depending on the bottom slope, between 5 and 11 July 1995. The study area was divided into
64 contiguous sections, each 400 m long. Target fish could be readily counted in this zone. The
underwater visual census was carried out over a period of 7 days, representing 50 h of observation time
by two snorkel divers. All D. labrax and S. aurata seen were counted and their total lengths estimated for
each separated 400 m section while snorkelling along the shoreline.
The distributions and observed abundances of these two species were then plotted on a map of the
coastline. The 25 sections of the protected and the 39 sections of the unprotected area were each used as
replicates in the analyses. Statistical analysis was performed using an unpaired non-parametric test of the
mean densities of each species (Mann – Whitney U test). In addition, we computed the coefficient of
variation (CV= 100 ×S.D./mean) in order to assess the heterogeneity of the two species’ spatial
distributions along this shoreline. The size distribution of D. labrax was compared between protected and
unprotected areas using a chi-square test on size frequency classes. For S. aurata, however, numbers of
fish in the samples from outside the reserve were not large enough to perform this test.
RESULTS
Abundance data showed a high degree of difference between the protected and unprotected areas for the
European seabass (D. labrax). Mean density in the marine reserve was 3.929 5.96 per 400 m, compared
to 0.6991.04 per 400 m outside the protected area; this difference was highly significant (p= 0.0002). The
heterogeneity of the spatial distributions seemed to be roughly equivalent, the coefficients of variation
inside and outside the reserve both being around 150% (152.0% versus 150.7%, respectively, see Table 1).
The demographic structure of D. labrax also varied between the protected and unprotected areas, with the
larger modal size distribution occurring inside the marine reserve (mode 350 mm) compared with the
unprotected area (mode 200 mm) (Figure 2). The differences in the mean length values were even greater
Table 1. Comparisons of mean densities and demographic structures of Dicentrarchus labrax in the protected
and unprotected areas
Density (individuals/400 m)
Coefficient of variation (%)
Protected area
Unprotected area
Statistical tests
Mean
Mean
Mann–Whitney U
3.92
152.04
S.D.
5.96
0.69
150.72
S.D.
1.04
Z value
p level
−3.667
0.0002
Chi square
Mean length (mm)
Total counts
Copyright © 2001 John Wiley & Sons, Ltd.
381
98
222
212
27
87
 2 value
p level
36.040
B0.0001
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 1 – 9 (2001)
EFFECTS OF MARINE RESERVE PROTECTION ON SPEARFISHING TARGET SPECIES
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Figure 2. Length class distributions of (a) D. labrax and (b) S. aurata in the protected and unprotected areas.
than the modal size differences in this case of the European seabass. Inside the protected area mean fish
length was 381 mm, and outside it was 212 mm. A chi-square test on the two size distributions showed
a highly significant difference at the p =0.0001 level, with fish of this species being significantly larger
within the area of the Cerbère/Banyuls-sur-Mer marine reserve.
For the gilthead seabream (S. aurata) (Table 2), the data showed a much greater difference in
abundance (0.689 1.4 fish per 400 m in the marine reserve versus 0.059 0.22 per 400 m in the
unprotected area). Since only two individuals of this species were censused outside the marine reserve,
whereas 17 specimens were censused inside it, this difference was also significant (p= 0.0085). S. aurata
appeared to be more aggregated than D. labrax, with the coefficient of variation exhibiting a higher value
in the protected area (205.9%). However, too few individuals of S. aurata were counted to conclude
anything about heterogeneity outside the reserve area. Abundances mapped along the shoreline (Figure 1)
also indicate the overall aggregation tendencies in the spatial distributions of these two species.
Copyright © 2001 John Wiley & Sons, Ltd.
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 1 – 9 (2001)
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J.-Y. JOUVENEL AND D.A. POLLARD
Table 2. Comparisons of mean densities and demographic structures of Sparus aurata in protected and
unprotected areas
Density (individuals/400 m)
Coefficient of variation (%)
Protected area
Unprotected area
Statistical tests
Mean
Mean
Mann–Whitney U
0.68
205.88
S.D.
1.40
0.05
440.00
S.D.
0.22
Z value
p level
−2.631
0.0085
Chi square
Mean length (mm)
Total counts
379
17
70
400
2
0
 2 value
p level
n.c.
n.c.
n.c., not computed because of inadequate sample size.
DISCUSSION
Abundances of D. labrax were considerably higher in the marine reserve area, as has already been
observed for other target-fish species in other Mediterranean marine protected areas (Garcia-Rubies
and Zabala, 1990; Harmelin et al., 1995). The spatial distribution of seabass showed a general
preference for capes with significant underwater slopes. Their overall distribution, however, was
relatively homogeneous along the protected and the unprotected coastlines.
Differences observed in the spatial distributions of seabass individuals of different sizes were also of
interest. The length frequency distributions of these fishes showed that the shallow water population in
the marine reserve comprised larger individuals. However, there was a similar incidence of occurrence
of fishes 200 mm length inside and outside the marine reserve area (i.e. about 11–12 individuals in
each case). In spite of the relatively small numbers, if there was an important human predation impact
on these smaller fish, densities of these 200 mm specimens outside the marine reserve could have
been expected to be lower than those recorded.
In addition to the probable removal of many larger seabass from the unprotected areas by
spearfishing, such generally older individuals may also be displaying a conditioned behaviour which
induces them to seek more undisturbed (e.g. unfished) sites. Behavioural responses of this species have
been studied mainly in relation to its aquaculture. For example, like a number of other fish species,
seabass are readily able to use self-feeders in cages or raceways (Popper and Zohar, 1988). Also, wild
fish can precisely follow the timing of feeding at offshore aquaculture cages, arriving to feed on waste
food pellets under the cage structures (Divanach, personal communication). This species also shows a
considerable ability for adaptive behaviour in relation to human impacts in its environment. Seabass
can thus reportedly recognize spearfishing equipment being carried by a diver, and although to our
knowledge this behaviour has never been studied scientifically, many spearfishing magazines have
discussed this issue. In addition, shallow inshore waters offer a relative abundance of food resources.
For the highly carnivorous D. labrax, a large part of its mobile prey, such as small fishes and
decapod crustaceans, lives in subsurface waters between 0 and 5 m depth. Deeper waters are generally
less well supplied with these smaller prey fishes (Harmelin-Vivien et al., 1995; Macpherson et al.,
1996).
Copyright © 2001 John Wiley & Sons, Ltd.
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 1 – 9 (2001)
EFFECTS OF MARINE RESERVE PROTECTION ON SPEARFISHING TARGET SPECIES
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In the case of S. aurata, the observed difference in abundance was very significant between sites, the
mean density in the marine reserve being much higher than in the unprotected area (where, in fact,
the only two specimens observed were found relatively close to the marine reserve boundary). All
individuals recorded were relatively large fish. Their lengths ranged from 300 to 550 mm, which
corresponded to ages of 3 and 8/10 years, respectively (Bach, 1985; FishBase, 1997).
Shallow waters between 0 and 10 m depth are usually preferred by spearfishermen, whereas the use
of professional fishing methods is negligible in these shallow rocky inshore waters in the
Banyuls-sur-Mer region. That spearfishing is likely to be largely responsible for the results observed in
this study, either directly and/or indirectly, is supported by the findings already recorded for other
sites in the Mediterranean Sea (Harmelin et al., 1995).
An aggregative distribution seemed to be more pronounced in the case of S. aurata than D. labrax.
S. aurata also utilizes similar shallow inshore habitats at the northern limit of its geographical
distribution (Davis, 1988). This supports the suggestion that such rocky infralittoral areas may be
seasonally important in the ecology of the adults of this species. A great part of its trophic
requirements (e.g. mussels and oysters) settle and grow between the surface and a few metres depth
(Rosecchi, 1985), and the greatest single density of fish recorded during this study was associated with
an area dominated by mussels. These mussels (Mytilus gallopro6incialis) had settled around
waste-water drainage sites on rocks near the surface. This fish species is also known to cause
significant damage on offshore mussel aquaculture sites in the region of Banyuls-sur-Mer. Spearfishing
is prohibited around these commercial aquaculture sites, where this species can feed unhindered.
S. aurata is also known to be very difficult to approach underwater in unprotected areas. This
species, like the seabass, shows an adaptative capacity which results in it avoiding sites commonly
targeted by spearfishers. The protected status of the preferred sites in this study thus seems to be the
main explanation of the observed densities. The single larger aggregation of seabream observed was
attributed to the presence of the dense mussel population identified in one part of the protected area.
The conjunction of the protected area with such an important trophic resource may thus have been
the main factor structuring the spatial distribution pattern of this species in this particular area.
In conclusion, these two target-fish species both mainly occur in protected shallow water of areas
along this Alberian rocky coastline during summer. This behavioural trend has also been observed
previously for other fishes in other marine protected areas in the Mediterranean Sea (AMPN, 1980;
Harmelin et al., 1995). The availability of appropriate food before and/or after reproduction is
essential for the spawning and survival success of most mature fishes (Wootton, 1990), and such
shallow inshore waters offer important trophic resources. Typically, however, this environment is
elsewhere generally avoided by these two species, which retreat to deeper waters, presumably due to
fishing pressures, in most unprotected areas. The same phenomenon could also apply in relation to
some other target-fish species, such as various species of sparids of the genus Diplodus (Harmelin,
1987). Similar studies should thus be undertaken on the influence of spearfishing on the behaviour of
populations of other target-fish species. Environmental constraints, such as those due to the impacts of
spearfishing, may thus have important local effects on fish population dynamics and structure,
particularly in shallower inshore waters.
The differences observed here between target-fish densities and sizes inside and outside the marine
reserve area are most probably largely a consequence of mortality due to fishing pressure, but it is
suggested here that spearfishing may also strongly affect the behaviour of these important target-fish
species along these Alberian rocky shores. Further, more detailed, studies in this area would help to
clarify these points. The removal of spearfishing pressure in other areas may also allow the restoration
of more natural fish behaviour and distribution within them. Because behavioural knowledge of the
Mediterranean rocky reef ichthyofauna is still relatively limited, the implications of such anthropogenic
perturbations on the ecology of these fishes tend to remain unrecognized.
Copyright © 2001 John Wiley & Sons, Ltd.
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 1 – 9 (2001)
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J.-Y. JOUVENEL AND D.A. POLLARD
ACKNOWLEDGEMENTS
Dr J.-G. Harmelin of the Station Marine d’Endoume, Marseille, the journal editor, and two anonymous referees are
all thanked for useful comments on the manuscript, and special thanks are due to Thomas Cantens for his assistance
with the fish censuses. Thanks are also due to the European Community for financial support of this research
program. The study was sponsored by both the European Community (D.G. XIV section, MED 92/007) and the
European Associated Laboratory (LEA) ‘Science de la Mer’ Program.
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