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Top predators have strong influence on the structure and dynamics of marine ecosystems. These organisms have been largely used as indicators to assess the effectiveness of marine protected areas (MPAs). In Brazil, the impact of fisheries on reef species, such as groupers and sea basses, and the importance of local marine reserves in the maintenance of these fish communities are still poorly understood. Here we assessed the assemblage of groupers and sea basses (Epinephelidae and Serranidae) inside and outside the Arvoredo Marine Reserve (AR), a MPA in Santa Catarina State, southern Brazil. Density and biomass of 13 fish species (7 Epinephelidae and 6 Serranidae) were recorded. The most abundant groupers were Epinephelus marginatus and Mycteroperca acutirostris, while Serranus flaviventris and Serranus balwini were the most abundant sea basses. Grouper biomass was significantly higher inside the reserve, indicating the effectiveness of this MPA for target and threatened species, such as Epinephelus marginatus. In contrast, biomass of sea basses was higher outside the MPA, as a possible result of prey release effect. Despite the higher grouper biomass inside AR, spearfishing records from the 60s indicate that there is still a long way to a full recovery of the biomass of top predators, especially groupers and sharks. Thus, a more effective enforcement and longer-term protection are critically necessary to restore fish stocks and ecosystem health in these reefs.
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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 514: 207 –215, 2014
doi: 10.3354/meps11032 Published November 6
INTRODUCTION
In marine ecosystems, the impact of fisheries and
the extent of ecosystem recovery following major dis-
turbances have been largely used as indicators to
assess the effectiveness of marine protected areas
(MPAs; Sale et al. 2005). Previous studies show that
mean size and abundance of target fish species are
relatively higher inside protected areas in compari-
son to unprotected areas (e.g. Roberts & Polunin
1991, Bohnsack 1998, Halpern & Warner 2002, Russ
2002, García-Charton et al. 2008, Kellner et al. 2010).
However, the impact of fisheries on Brazilian reefs
and the importance of local marine reserves in the
© Inter-Research 2014 · www.int-res.com*Corresponding author: sergio.floeter@ufsc.br
Recovery of grouper assemblages indicates
effectiveness of a marine protected area in
Southern Brazil
A. B. Anderson1, R. M. Bonaldo2, D. R. Barneche3, C. W. Hackradt4,
F. C. Félix-Hackradt5, J. A. García-Charton6, S. R. Floeter1,*
1Laboratório de Biogeografia e Macroecologia Marinha, Departamento de Ecologia e Zoologia,
Universidade Federal de Santa Catarina, Florianópolis, SC, 88010-970, Brazil
2Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, 05508-900, Brazil
3Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia
4Centro de Formação em Ciências Ambientais, Universidade Federal do Sul da Bahia, Porto Seguro, BA, 45810-970, Brazil
5Centro de Formação em Ciências, Tecnologia e Inovação, Universidade Federal do Sul da Bahia, Itabuna, BA, 45613-204, Brazil
6Departamento de Ecología e Hidrología, Universidad de Murcia, Campus Espinardo, 30100 Murcia, Spain
ABSTRACT: Top predators have a strong influence on the structure and dynamics of marine eco-
systems. These organisms have been largely used as indicators of the effectiveness of marine pro-
tected areas (MPAs). In Brazil, the impact of fisheries on reef species, such as groupers and sea
basses, and the importance of local marine reserves in the maintenance of these fish communities
are still poorly understood. Here we assessed the assemblage of groupers and sea basses (Epi-
nephelidae and Serranidae) inside and outside the Arvoredo Marine Reserve (AR), a MPA in
Santa Catarina State, southern Brazil. Density and biomass of 13 fish species (7 Epinephelidae and
6 Serranidae) were recorded. The most abundant groupers were Epinephelus marginatus and
Mycteroperca acutirostris, while Serranus flaviventris and S. balwini were the most abundant sea
basses. Grouper biomass was significantly higher inside the reserve, indicating the effectiveness
of this MPA for target and threatened species, such as E. marginatus. In contrast, biomass of sea
basses was higher outside the MPA, as a possible result of prey release effect. Despite the higher
biomass of groupers inside AR, spearfishing records from the 1960s indicate that there is still a
long way to a full recovery of the biomass of top predators, especially groupers and sharks. Thus,
a more effective enforcement and longer-term protection are necessary to restore fish stocks and
ecosystem health in these reefs.
KEY WORDS: Top predators · Reef fishes · Epinephelidae · Serranidae · Fisheries · Conservation ·
Rocky reef · Southwestern Atlantic
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 514: 207–215, 2014
maintenance of fish communities are still poorly
understood, as few studies have assessed the contri-
bution of management strategies in protecting local
reefs (but see Floeter et al. 2006, Francini-Filho &
Moura 2008).
Top predators have a strong influence on the
structure and function of marine communities, since
they play critical roles in maintaining the structure
and dynamics of food webs in these systems (Dulvy
et al. 2004, Hutchings & Baum 2005, Baum & Worm
2009). Reductions in the biomass and abundance of
top predators may trigger potentially irreversible
cascade effects that destabilize food webs in the
marine environment (Dulvy et al. 2004, Heithaus et
al. 2008, Baum & Worm 2009). However, despite
recognition by marine biologists of such damaging
effects, numbers and biomass of top predators have
been dwindling dramatically over the last century,
with decreases of up to 90% in some regions (Heit -
haus et al. 2008). For this reason, biomass and abun-
dance of marine fishes, as well as other indices
associated to these variables (e.g. Large Fish Indica-
tor, the Large Species Indicator, the biomass-
weighted mean maximum length of fish species and
the biomass-weighted mean maturation length of
fish species of top predators targeted for fisheries),
are considered important to assess the effectiveness
of MPAs, as well as to evaluate the design, regula-
tion and enforcement of these areas (Spedicato et
al. 2005, García-Charton et al. 2008, Fung et. al.
2013).
Groupers (Epinephelidae) and sea basses (Ser-
ranidae) include a number of top and mesopredator
species susceptible to overfishing. The vulnerability
of epinephelids and serranids is usually explained by
their long life cycles, typically characterized by slow
growth rates, sex change and formation of spawning
aggregations in some species (Sadovy & Colin 2012).
Therefore, a number of groupers are currently
placed within ‘threatened’ categories of international
conservation indicators, such as the IUCN (Interna-
tional Union for Conservation of Nature) Red List of
Threatened Species (Craig et al. 2011, Bender et al.
2012, 2013, IUCN 2014, Sadovy de Mitcheson et al.
2013).
In an attempt to better protect sharks, groupers and
other threatened marine species, the Aichi Biodiver-
sity Targets for 2020 proposed the establishment of a
global and effective MPA management system (i.e.
Target 11; CBD 2010). Although Brazil is one of the
countries committed to achieve the proposed goals,
few studies have assessed the effectiveness of Brazil-
ian MPAs (e.g. Floeter et al. 2006, Francini-Filho &
Moura 2008, Gerhardinger et al. 2011). As a conse-
quence, the effects of existing local MPAs are still
largely unknown. Further information on the effec-
tiveness of Brazilian MPAs is critically important,
especially since most apex predator species, includ-
ing large sharks and groupers, have declined along
the Brazilian coast in the last few decades (Ferreira et
al. 2004, Floeter et al. 2006). For example, in Santa
Catarina State, the southernmost limit of the distribu-
tion of many tropical reef fishes in the Western
Atlantic (Hostim-Silva et al. 2006, Floeter et al. 2008,
Barneche et al. 2009), most top predators seem to
have disappeared likely as a result of overfishing
along the coast (Souza 2000). Reef fishes that were
once secondary top predators (e.g. groupers and sea
basses) now play the role of apex predators in these
marine ecosystems, and their populations have
clearly declined, along with reef sharks, from over-
fishing (Souza 2000).
In the present study, we assessed the assemblage
structure of groupers and sea basses inside and out-
side the Arvoredo Biological Marine Reserve, a
coastal MPA in Brazil. Both groupers and sea basses
are representative of predatory species; however,
while sea basses are usually smaller and less tar-
geted by fishers, grouper species generally attain
larger sizes and are heavily targeted (Bender et al.
2013, Sadovy de Mitcheson et al. 2013, A. B. Ander-
son pers. obs.). More specifically, we compared den-
sity and biomass of groupers and sea basses between
protected sites, where fisheries are restricted by fed-
eral law, and unprotected areas, where fisheries are
allowed.
MATERIALS AND METHODS
Study area
The study was conducted on subtropical reefs in
the vicinity of Florianópolis, Santa Catarina State,
southern Brazil (27° 35’ 41.08S; 48° 32’ 38.96”W).
Coastal and insular reefs in this region present simi-
lar geomorphology, characterized by steep granitic
rocky reefs that end in sandy bottoms, generally 12 to
15 m deep (Basei et al. 1992, Hostim-Silva et al. 2006,
Tomazzoli & Lima 2006).
Sampling was conducted at a total of 8 sites (3 pro-
tected and 5 unprotected), grouped into 3 sectors: Sec-
tor 1 —unprotected northwest coast (CO): (1) Cape
Araçá (Porto Belo City), (2) Cape Sepultura (Bombin-
has City); Sector 2 —Arvoredo Biological Reserve
(AR): (1) Arvoredo Island, (2) Galé Island and (3)
208
Anderson et al.: Recovery of groupers in southern Brazil
Deserta Island; Sector 3 —unprotected southern
islands (UI): (1) Arvoredo Island, (2) Aranhas Island
and (3) Xavier Island (Fig. 1). The 3 protected reefs
within Sector 2 are inside the Arvoredo Marine Bio-
logical Reserve (AR), about 11 km off northern Flori-
anópolis. AR has been designated a no-take marine
protected area since 1990 and encompasses 17800 ha.
In 2000, AR officially became a no-entry area, where
harvesting and human presence are strictly forbid-
den by law (researchers and managers excepted).
Arvoredo Island is located at the border of the MPA,
containing both protected and unprotected portions
(see Fig. 1). On the unprotected side of the island,
activities such as SCUBA diving and angling are
allowed. CO sites are characterized by high levels of
anthropogenic disturbances, such as recreational
fisheries, small vessel traffic, freshwater discharge
and sewage disposal. UI sites are also affected by
recreational fisheries and boat traffic, but at lower
levels.
The entire study was conducted during the austral
summer of 2011, between February (sites at UI and
CO, see below) and March and April (sites within
AR). During the study, water temperature ranged
from 22 to 28°C and underwater visibility ranged
from 4 to 15 m at all study sites.
Data collection
Underwater visual census (30 × 4 m strip transects =
120 m2) was used to quantify density and biomass of
grouper and sea bass populations and to explore topo-
graphic patterns at the sites. A scuba diver swam 1 m
above sub stratum along each transect, while unrolling
a measuring tape, recording all grouper and sea bass
(Epinephelidae and Serranidae) individuals found
and classifying them into species and 5 cm total
length (TL) categories. Fish TL was used to estimate
biomass for each species at each study site using pub-
lished weightlength relationships, according to the
following equation: W = a ×TLb, in which Wis the
total wet weight in grams, aand bare species-specific
parameters of the relationship, and TL is the total size
in cm (Froese & Pauly 2013).
At each study site, 2 depth strata were sampled:
slope and interface. Slope (S) was considered the
area between the water surface and half of the total
depth (TD). Thus, if TD = 6 m, S = 0 to 3 m. Interface
(I) corresponded to the transition zone between the
rocky reef and the non-consolidated substratum
typically sandy bottom in this case. Maximum TD
varied from 5 m at Cape Sepultura to 23 m at Xavier
Island. For each depth stratum, 9 transects were sur-
veyed, totalling 18 transects (2160 m2) sampled per
site. All transects were conducted in the morning.
Data analysis
One-way ANOVA was used to evaluate differ-
ences in average total (i.e. groupers and basses al -
together) density and biomass across the 8 study
sites. We also used ANOVA to test for differences in
average biomass across protection status (sectors
AR, UI, CO) for groupers and basses separately. In
both tests, when significant differences were found,
Tu key HSD post hoc test was used to verify sources
of variation. Before both analyses, assumptions of
normality and homoscedasticity were assessed with
the Kolmogorov-Smirnov/Lilliefors and Bartlett’s
tests (Underwood 1981, Snedecor & Cochran 1989,
Zar 1999).
Permutational Multivariate Analysis of Variance
based on the Bray-Curtis dissimilarity matrix (PERM-
ANOVA, Anderson 2001) was used to test for dif -
ferences in assemblage structure, both in terms of
density and biomass. PERMANOVAs (9999 permuta-
tions) were performed following a design with 3 fac-
tors: (1) protection status represented by Sector (Se):
fixed, with 3 levels and unbalanced (AR, UI and CO);
209
Fig. 1. Study area near Florianópolis, southern Brazil. The
dashed polygon represents the limits of the MPA of Ar-
voredo Marine Biological Reserve. The numbers indicate
the study sites within each sector
Mar Ecol Prog Ser 514: 207–215, 2014
(2) Site [Si(Se)]: random and nested within Sector,
with 8 levels and unbalanced (3 AR sites, 3 UI sites
and 2 CO sites; see Fig. 1); and (3) Depth Stratum
(St): fixed and orthogonal, with 2 levels (slope and
interface).
RESULTS
A total of 6 bass species (non-targeted), and 7
grouper species (targeted) were recorded across the
8 study sites. Epinephelus marginatus and Mycterop-
erca acutirostris were the dominant groupers in terms
of biomass and density, while Serranus flaviventris
and S. baldwini were the dominant sea basses in
both density and biomass across the 8 study sites
(detected in 6 and 4 study sites, respectively). Among
the 8 study sites, 2 islands presented higher species
richness of sea basses and groupers: Deserta Island
(AR) and Xavier Island (UI), with 9 and 10 species
detected, respectively (Table 1).
Mean grouper biomass was, on average, higher in -
side the reserve (F= 126.2, p < 0.001, Figs. 2 & 3). These
differences mostly resulted from the higher number
of larger fish (TL > 30 cm) inside AR (Table A1). Also,
large individuals of species targeted by fisheries,
such as M. microlepis, M. bonaci, M. interstitialis and
E. morio, were found exclusively within AR.
Two species of sea basses presented higher bio-
mass among small species: S. flaviventris and Diplec-
trum radiale. Mean biomass of sea bass was not sig-
nificantly higher inside AR (Fig. 3). S. baldwini was
mostly associated with rodolith beds in Deserta and
Aranhas Islands and was the only species with a con-
siderably higher biomass in side AR. S. flaviventris
and D. radiale were detected mostly in shallow areas
(maximum 5 m deep) at the interface.
Differences in the distribution of fish biomass
(Fig. 4) among sites were related to ‘Protection
Sector’ (p = 0.024), but not to ‘depth strata’ (p = 0.075)
(PERMANOVA, 9999 permutations). Differences in
density revealed virtually the same patterns (Table 2).
DISCUSSION
To the best of our knowledge, this is the first study
to assess the effectiveness of the Arvoredo Marine
Biological Reserve (AR) in protecting the heavily tar-
geted piscivorous fishes. The overall higher biomass
of groupers inside AR in comparison to unprotected
sites suggests that the protected area is highly impor-
tant to sustain populations of large predatory fishes,
210
Species Arvoredo Reserve (no-take zone; AR) Unprotected islands (UI) Unprotected coast (CO) IUCN
Deserta Is. Galé Is. Arvoredo Is. Arvoredo Is. Aranhas Is. Xavier Is. C. Sepultura C. Araçá
D B D B D B D B D B D B D B D B
EPINEPHELIDAE
Epinephelus marginatus 5.4 1918.3 5.7 2789.0 1.7 772.3 1.4 277.3 3.8 564.0 3.4 564.8 0.7 174.8 0.4 43.6 EN
E. morio 0.1 11.9 – – 0.1 70.6 – – – – – – – – – NT
Hyporthodus niveatus 0.1 8.6 0.1 0.1 – – 0.1 1.0 VU
Mycteroperca acutirostris 1.0 485.0 1.4 305.2 2.4 2281.4 2.1 797.2 1.0 245.7 1.1 204.4 0.6 126.5 2.8 479.6 LC
M. bonaci 0.2 212.2 – – – – 0.1 32.1 – – 0.1 5.5 0.1 11.2 – – NT
M. interstitialis 0.2 57.1 – – – – 0.1 36.4 – – 0.1 1.0 – – – – VU
M. microlepis 0.1 52.4 – – – – – – – – – – 0.1 10.1 – – LC
SERRANIDAE
Diplectrum formosum 0.1 6.3 – – – – – – 0.1 6.3 0.1 6.3 – – – – nc
D. radiale 0.1 8.2 – – 3.0 31.5 nc
Dules auriga 0.1 1.7 – – – – nc
Serranus atrobranchus 0.1 0.9 0.4 7.2 0.2 2.9 – – – nc
S. baldwini 1.1 5.9 – – – – 0.1 0.2 0.4 2.1 0.1 0.2 – – – – nc
S. flaviventris 0.1 1.2 0.4 12.5 – – 0.1 1.2 – 0.1 0.1 0.8 22.3 1.9 91.5 nc
Table 1. Mean density (D) and biomass (B, grams) of Epinephelidae and Serranidae per 120 m2at 3 protected (within the Arvoredo Reserve) and 5 unprotected sites (UI
and CO) in Southern Brazil. IUCN categories: EN = Endangered, NT = Near-Threatened, VU = Vulnerable, LC = Least Concern; (–) zero occurrence; nc = not classified
Anderson et al.: Recovery of groupers in southern Brazil
as observed in other rocky reefs (Hackradt et al.
2014). These predators are widely considered impor-
tant for maintaining the structure and dynamics of
marine food webs (Dulvy et al. 2004, Heithaus et al.
2008, Baum & Worm 2009).
Among the 7 species of groupers recorded in the
present study, 3 are considered threatened according
to the IUCN Red List of Threatened Species (Bender
et al. 2012, IUCN 2014) (Table 1). Indeed, large
reproductive individuals of Epinephelus marginatus
were found exclusively inside AR, suggesting that
the reserve acts as a refuge for species heavily tar-
geted by fisheries in the region, particularly since no
other no-take MPA exists near Florianópolis.
In addition to the higher richness of grouper spe-
cies inside AR, grouper individuals were usually
larger in protected sites, which may have direct
implications for the impact of these fishes in the
ecosystem. Body size and mass directly shape the
biology of fishes in a number of ways, as fishes of
different sizes and ontogenetic stages may have
different energetic and diet requirements (Eggle-
ston et al. 1998, Barneche et al. 2014), microhabitat
utilization and home ranges (Dahl gren & Eggleston
2001). As a consequence, ind ividuals of different
sizes may play different roles in the marine ecosys-
tem, either by targeting different prey or by focus-
ing their activities in distinct reef zones. The
removal of larger specimens of a given species
from the ecosystem may change the structure and
dynamics of the assemblage. Furthermore, larger
fish make a disproportionately higher contribution
to the production of eggs and gametes, and their
larvae usually present higher survivorship in com-
parison to those produced by smaller individuals
(Birkeland & Dayton 2005). The reduction in fish
size may thus have direct and negative impact on
the reproductive potential, with severe and detri-
mental consequences to the maintenance and
growth of the population.
At unprotected sites, density and biomass of large
groupers were reduced, whereas density and biomass
of sea basses were increased (though the difference
was not significant; ANOVA, F= 2.69, p = 0.16)
(Tables 1 & A1, Fig. 3). This process, termed ‘prey re-
lease effect’ (Dulvy et al. 2004), is usually observed in
reefs with overexploitation of top predatory species,
such as sharks and large groupers, in which popula-
tions of smaller piscivorous fishes, such as sea basses,
increase in abundance. This pattern seems to be the
case for the present study, considering the observed
differences in environmental characteristics across the
8 study sites and the contrasts in bass and grouper as-
211
Fig. 2. Density (top) and biomass (bottom) (mean + SE) of
groupers (Epinephelidae) and sea basses (Serranidae) at 8
reefs: 3 protected sites in the Arvoredo Marine Reserve (AR)
and 5 unprotected sites: 3 islands (UI) and 2 coastal sites
(CO). Different letters above bars indicate significant differ-
ences (Tukey HSD, p < 0.05)
Fig. 3. Biomass (mean + SE) of Epinephelidae (top) and Ser-
ranidae (bottom) species at 8 reefs: 3 protected sites in the
Arvoredo Marine Reserve (AR) and 5 unprotected sites: 3 is-
lands (UI) and 2 coastal sites (CO). Different letters above
bars indicate significant differences (Tukey HSD, p < 0.05)
Mar Ecol Prog Ser 514: 207–215, 2014
semblages apparently related to reef protection sta-
tus. The reduced pressure of bigger predatory spe -
cies in unprotected reefs around Florianópolis is thus
a probable cause for the increased population of sea
basses in fish assemblage at local reefs.
Despite AR effectiveness in contri -
buting to a higher biomass of
groupers within the reserve, our
results still raise questions concerning
its management, considering the
MPA’s age (over 20 yr), high protec-
tion status (no entry), and large area.
In the early 1960s, for example, 2
local fishers during a 3 h spearfishing
trip at Galé Island (currently within
the MPA) caught 5 grey nurse shark
Carcharias taurus and 3 Atlantic
goliath grouper Epine phe lus itajara
(Fig. A1). This type of catch was not
uncommon based on the considerable
number of reports and photographs of
similar activities around Florianópolis
between 1940 and 1960 with equally
high biomasses in fish caught within
a few hours (e.g. Souza 2000). In con-
trast, during the 60 h of SCUBA dives
in the present study, not a single indi-
vidual of C. taurus or E. itajara was
observed. Furthermore, in more than
300 h of monitoring the studied fish
communities over the last 5 yr, neither
of these species has been sighted (A.
B. Anderson, D. R. Barneche & S. R.
Floeter pers. obs.). This difference in
predatory fish biomass between AR in
the present study and reefs off Flori-
anópolis during the 1960s suggests
that the effectiveness of the re serve
has not reached its real potential,
despite the current larger grouper
biomass in AR in comparison to unpro-
tected reefs.
Previous works on the inference of
MPA’s effectiveness based on grou -
pers sizes, biomass and abundance
found that time/age of the MPA could
be crucial to restore grouper biomass
due to their long life spans and repro-
ductive behaviours (García-Charton et
al. 2008, Sadovy & Colin 2012, Fung at
al. 2013). The time needed for a mar-
ine reserve to become effective (i.e.
the time taken to restore populations
of target species and ecosystem biodiversity) is criti-
cal for the formulation of marine management strate-
gies (Halpern 2003, Lotze et al. 2006, Claudet et al.
2008). This subject, however, is quite controversial,
as some studies have found significant increases in
212
Fig. 4. Multivariate PERMANOVAs comparing biomass (mean + SE) distribu-
tions of Epinephelidae and Serranidae among 8 reefs, considering protection
sector (left) and depth stratum (right) as factors. See ‘Materials and methods’
for full description of study sites and sampling strategy
Source df SS MS Pseudo-Fp Unique
(perm) perms
Se 2 41040 20520 2.8761 0.0495 280
St 1 3242.5 3242.5 2.2727 0.1108 9953
Si(Se) 5 35673 7134.5 7.056 0.0001 9899
St×Se 2 10326 5163.2 3.619 0.0268 9944
St×Si(Se) 5 7133.5 1426.7 1.411 0.0962 9907
Res 128 1.2942 × 10–5 1011.1
Total 143 2.2642 × 10–5
Table 2. Multivariate PERMANOVA evaluating combined densities of Epine -
phelidae and Serranidae species as a function of protection status (Se), site (Si)
and depth stratum (St). Bold indicates significant (p < 0.05) results. p (perm): p-
value of permutational analysis; Unique perms: number of unique permutations
Anderson et al.: Recovery of groupers in southern Brazil
fish density and species richness after only 3 yr of
protection (e.g. Halpern & Warner 2002, Russ et al.
2005, Claudet et al. 2006), while in others this recovery
took decades (e.g. Micheli et al. 2004, Russ & Alcala
2004, Fung et al. 2013).
A possible reason for the lower than expected bio-
mass of predatory fishes at AR, given its establish-
ment time and protection status, includes the prac-
tice of illegal fishing, which has been taking place
since the reserve’s designation. As observed over the
last few years, an increase of AR enforcement, asso-
ciated with the application of management strategies
focusing on environmental education of local com-
munities, is expected to improve the effectiveness of
this protected area. However, as in most MPAs
around the world, a considerable lag time may exist
for educating the public about the importance of pro-
tecting these reefs and their associated biota (c.f.
Godoy et al. 2006, Gerhardinger et al. 2009, 2011).
CONCLUSIONS
The present study suggests that the Arvoredo
Marine Biological Reserve may have critical impor-
tance as a refuge for reef species heavily targeted
for fisheries (such as groupers) in southern Brazil.
However, despite recent efforts in research on the
conservation and management of the Brazilian
coast, the current protection of less than 1% of the
coastline (regarded as no-take areas) and the poor
enforcement of the existing no-take/no-entry zones
are far from ideal (Gerhardinger et al. 2011). There-
fore, the establishment of more protected marine
areas that encompass the nursery areas on the
Brazilian coast, along with proper enforcement, is
critical to the protection of endangered and vulnera-
ble marine species. The removal of key species,
such as top predators, has direct and detrimental
implications on the size of fish stocks and on the
dynamics and structure of the ecosystem. Thus, pro-
tecting the reef ecosystem also de pends on protect-
ing these species from exploitation.
Acknowledgements. We thank the Ecology and Hydrology
Laboratories, University of Murcia, Spain, and the Marine
Macroecology and Biogeography Lab, UFSC, Brazil, for help
with field trip logistics. We also thank H. S. Souza (in memo-
riam), who generously gave full access and use of his book
contents, L. Gerhardinger, M. Freitas, and F. Grecco for field
support, and the Fundación Banco Bilbao Vizcaya (FBBVA)
and CAPES (Brazil) for financial support (Projeto Eco-
Garoupa). S.R.F. is supported by CNPq (grant # 309472/
2011-3).
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Anderson et al.: Recovery of groupers in southern Brazil 215
Appendix.
Table A1. Frequency of occurrence (FO) and mean number of individuals in 4 size classes (510, 1120, 2130, > 31 cm total
length) of 2 fish species (Epinephelus marginatus and Mycteroperca acutirostris) at reefs around Florianópolis, southern
Brazil. Study sites included 3 protected sites in the Arvoredo Marine Reserve (AR) and 5 unprotected sites: 3 islands (UI) and 2
coastal sites (CO). For each site, FO was calculated dividing the absolute frequency of individuals in a size class by the total
number of transects (n = 18)
Study sites 510 cm 1120 cm 2130 cm >31 cm
FO Mean no. FO Mean no. FO Mean no. FO Mean no.
(%) (±SE) (%) SE) (%) (± SE) (%) (±SE)
Epinephelus marginatus
Galé Island (AR) 38.89 0.5 ± 0.19 88.89 2.61 ± 0.49 61.11 1.33 ± 0.34 66.67 1.22 ± 0.35
Deserta Island (AR) 38.89 0.5 ± 0.17 94.44 2.33 ± 0.34 83.33 1.56 ± 0.25 61.11 1.06 ± 0.34
Arvoredo Island (AR) 5.56 0.06 ± 0.06 38.89 0.67 ± 0.24 27.78 0.28 ± 0.11 44.44 0.72 ± 0.23
Aranhas Island (UI) 33.33 0.61 ± 0.22 77.78 2.17 ± 0.42 44.44 0.78 ± 0.25 22.22 0.28 ± 0.14
Xavier Island (UI) 66.67 0.94 ± 0.21 72.22 1.39 ± 0.29 44.44 0.72 ± 0.23 27.78 0.33 ± 0.14
Arvoredo Island (UI) 27.78 0.28 ± 0.11 55.56 0.72 ± 0.19 22.22 0.33 ± 0.18 11.11 0.11 ± 0.08
Cape Araçá (CO) 0 0 16.67 0.22 ± 0.13 16.67 0.17 ± 0.09 0 0
Cape Sepultura (CO) 0 0 22.22 0.28 ± 0.14 33.33 0.33 ± 0.11 5.56 0.06 ± 0.06
Mycteroperca acutirostris
Galé Island (AR) 0 0 55.56 0.83 ± 0.22 33.33 0.44 ± 0.17 16.67 0.17 ± 0.09
Deserta Island (AR) 0 0 27.78 0.33 ± 0.14 27.78 0.28 ± 0.11 22.22 0.39 ± 0.2
Arvoredo Island (AR) 0 0 16.67 0.22 ± 0.13 22.22 0.28 ± 0.14 66.67 1.94 ± 0.44
Aranhas Island (UI) 5.56 0.11 ± 0.11 38.89 0.5 ± 0.17 22.22 0.22 ± 0.1 16.67 0.17 ± 0.09
Xavier Island (UI) 0 0 38.89 0.61 ± 0.2 27.78 0.33 ± 0.14 11.11 0.11 ± 0.08
Arvoredo Island (UI) 11.11 0.17 ± 0.12 33.33 0.67 ± 0.28 22.22 0.39 ± 0.2 33.33 0.83 ± 0.39
Cape Araçá (CO) 5.56 0.11 ± 0.11 61.11 1.39 ± 0.5 66.67 1.22 ± 0.31 11.11 0.11 ± 0.08
Cape Sepultura (CO) 11.11 0.11 ± 0.08 27.78 0.28 ± 0.11 5.56 0.06 ± 0.06 11.11 0.11 ± 0.08
Fig. A1. Catch of 2 spearfishermen during 3 h of activities at Galé Island,
southern Brazil, in 1960: 3 goliath groupers Epinephelus itajara (left) and 5
sand tiger sharks Carcharias taurus (right) (extracted from Souza 2000)
Editorial responsibility: Christine Paetzold,
Oldendorf/Luhe, Germany
Submitted: October 16, 2013; Accepted: September 8, 2014
Proofs received from author(s): October 22, 2014
... The study found a clear decline in the absolute and relative abundance of the E. itajara in the early 1960s and during the 1970s, but underlined that before the 1950s, the stock, while considered pristine at this time, already suffered a significant decline. Analogously, Anderson et al. (2014) reported the abrupt decay in grouper abundance around Florianópolis (Santa Catarina State, southern Brazil) since the early 1940s based on the historical photographs taken in the area-documented by Souza (2000), combined with contemporary UVC data. Silvano and Valbo-Jørgensen (2008), interested in estimating the reliability of ethno-ichthyological surveys such as described before, argued to formulate hypotheses based on LEK studies. ...
... Whereas not all species positively respond to protection , Floeter et al. 2006, Claudet et al. 2010, Anderson et al. 2014, Edgar et al. 2014, Rojo et al. 2019, heavily exploited ones such as groupers are more likely to benefit from the implementation of an MPA. There are many examples of direct benefits of the prohibition of fishing activities on the abundance, biomass, and/or size of groupers inside MPAs worldwide, both in temperate and tropical areas (Nemeth 2005, Sadovy de Mitcheson and Colin 2012, Anderson et al. 2014). ...
... Whereas not all species positively respond to protection , Floeter et al. 2006, Claudet et al. 2010, Anderson et al. 2014, Edgar et al. 2014, Rojo et al. 2019, heavily exploited ones such as groupers are more likely to benefit from the implementation of an MPA. There are many examples of direct benefits of the prohibition of fishing activities on the abundance, biomass, and/or size of groupers inside MPAs worldwide, both in temperate and tropical areas (Nemeth 2005, Sadovy de Mitcheson and Colin 2012, Anderson et al. 2014). ...
... The members of subfamily Epinephelinae (Serranidae), which includes the grouper genera Mycteroperca and Epinephelus, are typically apex predators and are of great importance for fishing worldwide (Craig et al., 2011). Large predators have important ecological functions in reef ecosystems and play a key role in maintaining the trophic structure and functioning of communities (Anderson et al., 2014). In marine protected areas (MPAs), monitoring recommendations for conservation programs include an annual fishbased visual census, where apex predators are utilized as indicator species to examine trends and evaluate the effectiveness of different levels of protection on the ecosystem (Essington et al., 2006). ...
... MPAs are considered very effective for the protection and recovery of populations of large reef predators affected by fishing, as fishing is banned or controlled within them (Guidetti, 2007). Positive effects of MPAs, such as increased abundance of grouper genera in protected areas, have also been observed (Anderson et al., 2014). In addition to protecting adult individuals who can reproduce, MPAs can potentially benefit fisheries through repopulation of adjacent areas via dispersal of adults (spillover) or dispersal of larvae by marine currents (Macpherson & Raventos, 2006;Andrello et al., 2013Andrello et al., & 2017. ...
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... The creation of marine no-take zones (NTZs) has been considered one of the most effective tools in restoring and preserving biodiversity in coral reef environments (Halpern & Warner 2003, Lester et al. 2009, Edgar et al. 2014. Since the establishment of the first NTZs on coral reefs, a large body of evidence has shown that these protected areas are effective in increasing fish size, abundance, and biomass (Polunin & Roberts 1993, Gell & Roberts 2003, Halpern 2003, recovering populations of endangered species (Afonso et al. 2011, Anderson et al. 2014, restoring the complexity of ecosystems through reestablishment of trophic cascades (Harborne et al. 2008, Leleu et al. 2012, and promoting an overall increase in resilience and complexity within their boundaries (Micheli et al. 2012, Barnett & Baskett 2015. ...
... Positive effects of NTZs for fish communities, characterized by increased fish density and larger body size within the protected area, have been well documented worldwide (Halpern 2003, Lester et al. 2009, Malcolm et al. 2018, Gilchrist et al. 2020) and in Brazil (Floeter et al. 2006, Anderson et al. 2014 ...
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Movement is a key factor that shapes the distribution and structure of fish populations and influences the extent of the benefits provided by conservation and management measures, such as the implementation of marine no-take zones (NTZs). We used visual surveys and acoustic telemetry to investigate density and movement of 2 Brazilian endemic and highly targeted reef fish species inside and outside a coral reef NTZ, and subsequently inferred the effectiveness of the NTZ for protecting these species. To do so, visual surveys were performed on protected and unprotected reefs between 2016 and 2017. Moreover, 20 gray parrotfish Sparisoma axillare and 9 Brazilian snapper Lutjanus alexandrei were tagged with acoustic transmitters and passively monitored from December 2016 to October 2017. For both species, fish densities were significantly higher within the NTZ. Also, both species presented a high residence index over the short term, indicating they were full-time residents of the monitored area until detections were permanently lost. The absence of detections may indicate relocation to deeper reefs, predation, or fishing mortality when fish left the NTZ. Home ranges were small (0.10 to 0.45 km ² ), and both species presented spatially segregated subgroups within the populations. On average, the percentage of the home ranges within the NTZ was 88% for S. axillare and 95% for L. alexandrei . The results showed that small NTZs that are important to part of the life cycle of a target species are an effective measure to conserve reef fish populations, and also highlight the importance of fisheries management outside NTZs.
... Marine fishery resources need to be better managed worldwide to primarily counteract overfishing and on-going negative environmental changes (Jackson et al., 2001;Link & Watson, 2019). Despite some success stories of effective management and documented stock rebounds through for instance marine protected areas (e.g., Anderson et al., 2014), a general trend is a worldwide decrease in the quality and quantity of catches. Better management is called upon at all geographical scales, from offshore industrial fisheries in the high latitude seas (McBride et al.,2014) to small scale artisanal fisheries in remote tropical tenures, for both finfish and invertebrates (Alati et al., 2020;Warren & Steenbergen, 2021). ...
Thesis
Effective conservation and sustainable resource management are critical. Systematic Conservation Planning (SCP) identifies the areas that best meet the trade-offs between conservation objectives and costs, providing managers with a transparent decision support. However, our state of the art indicates a tendency for marine SCP in Oceania to be too generic regarding local needs, revealing several orphaned themes, yet crucial locally. This thesis aims to fill this gap by examining four research questions, applied to three lagoons in French Polynesia. 1. How can ciguatera be integrated into SCP? 2. Can SCP guide pearl farming management? 3. Can SCP make a useful contribution to traditional management? 4. How can strategies for diversifying activities be designed with SCP? Connected to the problems of managers, to local criteria and based on spatial data from surveys of fishers, this thesis formalizes a new method for integrating ciguatera into the SCP and produces original results with optimized costs. Two strong aspects emerge: optimizing traditional fisheries management and identifying areas for reintroducing pearl oysters. This confirms the practical interest and the initial choice of a “think globally, act locally” approach. In a context where commitments for conservation and sustainable management are multiplying, the SCP proves to be a precious tool to reduce the gap between research and action by translating, in conjunction with the managers, international ambitions into adapted local responses.
... Groupers are top predators in coral reef ecosystems, playing key roles in the formation of coral reef biotic communities (Anderson et al. 2014;Ranjeet et al. 2015). Groupers are a major target of the reef fisheries operating in almost all Indonesian coral reef areas due to their high market value and rising market demand (Khasanah et al. 2019). ...
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... Marine fishery resources need to be better managed worldwide to primarily counteract overfishing and on-going negative environmental changes (Jackson et al., 2001;Link and Watson, 2019). Despite contrasted status between countries and some success stories of effective management and documented stock rebounds through, for instance, marine protected areas (e.g., Anderson et al., 2014;Cochrane, 2021;Hilborn et al., 2020), a general trend is a worldwide decrease in the quality and quantity of catches (Pauly and Zeller, 2016). Better management is called upon at all geographical scales and a wide range of fishery types, from offshore industrial fisheries in the high latitude seas (McBride et al., 2014) to small scale fisheries such as in Europe (Frangoudes et al., 2020;García-Lorenzo et al., 2019) or traditional artisanal fisheries in remote tropical tenures, for both finfish and invertebrates (Alati et al., 2020;Warren and Steenbergen, 2021). ...
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