Inuence of the articial reef size conguration on transient

ichthyofauna e Southeastern Brazil

P.V. Gatts
a
, M.A.L. Franco
a
, L.N. Santos
b
, D.F. Rocha
a
, I.R. Zalmon
a, *
a
Centre of Biosciences and Biotechnology, University of North Rio de Janeiro State, Campos, RJ 28013-602, Brazil
b
Department of Ecology and Marine Resources, Federal University of Rio de Janeiro State, Rio de Janeiro, RJ 22061-010, Brazil
a r t i c l e i n f o
Article history:
Available online
a b s t r a c t
To investigate how variations in the volume of articial reefs affect the structure and composition of the
transient ichthyofauna, reefball-type concrete modules were arranged at 9 m of depth along the northern
coast of the state of Rio de Janeiro. The modules were arranged in three congurations, each in triplicate:
(1) solitary modules (1 m
3
), (2) side-by-side modules (2 m
3
) and (3) modules forming a triangle (3 m
3
).
The surrounding ichthyofauna were sampled in two periods of the year (dry: September 2009 and
October 2010; rainy: April 2010 and April 2011) with gillnets to record the richness, species diversity,
number of individuals and biomass per volume unit. The total mean values of richness, diversity, number
of individuals and biomass did not differ signicantly among the reef volumes. However, when these
variables were analyzed per standardized volume unit, there was an increase in these variables with the
increase in reef volume, considering all the transient ichthyofauna as well as the most representative
families, Ariidae and Sciaenidae. A non-metric multidimensional scaling ordination analysis revealed
differences in the composition of the ichthyofauna between the sampling periods, dominated by
Sciaenidae (Stellifer rastrifer, Paralonchurus brasiliensis, Larimus breviceps and Cynoscion virescens) in the
dry period and by Ariidae (Aspistor luniscutis) and Carcharinidae (Rhizoprionodon porosus) in the rainy
period. The results suggest that the increase in module size from 1 to 3 m
3
may result in slight alterations
in the community descriptors, with a decrease in the relative values of richness, diversity and density per
standardized volume unit. Furthermore, the effects of the seasonal ow of the Paraba do Sul River may
overlap the effects of reef conguration, mainly in the rainy period with higher ow. The implementation
of several dispersed 1 m
3
modules seems to be the most favorable conguration to attract transient
ichthyofauna, especially Ariidae and Sciaenidae, on the northern coast of the state of Rio de Janeiro.
2014 Elsevier Ltd. All rights reserved.
1. Introduction
Articial reefs are increasingly being used as tools for habitat
recovery, mainly due to their growing use in the increase of
biodiversity and recovery of sh stocks (Caddy, 1999; Fabi et al.,
2011; Feary et al., 2011; Polovina, 1991; Brown et al., 2014;
Walker and Schlacher, 2014). Such use is due, in part, to the
greater facility with which articial reefs can be managed in terms
of their architecture (e.g., material, size, complexity and arrange-
ment of the reef modules) in comparison to natural habitats. In this
sense, several studies have reported direct and positive impacts of
increases in complexity and size of reefs on the number of in-
dividuals (Campbell et al., 2011; Gratwicke and Speight, 2005),
biomass (Bohnsack et al., 1994; Bohnsack, 1989; Charbonnel et al.,
2002; Jordan et al., 2005; Sherman et al., 2002), richness
(Bohnsack, 1994; Gratwicke and Speight, 2005) and diversity of
shes (Fabi and Fiorentini, 1994; Hunter and Sayer, 2009).
Considering reef size, which can be measured in volume, area or
number of reef units, larger natural and articial reef systems can
support higher values of richness, number of individuals and sh
biomass (Bohnsack et al., 1994; Bohnsack, 1989; Campbell et al.,
2011; Jordan et al., 2005). However, the duplication or triplication
of the reef volume does not necessarily lead to an increase in total
values of these community attributes in the same proportion
(Jordan et al., 2005). Conversely, reefs of smaller dimensions
distributed in isolation or in patches may sustain higher density
and diversity of shes per standardized volume unit than larger and
isolated reefs (Ambrose and Swarbrick, 1989; Bohnsack et al., 1994;
Morton and Shima, 2013; Nanami and Nishihira, 2002; Randall,
1963; Schroeder, 1987).
* Corresponding author. Tel.: 55 22 2739 7137.
E-mail addresses: ilana@uenf.br, zalmon@censanet.com.br (I.R. Zalmon).
Contents lists available at ScienceDirect
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http://dx.doi.org/10.1016/j.ocecoaman.2014.06.022
0964-5691/ 2014 Elsevier Ltd. All rights reserved.
Ocean & Coastal Management 98 (2014) 111e119
In this context, this study evaluated the effects on the transient
ichthyofauna of different volumes of articial reefs installed on the
north coast of the state of Rio de Janeiro. The following hypothesis
was tested: the increase in volume from 1 m
3
to 3 m
3
of modular
units of an articial reef increases the reef's area of inuence on its
surroundings and consequently, the richness, species diversity,
number of individuals and biomass of the transient ichthyofauna in
comparison to smaller modules. The potential use of articial reefs
with different volumes and dispersal levels among modules as a
tool for the management of the transient ichthyofauna is also
briey discussed.
2. Methodology
2.1. Study site
The study site is located on the north coast of Rio de Janeiro
between the main mouth of the rivers Paraba do Sul (south) and
Itabapoana (north), approximately 25 km equidistant from these
two points (Fig. 1). The articial reef complex is located approxi-
mately ve nautical miles from the beach of Manguinhos (21

24
0
S,
41

55
0
W) at a depth of approximately 9 m (Zalmon et al., 2002).
The region can be characterized by two seasons, considering the
rainfall indexes and the ow of the Paraba do Sul river (Fig. 2): the
rainy period, with higher rainfall indexes and ow, which corre-
sponds to the summer months; and the dry season, with lower
rainfall indexes and ow.
2.2. Experimental design
The present study was performed using concrete reef modules
called reefballs (~1 m
3
). The modules possess orices of 20 cm of
diameter and an approximate weight of 500 kg. In studies evalu-
ating the spatial congurations of articial reefs, Santos et al. (2010)
suggested that the distance between reef modules of the same
treatment should not exceed 50 m because beyond this distance, a
depletion in the abundance and species richness associated with
the reef occurs. In this study, the reef complex with an approximate
area of 60 000 m
2
consists of 30 modular units, arranged in three
volumes separated by > 50 mto reinforce the independence among
the treatments tested. Besides, the design aimed to study spatial
scale issues related to the habitat use of commercial interest in the
local artisanal shery, such as Pomatomus saltatrix (bluesh), Gen-
idens genidens (guri sea catsh), Rhizoprionodon porosus (Caribbean
sharpnose shark), Isopisthus parvipinnis (bigtooth corvina), Cyn-
oscion microlepidotus (smallscale weaksh), Cynoscion jamaicensis
(Jamaica weaksh), Cynoscion virescens (green weaksh), Macrodon
ancylodon (king weaksh), Ophistonema oglinum (Atlantic thread
Fig. 1. Installation site and schematic drawing conguration of the articial reefs (AR) on the north coast of the state of Rio de Janeiro.
Fig. 2. Monthly mean ow of the Paraba do Sul River from 1995 to 2011 and specif-
ically of the years 2010 and 2011
Source: Laboratory of Environmental Sciences of the University of North Rio de Janeiro
State.
P.V. Gatts et al. / Ocean & Coastal Management 98 (2014) 111e119 112
herring) and Cetengraulis edentulus (Atlantic anchoveta) (Garcez,
2007). Therefore, to test the effect of the volume increase on the
sh assemblies, three triplicate treatments were used: a solitary
module (1 m
3
), two modules (2 m
3
) and three modules (3 m
3
), with
the modules in the grouped treatments separated by > 0.5 m
(Fig. 1). The precise location of the modules in the planned con-
gurations was obtained using a GPS.
2.3. Sampling
Four samplings were performed according to the local season-
ality (end of the dry periods: September 2009 and October 2010,
and end of rainy periods: April 2010 and April 2011) to obtain a
view of the ichthyofauna at times when the current climate con-
ditions had already lasted for a considerable period (to reduce the
inuence of the transition periods between seasons on the sam-
ples). Samples were collected with gillnets (n 27) with 25 m of
length, 3 m of height and 30 mm of mesh between adjacent nods
(Fig. 3). The nets were submerged for 24 h to capture the transient
diurnal and nocturnal species. The exclusive use of gillnets is
justied by two reasons: i) the shing gear is the same used by
artisanal shermen in the region, and ii) because of the strong
uvial inuence (Itabapoana River and, mainly, Paraba do Sul
River), the subaquatic visibility is very restricted, <0.5 m (Godoy
et al., 2002), preventing the application of the visual census
method typically employed in studies related to reefs.
2.4. Data treatment and analysis
According to Morton and Shima (2013), species richness, num-
ber of individuals, total biomass and biomass per standardized
volume unit can reect different responses of the ichthyic com-
munity associated to reefs. Therefore, to detect variation in the
structure of the transient ichthyofauna associated with each
experimental treatment and in each period (dry and rainy), the
following numerical descriptors were evaluated: richness, number
of individuals, total biomass and biomass per standardized volume
unit (m
3
), Shannon's diversity (H), Simpson's dominance (D) and
the importance percentage (PI) index, which considers the occur-
rence frequency, the number of individuals and the percentage of
biomass of each species (Zar, 1984). A permutational multivariate
analysis of variance (PERMANOVA) was applied to test differences
related to these descriptors among the different reef volume con-
gurations and sampling periods (dry and rainy). The BrayeCurtis
similarity matrix was used as the basis of the PERMANOVA, with
data permuted 9 999 times at p 0.05 per analysis (Anderson,
2005). Generalized additive models (GAMs) were used to deter-
mine spatial tendencies of the relationships between the volumes
of reef modules (predictive responses) and the attributes of rich-
ness, number of individuals and associated ichthyofauna biomass
(variable responses). GAMs are an extension of generalized linear
models that, in contrast to other regression models, do not require a
previous assumption of linearity between each variable and pre-
dictive response (Leps and

Smilauer, 2003). The complexity of the
model is determined by the process of step-by-step selection with
the Akaike information criterion (AIC) in the program CANOCO 4.5.
A canonical principal components analysis was used to evaluate
the effect of the reef volumes tested (1, 2 and 3 m
3
) on the compo-
sition and structure of the transient ichthyofauna, using the matrix
of the number of individuals of each species and the BrayeCurtis
distance with 9 999 permutations (Anderson, 2004). This analysis
nds the axis (or axes) inthe space of principal components that best
discriminates the reef volumes, previously dened, considering the
matrix of correlation between the number of individuals and each
volume tested (Anderson, 2004). The seasonal changes in the
composition and structure of the ichthyofauna associated with the
different reef volumes were tested with a non-metric multidimen-
sional scaling ordination analysis, using the BrayeCurtis coefcient
as a measure of similarity (Clarke and Warwick, 2001).
3. Results
3.1. Composition and structure of the ichthyofauna
In the four sampling campaigns, 31 species and 10 families were
recorded. Of these species, seven species represented in number of
individuals 80.22% of the transient ichthyofauna (Table 1): Aspistor
luniscutis (23.06%), Cynoscion virescens (20.22%), Larimus breviceps
(11.16%), Rhizoprionodon porosus (7.35%), Isopisthus parvipinnis
(6.99%), Paralonchurus brasiliensis (6.32%) and Stellifer rastrifer (5.13%).
The ichthyic composition was similar in the reef volumes, with
11 species in common and 3, 6 and 2 species exclusive to
the treatments of 1, 2 and 3 m
3
, respectively (Table 1). Aspistor
luniscutis predominated in the three volumes (PI: 1 m
3
24.57%,
2 m
3
29.30%, and 3 m
3
16.25%), along with C. virescens (22.52%)
and P. brasiliensis (11.61%) in the volume of 1 m
3
, L. breviceps (22.30%)
and R. porosus (20.45%) in the intermediate volume and C. virescens
(34.90%) and I. parvipinnis (16.79%) in the treatment of 3 m
3
.
3.2. Community attributes
The transient ichthyofauna did not differ signicantly regarding
the descriptors richness, number of individuals, biomass, diversity
and dominance in the three reef volumes tested (1, 2 and 3 m
3
) or
temporally (dry and rainy seasons) (Table 2).
The highest total values of richness and number of individuals
were recorded in the 3 m
3
reefs (Figs. 4A and C), and the highest
biomass values were recorded in the 2 m
3
volume (Fig. 4E).
Considering the data per standardized volume unit, higher rich-
ness, number of individuals and biomass values were observed in
the reef volume of 1 m
3
(Figs. 4D, E and 4F). In these descriptors, the
generalized additive models with the Akaike information criterion
(AIC) highlight a reduction tendency regarding the volumes tested
(Fig. 5B e AIC, linear F1, 36 4.18, P 0.02; 5D e AIC, linear F1,
36 3.39, P 0.07; and 5F e AIC, linear F1, 36 3.17, P 0.05).
Considering the families, there were a greater number of in-
dividuals of Ariidae and Sciaenidae in the 1 m
3
modules (Figs. 5A
Fig. 3. Schematic drawing showing the placement of the gill-nets relative to the reef
modules.
P.V. Gatts et al. / Ocean & Coastal Management 98 (2014) 111e119 113
and B), whereas Carcharhinidae and Carangidae were the most
abundant in the 2 m
3
modules (Figs. 5C and D). The generalized
additive models indicated decreasing tendencies in the density of
Ariidae (F
1,36
2.34, P 0.11) and Sciaenidae (F
1,36
3.63, P 0.06)
relative to the volumes tested when analyzed based on the stan-
dardized volume unit (Figs. 5A and B).
The canonical principal components analysis revealed that the 1
and 2 m
3
reef volumes were more similar to each other, both
located more to the right in the diagram, than to the 3 m
3
volume
for sharing the species Larimus breviceps, Odontognathus mucronatus,
Anchoa spinifer, Bagre marinus and Macrodon ancylodon (Fig. 6). The
ichthyic composition of the 3 m
3
volume (Cynoscion virescens, Iso-
pisthus parvipinnis, Stellifer rastrifer, Menticirrhus americanus and
Cynoscion jamaicensis) was marginally distinct (p 0.06) (Fig. 6).
3.3. Seasonal effects in the pattern of use of reefs
The non-metric multidimensional scaling ordination revealed a
higher association of the transient ichthyic community with the
sampling period than with the reef volumes tested (PERMANOVA:
P 0.001) (Fig. 7).
The temporal variation in the pattern of association of species was
evidenced in all the treatments in the reef complex (Fig. 8A) and in
each volume tested, revealing a seasonal distribution of the main
species in the region (Figs. 8B, C and 8D). Rhizoprionodon porosus and
Aspistor luniscutis predominated in the rainy period, whereas Stellifer
rastrifer, Paralonchurus brasiliensis, Larimus breviceps and Cynoscion
virescens were more abundant in the dry period (Fig. 8).
4. Discussion
The relatively low values recorded for the number of species
and richness of shes may be related to some factors associated
with the characteristics of the region as well as to the method of
capture applied. Articial reefs are visually detected by the
ichthyofauna or, if this does not occur, are found passively (Schroeder,
1987). However, the small scale of the volume variation of the
structure may have been insufcient for transient shes and,
consequently, for the detection of clear patterns of this ichthyo-
fauna in articial reefs.
The limitation of the use of gillnets should be taken into account
when comparing the composition of the ichthyofauna observed in
this study to previous investigations in the same reef area. Zalmon
et al. (2002) evaluated the possible modications of the ichthyo-
fauna promoted by an articial reef composed of tires and concrete
in this same area using gillnets, and of the species they found, 17
were in common with this study. In contrast, Brotto and Zalmon
(2007) investigated the ichthyic assembly associated to the reef
complex using the visual census technique, and because of the
limitations due to low visibility, only four of the species they
observed were in common with the present study. In a more recent
work performed in this area by Santos et al. (2010) with both
sampling techniques (visual census and gillnets), 12 species were
identied in common with the present study, of which the most
representative species belong to the families Haemulidae and Ser-
ranidae. In the present study, the Haemulidae corresponded to
1.33% (N 3) of the total number of individuals collected, whereas
Serranidae were not recorded.
Furthermore, because of its mesh, a gillnet may restrict the
sampling of individuals according to their length, and because of its
low selectivity, gillnets facilitate the collection of species with
different life habits, such as benthonic, pelagic or transient (Acosta,
1997; Nielsen and Johnson, 1983). Therefore, the differences in the
data obtained through this ichthyofauna sampling method may be
a consequence of gear limitations. However, in addition to the high
local turbidity (Secchi: 0.5 m), this shery art is traditionally
Table 2
PERMANOVA of richness, abundance, biomass, Shannon's diversity (H) and Simp-
son's dominance (D) of the ichthyic species captured in each reef volume (1, 2 and
3 m
3
) and sampling period (dry and rainy).
Factor df F P
Species richness
Volume 2 0.301 0.743
Period 1 0.280 0.597
Volume Period 2 0.120 0.885
Residual 30
Total 35
Individual numbers
Volume 2 0.464 0.627
Period 1 0.018 0.895
Volume Period 2 0.113 0.893
Residual 30
Total 35
Biomass
Volume 2 0.448 0.637
Period 1 0.674 0.419
Volume Period 2 0.096 0.902
Residual 30
Total 35
Shannon's Diversity (H)
Volume 2 0.022 0.980
Period 1 0.330 0.557
Volume Period 2 0.112 0.892
Residual 30
Total 35
Simpson's Dominance (D)
Volume 2 2.579 0.097
Period 1 0.001 0.969
Volume Period 2 0.050 0.951
Residual 30
Total 35
df: degrees of freedom.
Table 1
Composition and importance percentage (IP) of the ichthyic species captured in each
reef volume (1, 2 and 3 m
3
) and in total.
IP
Family Species 1 m
3
2 m
3
3 m
3
Total
Ariidae Aspistor luniscutis 24.57 29.30 16.23 23.05
Bagre marinus 1.64 3.55 0.92 2.02
Genidens genidens 2.27 2.07 0.53 1.54
Carangidae Caranx latus 4.56 1.28
Chloroscombrus chrysurus 1.00 0.94 2.37 1.50
Oligoplites saliens 2.60 0.89
Selene setapinnis 0.46 0.16
Carcharhinidae Rhizoprionodon porosus 20.45 0.88 7.35
Clupeidae Odontognathus mucronatus 0.46 0.16
Opisthonema oglinum 1.14 0.67 0.82 0.86
Engraulidae Anchoa spinifer 0.55 0.19
Cetengraulis edentulus 1.05 0.29
Haemulidae Haemulon steindachneri 0.70 0.24
Orthopristis ruber 2.89 1.09
Kyphosidae Kyphosus sectatrix 3.89 1.09
Pristigasteridae Pellona harroweri 0.91 0.53 0.44
Sciaenidae Cynoscion jamaicensis 0.06 0.02
Cynoscion microlepidotus 6.90 2.21 3.32 3.94
Cynoscion sp. 0.06 0.02
Cynoscion virescens 22.52 2.23 34.86 20.21
Isopisthus parvipinnis 1.46 0.77 16.78 6.99
Larimus breviceps 7.92 22.30 3.41 11.15
Macrodon ancylodon 6.52 2.24
Menticirrhus americanus 0.92 0.35
Paralonchurus brasiliensis 11.61 8.13 6.32
Stellifer rastrifer 7.65 0.70 7.28 5.12
Stromateidae Peprilus paru 0.91 2.99 0.56 1.49
Total 100.00 100.00 100.00 100.00
P.V. Gatts et al. / Ocean & Coastal Management 98 (2014) 111e119 114
applied in the north coast of the state of Rio de Janeiro by local
artisanal shermen, justifying its use in scientic investigations
(Brotto and Zalmon, 2007; Franco, 2013; Santos et al., 2010; Zalmon
et al., 2002).
The results of this study reveal that the reef volumes of 1, 2 and
3 m
3
act distinctly on the structure of the ichthyic transient com-
munity. The increase in the reef volume in the scale proposed led to
a reduction in the values of richness, density and biomass of species
per unit of volume as well as in the diversity of the referred com-
munity, refuting the hypothesis tested.
Several authors (Bohnsack, 1994; Campbell et al., 2011;
Greywacke and Speight, 2005; Jordan et al., 2005; Schroeder,
1987) reported a direct relationship of richness, number of
individuals, biomass and species diversity with reef volume or size.
Gratwicke and Speight (2005) justied such a relationship through
an increase in articial consolidated substrate resulting in greater
xation of periphyton (important marine primary producers) and,
consequently, of herbivores (including shes) and their potential
predators. Campbell et al. (2011) observed that an increase in the
number of reefs increased the availability of prey and of refuge
areas but reduced the distance among the articial structures and,
consequently, the movement of the ichthyofauna during foraging.
Therefore, there is an increase in the efciency of the consumption
of prey by shes (Bohnsack, 1994; Jordan et al., 2005; Krivan, 2013),
resulting in higher number of individuals and higher biomass. It
should be noted that the authors cited did not test such results per
Fig. 4. Relative number of species, number of individuals and biomass per volume (A, C and E) and per standardized volume unit (B, D and F) of the transient ichthyic community in
each reef volume (1, 2 and 3 m
3
). The lines represent the generalized additive models selected based on the Akaike information criterion.
P.V. Gatts et al. / Ocean & Coastal Management 98 (2014) 111e119 115
standardized volume unit, in contrast to our study, which is a
pioneer in two aspects: 1) approaching transient ichthyofauna re-
sponses (poorly approached in reef studies) and 2) showing un-
expected effects contrasting with the expectations for the resident
ichthyofauna.
Because the duplication or triplication of the reef volume does
not necessarily lead to an increase in the values of the community
attributes in the same proportion, it is suggested (Morton and
Shima, 2013; Schroeder, 1987) that these numerical indicators,
such as richness, number of individuals and biomass, be converted
to a standardized unit. Smaller reefs and/or reefs with patchy dis-
tribution and complexity may sustain higher density and diversity
of shes per standardized volume unit than larger and isolated
reefs (Ambrose and Swarbrick, 1989; Bohnsack et al., 1994; Nanami
and Nishihira, 2002; Randall, 1963).
Nanami and Nishihira (2002) recorded higher values of density
and richness of ichthyic species in small reefs and in reefs with
patch distribution and complexity due to the higher diversity and
Fig. 5. Number of individuals per standardized m
3
(log
10
) of families Sciaenidae (A), Ariidae (B), Carcharhinidae (C) and Carangidae (D) in the transient ichthyic community in each
reef volume (1, 2 and 3 m
3
). The lines represent the generalized additive models selected based on the Akaike information criterion (AIC).
Fig. 6. Ordination diagram of the canonical principal components analysis of the
number of individuals captured in relation to each reef volume tested (1, 2 and 3 m
3
).
The circles correspond to the 95% condence interval.
Fig. 7. Non-metric multidimensional scaling of the ichthyic community in each reef
volume (1, 2 and 3 m
3
) and sampling period (dry and rainy).
P.V. Gatts et al. / Ocean & Coastal Management 98 (2014) 111e119 116
coverage of corals (refuges) and of feeding resources available (e.g.,
small crustaceans). Others, such as Randall (1963); Bohnsack et al.
(1994) and more recently Morton and Shima (2013), found more
elevated sh densities in solitary articial structures, claiming that
fragments of isolated and disperse habitats possess stronger border
effects and higher concentrations of predators in these environ-
ments than in more aggregated reefs (Macreadie et al., 2010; Smith
et al., 2011), resulting in a greater vulnerability of prey. Such an
indirect relationship of reef volume versus richness and number of
individuals of the ichthyofauna evidenced in the articial reefs in
the north coast of the state of Rio de Janeiro suggests that the non-
linear increase in the number of individuals with the increase in the
reef size might be the result of a higher marginal effect in the 1 m
3
modules (with a higher percentage of interface sand/reef area).
Therefore, small reefs possess a higher attractive effect per unit
area, that is, they attract shes of an area proportionally higher than
larger reefs, resulting in higher densities (Ambrose and Swarbrick,
1989; Schroeder, 1987).
Talbot et al. (1978) suggest that predation is one of the main
factors that regulate ichthyic communities in isolated habitats
associated with sandy substrates. In articial reefs, the availability
of prey is cited as the main factor responsible for attracting tran-
sient shes (Harding and Mann, 2001; Simonsen, 2008). In our reef
complex, the main sh species were classied by Santos et al.
(2010) as piscivores (Larimus breviceps, Cynoscion virescens, Cyn-
oscion jamaicensis and Rhizoprionodon porosus) and invertivores
(Aspistor luniscutis, Paralonchurus brasiliensis and Stellifer rastrifer).
Therefore, it is probable that the ichthyofauna was concentrated
mainly in the 1 m
3
articial reefs due to the higher vulnerability of
the prey (shes and invertebrates) available in the concrete struc-
tures and in the adjacent unconsolidated substrate in comparison
to larger reefs and reefs separated by more distance (Zalmon et al.,
2014). Furthermore, the smallest reefs shared several species with
the 2 m
3
volume, corroborating the hypothesis that the smallest
reefs are more efcient in attracting the transient ichthyofauna.
Larger modules, such as the 3 m
3
ones, display greater complexity
in terms of refuge availability in addition to small gaps among the
structures that hinder the access to larger transient shes (Hixon
and Beets, 1989; Jordan et al., 2005; Major, 1978), attracting small
potential prey and, consequently, inuencing the composition and
diversity of the ichthyofauna.
The pattern of association of the transient ichthyofauna species
revealed a seasonal effect, evidencing the potential effect of the
Paraba do Sul River on the articial reef complex and on each
spatial conguration tested, resulting in a temporal distribution
pattern of the main species and masking the differences regarding
reef size. Berkstrom et al. (2013) highlight the importance of
combining habitat conguration at different scales with connec-
tivity of the surrounding habitats in structuring sh communities
in a tropical embayment.
As observed by Brotto and Zalmon (2007), adverse environ-
mental conditions (for example, strong bottom currents, turbid
waters and the presence of a polyhaline plume) are most likely the
key factors that affect the colonization patterns of shes in articial
reefs in the north coast of the state of Rio de Janeiro (Krohling and
Zalmon, 2008; Santos et al., 2010). Schmidt et al. (2008) and
Denadai et al. (2012) determined that the reproduction and
development period of Aspistor luniscutis, the most representative
species in the present study, is related to the hotter months of the
year and/or times with large quantities of uvial waters, justifying
the predominance of this species in the summer, corresponding
to the rainy period and the period of higher ow of the Paraba do
Sul River.
In general, the main species of the family Sciaenidae captured in
the articial reefs along the north coast of Rio de Janeiro live close
to the mouths of large rivers and are predominant in the region
during the entire year (Fulg^ encio, 2004; Gomes et al., 2003; Militelli
et al., 2013; Souza and Chaves, 2007), with young and adult in-
dividuals using estuarine and shallow water areas for growth and
feeding (Godefroid et al., 2004; Menezes and Figueiredo, 1980).
These species are found in beach environments in the periods of
reproduction and recruitment, which occur from spring to fall
Fig. 8. Relative distribution of the number of individuals (%) of the most representative species (PI > 5%): A e all reef volumes; B e 1 m
3
; C e 2 m
3
; D e 3 m
3
. RS: rainy season; DS:
dry season.
P.V. Gatts et al. / Ocean & Coastal Management 98 (2014) 111e119 117
(Godefroid et al., 2004). This migratory behavior of the species of
family Sciaenidae justies their predominance in the articial reefs
during the dry period.
In summary, although widely accepted for the resident ichthyo-
fauna, the hypothesis tested was refuted, considering that the
increase in the reef volume in the scale from 1 to 3 m
3
did not
correspond to the change in richness, number of individuals,
biomass and species diversity of the transient ichthyofauna. The
analysis per standardized volume unit revealed higher values of the
community descriptors and abundance of the most representative
families, Ariidae and Sciaenidae, in the 1 m
3
modules, suggesting
that small reefs attract a higher variety of representatives of the
transient ichthyofauna from a proportionally larger area than reefs
with greater volume.
5. Conclusions
The differences in the association pattern of species as a function
of the dry and rainy periods indicate that the seasonal inuence of
the ow of the Paraba do Sul River may mask the effects of the
different spatial congurations tested. This study highlights the
importance of combining habitat conguration at different periods
to fully understand and manage the tropical seascape. Therefore,
this factor should be considered in the implementation of articial
reefs in typically seasonal regions, such as those under strong in-
uence of uvial discharges, aiming for the management of the
transient ichthyofauna.
Acknowledgments
This work was funded by the Funda~ ao de Amparo a Pesquisa
Carlos Chagas Filho e FAPERJ, Brazil (E-26/110.437/2010) and the
Brazilian Agency for Research Development e CNPq (470997/2010-
9). We are grateful to Dr. Bruno P. Masi for his diving assistance.
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