O R I G I N A L Effects of substratum type on fish assemblages in shallow areas of a tropical...

ORIGINAL ARTICLE

Effects of substratum type on fish assemblages in shallowareas of a tropical estuaryJos�e Amorim Reis-Filho1,2 & Alexandre Clistenes de Alcantara Santos3

1 Laborat�orio de Ecologia Bentonica, Universidade Federal da Bahia - UFBA, Salvador, Brazil

2 ECUS Institut. Education, Science and Socio-Environmental Utility, Salvador, Brazil

3 Laborat�orio de Ictiologia, Universidade Estadual de Feira de Santana, Feira de Santana, Brazil

Keywords

Bioindicator species; fish fauna; Paraguac�uriver; sedimentation; tropical estuary.

Correspondence

Jos�e A. Reis-Filho, Laborat�orio de Ecologia

Bentonica, Universidade Federal da Bahia,

Ondina, 40170-000, Salvador, Brazil.

E-mail: [email protected]

Accepted: 8 August 2013

doi: 10.1111/maec.12102

Abstract

While there is already a comprehensive understanding of the effects of environ-

mental variables, such as dissolved oxygen, temperature and salinity, on the

structure, biomass and metabolism of aquatic biota in estuarine habitats, the

effect of sedimentation, a harmful underlying factor, remains unclear. The aim

of this study was to assess the differences in fish assemblages along the freshwa-

ter to salt water gradient of a large tropical estuary, and to evaluate the effects

on them of habitat disturbance associated with shallow water sedimentation in

the intertidal areas. Fish and environmental variables were recorded in the

upper, middle and lower salinity zones of the estuary at ebb tide in both the

dry and wet seasons. Sediment samples associated with different levels of habi-

tat disturbance were analysed using granulometry, and their organic content

and dissolved oxygen levels were quantified. Water temperature, salinity, pH

and dissolved oxygen levels were also measured. Habitat disturbance was found

to be correlated with the density, biomass and richness of fish assemblages.

A total of 77 species were recorded, forming two distinct fish assemblages, with

the Eleotridae family dominating in the upper zone, and Gerreidae, Gobiidae

and Tetraodontidae the most common in the middle and lower estuary.

Changes in the structure of fish assemblages, including reductions in density,

biomass and richness, were associated with disturbance to natural features,

where muddy sediment was replaced by sandy sediment and the quantity of

organic matter fell. Atherinella brasiliensis was the species which showed a pref-

erence for the disturbed areas in the middle and lower zones, while Dormitator

maculatus showed a preference for them in the upper estuary. They may be

taken as indicators of habitat disturbance due to shallow sedimentation.

Introduction

Estuaries and their surroundings provide refuge, feeding

and reproduction sites, as well as nurseries for fish, but

are found in areas where the generation of stressors is

particularly high, since they also attract diverse human

activities (Sheaves et al. 2012). The quantity and intensity

of agents produced by those activities are having an

increasing impact on many coastal areas (Halpern et al.

2008), and estuaries which, being particularly vulnerable,

have been severely degraded (Kennish 2002; Lotze et al.

2006). Many estuarine fish species are economically valu-

able and habitat disturbance also has the potential to

affect the dynamics of traditional communities and their

fisheries (Jenkins et al. 1997; Franc�a et al. 2012).

To assess environmental and ecological changes within

an estuary, many studies have used fish communities to

direct management actions (Whitfield & Elliott 2002;

Harrison & Whitfield 2004; Ode et al. 2005). Although

assessments based on nekton assemblage structure have

Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH 1

Marine Ecology. ISSN 0173-9565

an obvious appeal to managers, the imperative to pro-

duce the most accurate measurements possible has seen a

move away from simple composite measurements

towards complex multivariate approaches. Ideally, effec-

tive assessments should be simple to construct and com-

municate, relate directly to definable biological attributes

and show demonstrable ranges for known impacts

(Sheaves et al. 2012). Despite the ‘estuarine quality para-

dox’, which suggests that estuarine fish assemblages are

adapted to a physically demanding environment, in which

natural and anthropogenic stressors have similar features

(Elliott & Quintino 2007), simple reporting approaches can

be developed, even when it is necessary to assess reliable

information prior to determine a broad set of environmental

quality indices, particularly on the potential for anthropogen-

ically altered sediments loads (Sheaves et al. 2012).

Sedimentation has been a threat to biodiversity in most

aquatic ecosystems (Atalah & Crowe 2010). Coastal areas

adjacent to catchments with considerable human develop-

ment, intensive irrigated agriculture or erosion due to

overgrazing are expected to receive increased sediment

loadings in the near future (Atalah & Crowe 2010) and

this constitutes a threat to fish fauna. Within the mosaic

of estuarine habitats, sub-tidal channels are among the

most frequently and heavily impacted by activities such

as dredging which cause sediment alterations (Wilber &

Clarke 2001; Franc�a et al. 2012). Changes in the sedi-

ments may result in a fall in the stocks of some species

(Perez-Ruzafa et al. 1991; Harley et al. 2001); however,

for intertidal areas in which the sediment type is already

a source of fish fauna variability (Le Pape et al. 2003;

Vinagre et al. 2006, 2010), little is known about the

effects of sedimentation in shallow waters on fish assem-

blages, especially in tropical regions, and the mechanisms

influencing them may well be different. In this context,

intertidal habitats with muddy sediments rich in organic

matter, which are predominant in many estuaries and

provide shelter and food for fish populations, are highly

relevant (Ribeiro et al. 2006; Vinagre et al. 2006).

The Paraguac�u River, which is the main tributary of

the Todos os Santos Bay, is one of the most important

aquatic systems in the state of Bahia, Brazil. This system

is of great importance for wildlife conservation and pro-

vides the main source of protein and income, i.e. con-

sumption and commercialization of fish and shellfish, for

the local communities (Barros et al. 2008; Reis-Filho

et al. 2011). The high rates of sedimentation can compro-

mise the maintenance and development of aquatic biota,

especially fish, which are already adapted to the natural

conditions. Furthermore, the lack of flooding events due

to a dam upstream which hinders the input and accumu-

lation of sediment may contribute to shallow habitat dis-

turbance. The aim of this study is to verify whether the

accumulation of sediment which differs from the original

cover alters shallow water fish assemblages, to detect the

effects of this on the fish population, and to determine

which variables should be taken into account in future

management actions.

Material and Methods

Study area

The Paraguac�u River basin has an area greater than

50,000 km2 and several anthropogenic activities, such as

domestic effluent and solid waste disposal and agriculture,

influence the system (CRA 2004). The estuary has an area

of 127.9 km2 (Fig. 1) and semi-diurnal tides, with spring

tides ranging between 1.8 and 2.9 m and neap tides of

0.6–1.5 m. In the rainy season from March to August the

monthly precipitation is �280 mm per month; in the dry

season it is �110 mm per month (Cirano & Lessa 2007).

The estuary’s hydrological regime was modified in 1985

by the completion of the Pedra do Cavalo dam and the

effects of river flow control on fish are already noticeable

(Reis-Filho et al. 2010). Human occupation of the hills

adjacent to the estuary has increased erosion rates, and

the contribution of sediment from the slopes is gradually

burying the estuary banks and mangrove vegetation,

slowly replacing the muddy sediment with sandy sedi-

ment. The estuary can be divided into three zones based

on salinity measurements: (i) the upper estuary, where the

influence of the tide is slight and fluvial reaches present

salinity values below 5; (ii) the dynamic middle estuary

(Iguape bay), where tide and river flows interact most

intensively, with an average depth of 5 m and including a

76.1-km2 area of dense mangrove; and (iii) the lower estu-

ary, with an average depth of 18 m (Cirano & Lessa

2007), where mangroves dominate the landscape and pas-

tures contribute to shallow sedimentation.

Experimental design and data analysis

Shallow areas along the estuary show evidence of habitat

disturbance, such as sandy substrate in shallow areas and

a decrease in mangrove vegetation due to marginal silting

(Supporting Information Appendix). Exploratory sam-

pling intended to quantify areas affected by sedimentation

served to identify two habitat types: disturbed and undis-

turbed. Three different sampling zones were defined on

the basis of salinity (Fig. 1; Garc�ıa et al. 2010) and the

randomized block design suggested by Hurlbert (1984)

was applied to both habitat types within each salinity

zone, with the aim of obtaining independent replicates.

Fish sampling was carried out in each salinity zone every

4 months from August 2009 to July 2010 using a seine

2 Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH

Effects of substratum type on fish assemblages Reis-Filho & Santos

net (15 m long, 2 m high and with 12-mm mesh wings

and a 9-mm cod-end mesh). Marginal transects of 50 m

were sampled in daylight on the three central days of the

full moon at the lowest level of the ebb-tide. The average

aperture of the seine net (distance from extremity to

extremity) was 7 m and the average depth 1.5 m. A total

of 120 samples were taken (five in disturbed areas and

five in undisturbed areas of each salinity zone) over

a

b

Fig. 1. Location of the Paraguac�u river estuary with sampling in each zone (black stars = disturbed habitat, empty stars = undisturbed habitat).


Reis-Filho & Santos Effects of substratum type on fish assemblages

4 months (Fig. 1). Using data on the distance between col-

lectors and by measuring the total distance covered at the

beginning and end of each drag using GPS (Garmin III), we

were able to calculate the area sampled using the formula

(A): A = D 9 h 9 X2, where D is the transect length, h is

the distance between collectors, and X2 corresponds to the

the head-rope length, which is equal to the path swept on

each trawl (adapted from Sparre & Venema 1995). In this

study, sampling was carried out at speeds of 0.5–1 m � s�1

and assuming that X2 = 0.3, each area sampled measured

100 m2, meaning the total area sampled for the entire estuary

measured 12,000 m2. Captured fish were immediately fixed

in a 4% formaldehyde solution to preserve diagnostic charac-

teristics and were weighed and identified in the laboratory.

Environmental parameters such as water and sediment

temperature, salinity, water pH, and the level of dissolved

oxygen in the water and the interstitial water of the sediment

were measured following the same spatial-temporal criteria

used for the fish samples. Temperatures were taken with a

digital thermometer, salinity was measured using an optical

refractometer, and dissolved oxygen was quantified using a

portable digital oximeter with a resolution of 0.01 mg�l�1.

Sediment samples from both disturbed and undisturbed

habitats in each salinity zone were analysed using granulom-

etry. The organic matter content was determined by the

Walkley–Black method as modified by Jackson (1982).

Statistical analysis

Distribution patterns of fish and differences in density,

biomass and richness were analysed using a sampling

plan based on both location (salinity zones and habitat

types) and seasonal change. A 2-way ANOVA was used to

analyse the disturbed and undisturbed habitats (fixed fac-

tor) and the upper, middle and lower estuaries (fixed fac-

tor). A one-way ANOVA was used to differentiate between

the wet and dry seasons. Data was log transformed to

verify that the distribution was normal. The Cochran test

was used to check the homoscedasticity of variance and

multiple comparisons were verified using the Student–Newman–Keuls’ (SNK) test. The alpha value was corrected

using Bonferroni’s method (0.012) to avoid Type I Error

(Underwood 1981). Estimates of negative variance were

approximated to zero and all other values were recalculated

according to the procedure described by Fletcher & Under-

wood (2002). STATISTICA 8.0 (StatSoft 2007; www.statsoft.

com) software was used to carry out the above-mentioned

analysis. A 2-way PERMANOVA with a reduced model using

9999 permutations and Bray–Curtis dissimilarities was car-

ried out on the raw data using PERMANOVA v.1.6 software

(Anderson 2005), and Euclidean distance was used for the

presence or absence of data to evaluate differences between

disturbed and undisturbed habitats and estuarine zones, as

well as their interactions regarding the composition of fish

species (Anderson 2001, 2005). Pseudo-variance compo-

nents, which can be considered to be analogues of univariate

ANOVA (Searle et al. 1992), were calculated for each term in

the model. Those components were expressed both as actual

variance and as percentages to determine their relative con-

tribution to the distribution pattern observed. To obtain

information about how different characteristics of the assem-

blages, such as abundance or rarity, influence the estimated

pseudo-variance components, those estimates were also cal-

culated as present/absent data.

Principal component analysis (PCA) was used to iden-

tify the relationships between stations and environmental

variables including water and sediment temperature, dis-

solved oxygen in water and interstitial water, pH, salinity

and the quantity of organic matter. The analysis was car-

ried out using the correlation matrix (standard deviation)

to balance the relative contribution of each variable on

the same scale and to preserve the Euclidean distance

(Legendre & Legendre 2003). The method of standardiza-

tion followed that proposed by Gotelli & Ellison (2011),

i.e. Ƶ = (i–�y)/s, where i is the value of each measurement,

�y is the mean of all values of that measurement, and s is

the estimated standard deviation. The assumption regard-

ing the normality of the variables was verified using the

Shapiro–Wilk test (Legendre & Legendre 2003). Water tem-

perature was the only variable which had to be log-trans-

formed(x + 1) to reach normal distribution. A 2-way ANOVA

was also done to find differences between disturbed and

undisturbed habitat and estuary zones, using the first three

axes extracted from the PCA for each salinity zone, since the

new variables generated were orthogonal and became inde-

pendent (Gotelli & Ellison 2011). The linear independence of

organic matter and dissolved oxygen in the sediment was

tested using the Pearson correlation to verify the absence of

covariance (Legendre & Legendre 2003).

A canonical correspondence analysis (CCA) was

applied to the fish density matrix (dependent data) and

to the environmental data matrix (independent data) to

investigate the relationships between species assemblages

and environmental variables. The ordination was carried

out independently for each salinity zone to decrease the

influence of salinity on the association between assem-

blages and other predicted variables. Finally, an ordina-

tion with samples from all three salinity zones was done

to observe the influence of salinity on the model

explained by other variables. This method evaluates dif-

ferent habitat preferences (niches) in the ordination dia-

gram (ter Braak & Verdonschot 1995). Since CCA is

sensitive to rare species (ter Braak 1987), species that

occurred in less than 20% of the samples were re-sized,

multiplying their relative frequency by their frequency of

occurrence (Orl�oci 1978). Inter-group correlation was



used to evaluate the relative importance of each environ-

mental variable in determining the ordination of species

abundance. The permutation for Monte Carlo was used to

test statistical significance (P < 0.05) for the contribution

of each variable in the CCA axes. Multivariate analyses for

ordination were carried out using R Project 2.12.0 (R

Development Core Team 2005).

Results

Spatial variance of environmental parameters

The highest salinity values, between 26 and 35, were

found in the lower estuary (the Paraguac�u channel). In

the middle estuary (Iguape Bay), salinity varied between 6

and 24, and in the upper estuary the values were between

0 and 6. There was no difference in salinity between the

dry and wet seasons, probably due to the dam, which reg-

ulates the downstream flow (Fig. 2). Values for dissolved

oxygen in interstitial water were significantly lower than

those found in the water column, almost reaching zero.

The values in disturbed areas, especially in the wet season,

were slightly higher than in undisturbed areas. Values for

organic matter were much higher in undisturbed muddy

margins than silted margins. Regarding the grain size of

sediment, we observed differences for entire estuarine

zones where disturbed habitats showed coarse sediments

and undisturbed habitats with lower sedimentation and

Fig. 2. Measurements of environmental

variables for disturbed and undisturbed

habitats in the upper, middle and lower

estuary in both dry and wet seasons.



small grains. In each of the estuarine zones, at least one

specific area showed a high level of disturbance, the

upper and lower estuary being the zones most affected

(Fig. 3). Since organic matter and dissolved oxygen in

interstitial water showed pronounced differences between

disturbed and undisturbed areas, Pearson correlation

analysis (R2 = 0.35, P-value = 0.63) was used to demon-

strate that those descriptors do not co-vary, by verifying

linear independence between them. The 2-way ANOVA of

the PCA, created by ordination, shows a difference

between disturbed and undisturbed areas [PC1:

F = 14.45, P-value = 0.001 (undist > dist); PC2:

F = 5.23, P-value = 0.03 (undist > dist)]. The difference

is a consequence of the high values for organic matter

found in muddy margins and the dissolved oxygen values

for interstitial water, which were higher in disturbed

areas. This analysis was carried out using the scores gen-

erated by the PCA to maximize the differences between

the original variables, since the Euclidean distance is pre-

served in the rotation procedure (Legendre & Legendre

2003). In the analyses of PCA, the first three axes explain

85.2% of the variation and axis I shows that the organic

matter variable was positively correlated to the vast

majority of muddy shallow areas in all three salinity

zones of the estuary.

Fish fauna composition

A total of 7987 fish from 77 different species (46 fami-

lies), weighing 76.27 kg, were collected (Table 1). The

greatest number of species (n = 7) were from the Gobii-

dae family, followed by Gerreidae (6), Carangidae (6) and

Engraulidae (5). The families with greatest densities in

the upper estuary were Eleotridae (43.7%), Gerreidae

(19.1%) and Tetraodontidae (15.2%). In the middle estu-

ary, Gerreidae (45.4%), Gobiidae (28.8%), Tetraodontidae

(16.7%) and Paralichthidae (11.5%) were the most abun-

dant families, and in the lower estuary, Gerreidae

(41.6%), Gobiidae (22.9%), Paralichthidae (12.5%) and

Atherinopsidae (11.3%) had the greatest densities.

In general, the species which represented the majority

(>70%) of individuals found in each estuary zone were:

Eleotris pisonis, Microphis brachyurus, Sphoeroides testudin-

eus, Dormitator maculatus, Eucinostomus argenteus,

Fig. 3. Distribution of grain size throughout

the Paraguac�u river estuary in broad areas

where there has been high sedimentation

and no or little effect. UE = Upper estuary,

ME = Middle estuary and LE = Lower estuary.

For sample points in both undisturbed and

disturbed areas see Fig. 1.



Table 1. Density (%) and biomass (%) of the fish captured in the Paraguac�u River estuary in the disturbed and undisturbed areas.

Species

Density (%) Average biomass (%)

Upper Middle Lower Upper Middle Lower

Eleotris pisonis 27.93 20.15

Dormitator maculatus 21.77 21.29

Microphis brachyurus 13.42 8.56

Astyanax sp. 1.92 2.98

Geophagus brasiliensis 1.11 5.89

Sphoeroides testudineus 8.91 11.91 1.23 12.07 14.53 9.87

Eucinostomus argenteus 6.71 9.49 5.94 9.61 10.82 7.11

Trinectes paulistanus 6.43 2.29 0.87 5.11 0.97 1.29

Diapterus rhombeus 3.29 25.2 23.9 7.45 31.4 25.6

Mugil sp. 3.72 2.98 2.91 1.98 2.39 1.87

Citharichthys spilopterus 1.19 8.62 8.61 1.43 3.41 2.78

Centropomus parallelus 1.02 2.51 1.98 3.98 6.34 3.71

Ctenogobius smaragdus 0.74 1.23 0.91 0.08 0.23 0.31

Ctenogobius stomatus 0.71 6.01 3.07 0.06 2.49 1.98

Achirus declives 0.54 1.98 0.27 0.08 1.82 1.21

Ctenogobius boleossoma 0.08 0.39 0.41 0.03 0.11 0.15

Mugil curema 0.08 1.07 0.08 0.03 0.03 0.03

Sphoeroides greeleyi 0.02 0.06 0.05 0.02 0.03 0.03

Ctenogobius stigmaticus 4.32 14.2 1.23 2.01

Atherinella brasiliensis 9.97 9.65 5.69 6.61

Sphoeroides greeleyi 0.97 6.08 1.27 4.98

Gobionellus oceanicus 0.98 1.17 2.11 3.21

Symphurus plagusia 0.15 0.09 0.23 0.18

Centropomus undecimalis 0.05 0.09 0.1 0.11

Eucinostomus melanpterus 0.12 0.09 0.09 0.05

Eucinostomus gula 0.05 0.25 0.04 0.18

Chaetodipterus faber 0.17 0.8 0.05 0.09

Caranx latus 0.23 0.39 0.9 1.09

Ogcocephalus vespertilio 0.31 0.22 1.8 2.2

Achirus lineatus 1.1 0.8 1.8 2.3

Diplectrum radialle 0.9 1.2 1.19 1.8

Bathygobius soporator 0.12 0.21 0.19 0.32

Lutjanus synagris 0.87 1.17 0.67 0.87

Prionotus punctatus 0.18 0.98 0.87 1.08

Anchoa marini 0.02 0.08 0.7 0.9

Polydactylus virginicus 1.19 0.76 1.02 0.98

Dactylopterus volitans 0.7 0.9 0.34 0.78

Paralichthys brasiliensis 0.32 0.87 0.7 0.91

Etropus crossotus 0.56 0.69 0.12 0.35

Lutjanus jocu 0.43 0.23 0.87 0.45

Oligoplites saliens 0.19 0.89 0.24 0.76

Anchoa spinifera 0.3 0.5

Stelifer rastrifer 0.9 1.75

Cynoscion microlepidotus 0.2 0.9

Cynoscion leiarchus 0.05 0.05

Hyporhamphus unifasciatus 0.09 0.05

Fistularia tabacaria 0.12 0.08

Carangoides bartholomaei 0.87 0.66

Chloroscombrus crysurus 0.09 0.08

Haemulon stendachneri 0.9 0.8

Archosargus rhomboidialis 0.1 0.9

Scomberomorus brasiliensis 0.09 0.1

Sphyraena guachancho 0.07 0.08

Sphyraena barracaduda 0.07 0.09



Trinectes paulistanus and Diapterus rhombeus, correspond-

ing to 88.4% of individuals found in the upper estuary;

Diapterus rhombeus, S. testudineus, E. argenteus, Citharich-

thys spilopterus, Ctenogobius stomatus, Ctenogobius stigmaticus

and Atherinella brasiliensis in the middle estuary (75.5%);

and D. rhombeus, Ctenogobius stigmaticus, Sphoeroides gree-

leyi, C. spilopterus, Ctenogobius stomatus, E. argenteus and

Atherinella brasiliensis in the lower estuary (71.4%; Fig. 4a–c).The species with greater densities that were common to all

three estuarine zones were: D. rhombeus [upper (3.29%),

middle (25.2%) and lower (23.9%)] and E. argenteus [upper

(6.71%), middle (9.49%) and lower (5.94%)].

Spatial and temporal fish fauna structure

Total fish density, biomass and richness were significantly

affected by habitat (Table 2; 2-way ANOVA), even though

the patterns of differences varied locally for the most abun-

dant species. Fish densities were usually greater in undis-

turbed areas than those affected by sedimentation and

there was no difference in density, biomass or richness

between the dry and wet seasons (P-value = 0.71, 0.67 and

0.52, respectively). The upper estuary had the lowest aver-

age density and biomass (30.9 ind�m�2 9 102 and

1966.6 g�m�2 9 102); the middle estuary showed the high-

est values (65.1 ind�m�2 9 102 and 4276.2 g�m�2 9 102);

and intermediate values were found in the lower estuary

(45.3 ind�m�2 9 102 and 2435.2 g�m�2 9 102). Species

richness was greatest in the lower estuary (69 species), with

intermediate values in the middle estuary (40 species) and

the lowest value in the upper estuary (18). There was a sig-

nificant interaction between habitats and salinity zones

(P = 0.002 and P = 0.001, respectively) with the greatest

fish densities and richness found in undisturbed areas of

the middle and lower estuary. The greatest component var-

iation was between sample replicates, i.e. residual variabil-

ity, followed by the contribution of the interaction of

habitat versus salinity zone for richness (Table 2).

There were significant differences in the dominant fish

density and biomass between the habitats and salinity

zones studied (Table 3). The biggest differences in density

in both disturbed and undisturbed areas were found in

the upper estuary and the greatest differences in biomass

were found in the middle and lower estuaries. The highest

multivariate variability for density occurred on the small-

est scale analysed, i.e. at the replicates and residual level.

The next greatest contribution was attributed to the inter-

action between salinity zones and habitats, due to the

habitat factor. The greatest variability regarding biomass

was due to the habitat factor. Results from data related to

Table 1. Continued

Species

Density (%) Average biomass (%)

Upper Middle Lower Upper Middle Lower

Lile piquitinga 0.4 0.06

Pomadasys corvaeniformes 0.5 0.3

Chilomycterus spinosus 1.2 2.9

Anchoa sp. 0.9 0.05

Albula vulpes 0.09 0.1

Oligoplites saurus 0.65 0.87

Anchoa elongata 0.09 0.86

Microgobius meeki 0.9 0.02

Strongylura marina 0.05 0.76

Scorpaena plumieri 0.05 0.05

Serranus flaviventris 0.09 0.67

Opistognathus cuvieri 0.05 0.05

Epinephelus itajara 0.05 0.8

Astrocopus y-graecum 0.05 0.05

Oligoplites palometa 0.05 0.05

Lobotes surinamensis 0.05 0.05

Eugerres brasiliensis 0.05 0.1

Gerres cinereus 0.05 0.9

Trinectes microphthalmus 0.05 0.05

Achantostracium quadricornis 0.05 0.05

Symphurus diomedianus 0.05 0.05

Syacium micrurum 0.05 0.05

Selene sp. 0.05 0.05

Gymnotorax ocelatus 0.05 0.05

∑ Fish 7987 76.27



presence/absence were similar to the results obtained

through residual data analyses (Table 3, PERMANOVA).

Changes in dominance between disturbed and undis-

turbed areas can be seen from the most abundant species

in each salinity zone. In the upper estuary, Eleotris pisonis,

Microphis brachyurus and Trinectes paulistanus showed the

greatest densities in undisturbed habitats and Dormitator

maculatus and Eucinostomus argenteus the greatest densi-

ties in disturbed habitat (Fig. 4a). Sphoeroides testudineus

did not appear to be affected by habitat changes in this

particular zone. In the middle estuary, Diapterus rhomb-

eus, S. testudineus, Citharichthys spilopterus, Ctenogobius

stomatus and Ctenogobius stigmaticus were the most abun-

dant species in undisturbed habitats (Fig. 4b). Atherinella

brasiliensis and E. argenteus, on the other hand, were

responsible for the greatest density values in impacted hab-

itats in the middle estuary (Fig. 4b). In the lower estuary,

D. rhombeus, C. stigmaticus, C. spilopterus and C. stomatus

were dominant in undisturbed areas, whereas A. brasilien-

sis and E. argenteus were dominant in disturbed areas

(Fig. 4c). In this salinity zone, Sphoeroides greeleyi did not

show exclusive preference for any type of habitat.

Influence of estuarine gradient and environmental variables

on fish assemblages

The simultaneous ordinations between species and envi-

ronmental variables in CCA matrices placed 10 species in

the upper, 12 species in the middle and 14 in the lower

estuary, based on density values. In the upper estuary, the

first two axes together explained 79.7% of the associa-

tions (Fig. 5a). Intra-group correlations showed that a

gradient between dissolved oxygen in interstitial water

and organic matter, which was positively associated with

axis I (P < 0.001), was responsible for structuring the

species Eleotris pisonis, Diapterus rhombeus, Trinectes pau-

listanus, Sphoeroides testudineus and Achirus declives in undis-

turbed habitats, and Dormitator maculatus and Eucinostomus

argenteus in disturbed habitats. In the middle and lower estu-

aries, the first two axes explained 88.6 and 91.2% of the asso-

ciations, respectively (Fig. 5b,c). Intra-group correlations

also showed organic matter and dissolved oxygen in intersti-

tial water as being responsible for structuring the species

D. rhombeus, S. testudineus, Citharichthys spilopterus, Cte-

nogobius stomatus and Ctenogobius stigmaticus in undis-

turbed habitats and Atherinella brasiliensis in disturbed

habitats. For the ordination of the entire estuary (Fig. 5d),

the Monte Carlo test revealed that organic matter and salin-

ity were the main contributors to species distribution

(P > 0.02 and P > 0.03, respectively). Axis I was positively

correlated with organic matter in undisturbed habitats and

salinity in both disturbed and undisturbed areas, especially

in samples taken from the middle and lower estuaries.

Discussion

Effects of habitat disturbance

The present study investigated whether fish assemblages

in intertidal estuarine habitats sampled in daylight at ebb

a

b

c

Fig. 4. Most abundant species in undisturbed and disturbed habitats in

the three salinity zones (upper, middle and lower estuary). Epis: Eleotris

pisonis; Mbra: Microphys brachiurus; Stes: Sphoeroides testudineus;

Dmac: Dormitator maculatus; Earg: Eucinostomus argenteus; Tpau:

Trinectes paulistanus; Drho: Diapterus rhombeus; Cspi: Citharichthys

spilopterus; Csto: Ctenogobius stomatus; Csti: Ctomogobius stigmaticus;

Sgre: Sphoeroides greeleyi; Abra: Atherinella brasiliensis.



tide differ according to the shallow water sedimentation.

There was a decrease in the number of fish species, bio-

mass and density in the upper estuary, probably due to

the reduced geographic area, scarce mangrove vegetation

and advanced sedimentation process, which results in

lower habitat availability for the local fish fauna. Vinagre

et al. (2006) provided an analysis of habitat availability

for estuarine fish, where the presence of intertidal habitat

and muddy sediments are relevant variables for the estab-

lishment of fish populations. Besides the predominance

of disturbed habitats in this salinity zone, which may rep-

resent a barrier to fish populations, the construction of a

dam located only 20 km upstream may have prejudiced

the maintenance of a favorable habitat for fish due to the

regulation of river flow, as has been observed in other

tropical estuaries (Baird & Heymans 1996; Rowell et al.

2008).

Sediment deposition is widely recognized as a major

problem for the functioning of coastal ecosystems (Atalah

& Crowe 2010). Habitat disturbance in the evaluated

areas, shown by a reduced level of organic matter in sedi-

ment, has already been demonstrated in other tropical

regions (Cunha-Lignon et al. 2009). In areas disturbed by

anthropogenic actions (agro-pastoral activities and urban-

ization), the levels of organic matter were smaller than

those found in undisturbed areas, a finding confirmed by

the present study. Our results indicate that fish have a

preference for undisturbed estuarine margins, especially

in the middle and lower estuary, and frequently those

with muddy facies instead of sandy facies associated with

areas where sedimentation has occurred. This preference

for muddy areas in Northern Brazil is also mentioned by

Paiva et al. (2008). Muddy areas have high levels of sus-

pended solids common inside estuaries and can support

demersal fish communities, which feed mainly on benthic

organisms (Camargo & Isaac 2003). Vinagre et al. (2010)

also showed that estuarine nurseries are characterized,

among other variables, by mud substrate and high fish

abundance.

The relationship between environmental variables and

the distribution of organisms has been studied in detail

in large estuaries exposed to anthropic pressure (Akin

Table 2. Results of 2-way ANOVA for density, richness and biomass.

Variance Habitat (H) Zones (Z) H 9 Z Residual

Transformation

df1 2 2 114

F F Ev F Ev Ev

Density 53.13*** 19.39** 2.9 10.56* 1.8 12.53 Log(x + 1)

Richness 49.79*** 15.14** 3.2 13.24** 5.4 17.66 b

Biomass 32.65** 11.84* 2.1 2.37 n.s. 0.0a 10.91 Log(x + 1)

aNegative values were set to zero according to Fletcher & Underwood (2002).bNo need to transformation for homogeneous variance.

*P < 0.05; **P < 0.01; ***P < 0.001.

Ev, components of variance estimate (percentual contributions); n.s., not significant.

Table 3. Result of multivariate analysis of variance with permutation (PERMANOVA) based on Bray–Curtis dissimilarity with the reduced model

(a) and data of presence/absence (b) of the most abundant species (see legend to Fig. 4).

Variance df MS F ES Variance df MS F ES

(a) Density (a) biomass

Zones (Z) 2 4385.88 12.27** 225.2 (10.1) Zones (Z) 2 5443.43 17.19*** 335.1 (15.5)

Habitats (H) 1 917.9 21.81*** 398.3 (17.9) Habitats (H) 2 908.3 19.19** 996.3 (46.7)

Z 9 H 2 903.2 6.23** 498.7 (22.4) Z 9 H 2 803.2 0.98n.s. 60.7 (2.7)

Residuals 110 761.9 1097.5 (49.4) Residuals 110 709.2 408.8 (35.1)

Total 115 Total 115

(b) Presence/absence

Zones (Z) 2 4911.09 14.09** 219.4 (9.7)

Habitats (H) 1 939.1 27.71*** 451.3 (18.9)

Z 9 H 2 917.3 7.05** 518.9 (23.1)

Residuals 110 777.4 1119.5 (49.9)

Total 115

P-values were obtained with 9999 permutations of randomization. **P < 0.01; ***P < 0.001; n.s., not significant.



et al. 2005). However, the association of such environ-

mental variables with the causes of disturbance has been

a challenging task. In the Paraguac�u estuary, a possible

factor contributing to increased stress levels in an already

stressful situation in shallow disturbed areas may be the

constant high salinity (>30), which contributes to the low

values for density, biomass and richness compared with

other estuary zones. In the Palmar River estuary in Ecua-

dor, constantly high salinity values allied with the water

retention upstream due to shrimp farms were found to

be responsible for a decrease in richness (Shervette et al.

2007). It is well known that fresh water discharge, espe-

cially associated with a rainy season, contributes to the

mixohaline conditions of estuaries, helping to increase

richness (Flores-Verdugo et al. 1990; Laroche et al. 1997),

and this does not occur in the Paraguac�u estuary due to

the flow control imposed by the dam upstream.

Another possible explanation for the degree of habitat

disturbance, especially in highly impacted areas located in

the middle estuary, is the regular variation in salinity val-

ues due to tidal pulses. Changes in this parameter can

limit species distribution, resulting in different fish

assemblages (Neves et al. 2010). Our results for disturbed

areas are similar to those mentioned above, but in undis-

turbed areas in the middle estuary we found high density

and richness, probably due to the availability of food and

better preserved mangrove forests. Martino & Able

(2003) suggested that patterns in fish assemblage struc-

ture across large spatial scales, i.e. >10 km, are due to

individual species’ responses to dominant environmental

gradients, whereas smaller scale (1 km) patterns are due

to habitat selection, competition, and/or predator avoid-

ance strategies. In the present study the level of organic

matter was the environmental variable which best

explained fish assemblages in the CCA for undisturbed

areas. However, when salinity was analysed separately in

the different zones, it did not appear to be a major factor

influencing fish assemblages in disturbed areas. Expected

fish fauna distribution patterns in estuary zones which

are closely related to salinity variation (Thiel et al. 1995;

Maes et al. 1998) may therefore not occur due to the

habitat disturbance caused by sedimentation.

In the current study, separate influences on the struc-

ture of fish fauna were elicited for sedimentation and

salinity, especially when evaluated separately (CCA

singles), suggesting that the additive model of multiple

a

b

c

d

Fig. 5. Canonical Correspondence Analysis (CCA) with data density for the estuarine zones (a, b, c) and the entire estuary (d). Epsi: Eleotris

pisonis; Adec: Achirus declives; Stes: Sphoeroides testudineus; Drho: Diapterus rhombeus; Tpau: Trinectes paulistanus; Mbra: Mirophis

brachyurus; Earg: Eucinostomus argenteus; Mug sp.: Mugil sp.; Ast. sp.: Atyanax sp.; Dmac: Dormitator maculatus; Ecro: Etropus crossotus; Clat:

Caranx latus; Csto: Ctenogobius stomatus; Emel: Eucinostomus melanopterus; Abra: Atherinella brasiliensis; Csti: Ctnegobius stigmaticus; Egul:

Eucinostomus gula.



variables is more appropriate for investigating other

important factors in the structuring of assemblages, such

as organic matter. These results support the contention

that the nature of interactions among multiple factors

depends on the combinations of variables a given factor

is subjected to (Crain et al. 2008), in this case spatializa-

tion according to salinity zones. The effects of sedimenta-

tion were characterized by a trade-off between sediment-

tolerant and sediment-sensitive species (Fig. 5) which

drove changes in fish assemblages.

Recently, a study into fish habitat conservation listed

the causes of habitat loss in South America. The list

included factors such as deforestation, the damming of

rivers, overfishing, the introduction of exotic species and

poor fisheries management (Barletta et al. 2010). Our

results also attribute habitat loss to the replacement of

muddy sediment, rich in organic matter, with sandy sedi-

ment. However, habitat disturbance due to shallow water

sedimentation requires further studies in a greater num-

ber of estuaries, possibly including the effects of lunar

phases, tides and diurnal variation, all of which may add

operational complexity but would certainly help to char-

acterize these effects with greater confidence. The Para-

guac�u River estuary is a large system which, as expected,

has a greater number of species than present in small

estuarine systems (Blaber 2000; Guzman & Raz-Huidobro

2002); however, without a parallel investigation into the

abundance of potential prey (Wouters & Cabral 2009), it

remains difficult to assess to what extent these results

may be influenced by variations in resource availability.

Measuring these effects is especially difficult in the

absence of historical data for the Paraguac�u region that

would allow us to compare the present situation with the

scenario prior to the construction of the Pedra do Cavalo

dam, which may contribute to sediment retention.

Bioindicator species

There is evidence that, in the gradual transition from a

more complex to a less complex habitat, there are often

species, known as colonizers, that are able to manage

such a transition efficiently (Airoldi et al. 2008). In the

shallow estuarine areas studied, especially in the middle

and lower estuaries, the loss of muddy habitats and the

reduction of resident fish fauna are evident from the par-

tial or total substitution of habitats with sandy substrate

and a loss of vegetation, as well as the dominance of pio-

neer species such as Atherinella brasiliensis and Eucinosto-

mus argenteus. In a scenario of environmental stress, such

as the one evaluated in the present study, species diversity

tends to diminish (Odum 1983). A stressful situation can

cause changes in the relative abundance of certain species

(Fausch et al. 1990), as in the example of Gerreidae fish

species, which, despite showing resistance to salinity

changes (Castillo-Rivera et al. 2005), reduced their habi-

tat use by 80% when environmental conditions were not

favorable (low level of organic matter and mostly sandy

sediment). The species A. brasiliensis is already known for

its resistance to numerous changes in habitat and was

found among the resilient species following the recent red

tide event in the adjacent Todos os Santos Bay, at the

mouth of the Paraguac�u River estuary (Reis-Filho et al.

2012).

Changes in fish community were observed in shallow

areas of the upper estuary, where Dormitator maculatus

presented high densities in comparison with Eleotris piso-

nis, Microphis brachyurus, Sphoeroides testudineus and

Trinectes paulistanus, which were dominant in undis-

turbed areas. Dormitator maculatus is common in transi-

tional habitats with salinity levels above 1.5 (Teixeira

1994; Miranda-Marure et al. 2004) and is abundant when

anthropogenic activities such as deforestation and pollu-

tion are present (Abilhoa & Duboc 2004).

Despite such gaps in our knowledge, the present study

has contributed to the discussion about heterogeneous

habitats in the estuarine environment as an essential place

occupied by macrophytes and wood debris which can

lead to structural complexity and consequently to a spa-

tial heterogeneity that may be favorable to increases in

fish diversity (Keefer et al. 2008). Our results show that a

structurally homogeneous habitat with mostly muddy

sediment can supply food in abundance, promoting high

fish density and richness. It is important to understand

how the inherent variability of fish assemblages in estua-

rine environments could be minimized by stratifying hab-

itat type and thereby the interaction with the

sedimentation levels. More accurate and specific

approaches, appropriate for each habitat type within an

estuary, are needed to produce stable and repeatable data

and represent the shallow fish fauna of an estuary as

completely as possible without becoming overwhelmed by

long explanations. The current approach gives us an

insight into the spatial division of fish fauna in a large

estuary, where the effects of shallow sedimentation and

the consequent habitat disturbance can cause changes in

fish assemblages. Although we sampled the whole salinity

gradient in this estuarine system, there were overt signs

of distress which might alter the expected spatial distribu-

tion patterns, such as the natural influence of the salinity

gradient on fish fauna.

Acknowledgements

The Coordenac�~ao de Aperfeic�oamento de Pessoal de N�ıvel

Superior (CAPES) provided a scholarship to J. A. Reis-Fil-

ho. ICHTUS (Environmental Solutions) Ltda. and the



Federal University of Bahia (UFBA) provided the infra-

structure and facilities for the work. The present study

was conducted with the authorization (no. 21581-7) of the

Instituto Chico Mendes de Conservac�~ao da Biodiversidade

(ICMBio). We would also like to thank Dr. Eduardo Mendes

da Silva (UFBA), Dr. Francisco Barros (UFBA) and Dr. Jo~ao

Paes Vieira (FURG) for their support during the writing

phase of this study. We also thank the two anonymous refer-

ees for their thoughtful comments.

References

Abilhoa V., Duboc L.F. (2004) Peixes - �Agua Doce. In: Mikich

S.B., B�ernils R.S. (Eds), Livro Vermelho da Fauna Ameac�adano Estado Paran�a. http://www.pr.gov.br/iap (accessed 3

April 2013).

Airoldi L., Balata D., Beck M.W. (2008) The Gray Zone:

relationships between habitat loss and marine diversity and

their applications in conservation. Journal of Experimental

Marine Biology and Ecology, 366, 8–15.

Akin S., Buhan E., Winemiller K.O., Yilmaz H. (2005) Fish

assemblage structure of Koycegiz lagoon-estuary, Turkey:

spatial and temporal distribution patterns in relation to

environmental variation. Estuarine, Coastal and Shelf Science,

64, 671–684.

Anderson M.J. (2001) A new method for non-parametric

multivariate analysis of variance. Australia Ecology, 26, 32–46.

Anderson M.J. (2005) PERMANOVA: A FORTRAN Computer

Program for Permutational Multivariate Analysis of Variance.

Department of Statistic, University of Auckland, New

Zealand, Auckland.

Atalah J., Crowe T. (2010) Combined effects of nutrient

enrichment, sedimentation and grazer lost on rock pool

assemblages. Journal of Experimental Marine Biology and

Ecology, 388, 51–57.

Baird D., Heymans J.J. (1996) Assessment of ecosystem

changes in response to freshwater inflow of the Kromme

River Estuary, St Francis Bay, South Africa: a network

analysis approach. Water SA, 22, 307–318.

Barletta M., Jaureguizar A.J., Baigun C., Fontoura N.F.,

Agostinho A.A., Jimenes-Segura L.F., Giarrizzo T., Fabr�e

N.N., Batista V.S., Lasso C., Taphorn D.C., Costa M.F.,

Chaves P.T., Vieira J.P., Correa M.F.M. (2010) Fish and

aquatic habitat conservation in South America: a

continental overview with emphasis on neotropical systems.

Journal of Fish Biology, 76, 2118–2176.

Barros F., Hatje V., Figueiredo M.B., Magalh~aes W.F., D�orea

H.S., Em�ıdio E.S. (2008) The structure of the benthic

macrofaunal assemblages and sediments characteristics of

the Paraguac�u estuarine system, NE, Brazil. Estuarine,

Coastal and Shelf Science, 78, 758–762.

Blaber S.J.M. (2000) Tropical Estuarine Fishes: Ecology,

Exploitation and Conservation. Blackwell Science, Melbourne:

372.

ter Braak C.J.F. (1987) The analysis of vegetation-environment

relationships by canonical correspondence analysis.

Vegetation, 69, 69–77.

ter Braak C.J.F., Verdonschot P.F.M. (1995) Canonical

correspondence analysis and related multivariate methods in

aquatic ecology. Aquatic Sciences, 57, 255–289.

Camargo M., Isaac V.J. (2003) Ictiofauna estuarina. In:

Fernandes M.E.B. (Ed.), Os Manguezais da Costa Norte

Brasileira. Fundac�~ao Rio Bacanga, S~ao Luis: 257.

Castillo-Rivera M., Montiel M., Sanvicente-An~orve L., Z�arate R.

(2005) Spatial, seasonal and diel distribution patterns of two

species of mojarras (Pisces: Gerreidae) in a Mexican tropical

coastal lagoon. Journal of Applied Ichthyology, 21, 498–503.

Cirano M., Lessa G.C. (2007) Oceanographic characteristics of

Ba�ıa de Todos os Santos, Brazil. Revista Brasileira de

Geof�ısica, 25, 363–387.

CRA – Centro de Recursos Ambientais – Cons�orcio Hydros

CH2MHILL. (2004) Diagn�ostico do Grau de Contaminac�~aoda Ba�ıa de Todos os Santos por Metais Pesados e

Hidrocarbonetos de Petr�oleo a Partir da An�alise das Suas

Concentrac�~oes nos Sedimentos de Fundo e na Biota Associada.

CRA, Bahia, Brazil: 366.

Crain C.M., Kroeker K., Halpern B.S. (2008) Interactive and

cumulative effects of multiple human stressors in marine

systems. Ecology Letter, 11, 1304–1315.

Cunha-Lignon M., Coelho-Jr C., Almeida R., Menghini R.,

Correa F., Schaeffer-Novelli Y., Cintr�om-Molero G.,

Dahdouh-Guebas F. (2009) Mangrove forests and

sedimentary processes on the south coast of S~ao Paulo State

(Brazil). Journal of Coastal Research, 56, 405–409.

Elliott M., Quintino V. (2007) The estuarine quality paradox,

environmental homeostasis and the difficulty of detecting

anthropogenic stress in naturally stressed areas. Marine

Pollution Bulletin, 54, 640–645.

Fausch K.D., Lyons J., Karr J.R., Angermeier P.L. (1990) Fish

communities as indicators of environmental degradation.

American Fisheries Society Symposium, 8, 123–144.

Fletcher D.J., Underwood A.J. (2002) How to cope with

negative estimates of components of variance in ecological

field studies. Journal of Experimental Marine Biology and

Ecology, 273, 89–95.

Flores-Verdugo F., Gonz�alez-Far�ıas F., Ram�ırez-Flores O.,

Amezcua-Linares A., Y�anez-Arancibia A., Alvarez-Rubio M.,

Day J.W. Jr (1990) Mangrove ecology, aquatic primary

productivity, and fish community dynamics in the

Teacap�an-Agua Brava lagoon-estuarine system (Mexican

Pacific). Estuaries, 13, 219–230.

Franc�a S., Vasconcelos R.P., Reis-Santos P., Fonseca V.F.,

Costa M.J., Cabral H.C. (2012) Vulnerability of Portuguese

estuarine habitats to human impacts and relationship with

structural functional properties of the fish community.

Ecological Indicators, 18, 11–19.

Garc�ıa M.L., Jaureguizar A.J., Protogino L.C. (2010) From

fresh water to the slope: fish community ecology in the R�ıo



de la Plata and the sea beyond. Latine American Journal

Aquatic of Research, 38, 81–94.

Gotelli N.J., Ellison A.M. (2011) Princ�ıpios da Estat�ıstica em

Ecologia. Artmed, Porto Alegre: 527.

Guzman A., Raz-Huidobro L. (2002) Fish communities in two

environmentally different estuarine systems of Mexico.


Halpern B.S., Walbridge S., Selkoe K.A., Kappel C.V., Micheli

F., D’Agrosa C., Bruno J.F., Casey K.S., Ebert C., Fox H.E.,

Fujita R., Heinemann D., Lenihan H.S., Madin E.M.P.,

Perry M.T., Selig E.R., Spalding M., Steneck R., Watson R.

(2008) A global map of human impact on marine

ecosystems. Science, 319, 948–952.

Harley X., Koubi P., Grioche A. (2001) Ecology of plaice

(Pleuronectes platessa) in fish assemblages of beaches of the

Opale coast (North of France) during spring 1977. Cybium,

25, 67–80.

Harrison T.D., Whitfield A.K. (2004) A multi-metric fish

index to assess the environmental condition of estuaries.


Hurlbert S.H. (1984) Pseudoreplication and the design of

ecological field experiments. Ecological Monographs, 54, 187–

211.

Jackson M.L. (1982) Analisis Quimico de Suelos. Omega,

Barcelona: 282–309.

Jenkins G.P., May H.M.A., Wheatley M.J., Holloway M.G.

(1997) Comparison of fish assemblages associated with

seagrass and adjacent unvegetated habitats of Port Philip

Bay and Corner Inlet, Victoria, Australia, with emphasis on

commercial species. Estuarine, Coastal and Shelf Science, 44,

569–588.

Keefer M.L., Peery C.A., Wright N., Daigle W.R., Caudill C.C.,

Clabough T.S., Griffith D.W., Zacharias M.A. (2008)

Evaluating the NOAA coastal and marine ecological

classification standard in estuarine systems: a Columbia

River estuary case study. Estuarine, Coastal and Shelf Science,

78, 89–106.

Kennish M.J. (2002) Environmental threats and environmental

future of estuaries. Environmental Conservation, 29, 78–107.

Laroche J., Baran E., Rasoanandrasana N.B. (1997) Temporal

patterns in fish assemblage of a semiarid mangrove zone in

Madagascar. Journal of Fish Biology, 51, 3–20.

Le Pape O., Chauvet F., Mah�evas S., Lazure P., Ch�erault D.,

D�esaunay Y. (2003) Quantitative description of habitat

suitability for the juvenile common sole (Solea solea, L.) in

the Bay of Biscay (France) and the contribution of different

habitats to the adult population. Journal of Sea Research, 50,

139–149.

Legendre P., Legendre L. (2003) Numerical Ecology. Elsevier

Science, Amsterdam: 853.

Lotze H.K., Lenihan H.S., Bourque B.J., Bradbury R.H., Cooke

R.G., Kay M.C., Kidwell S.M., Kirby M.X., Peterson C.H.,

Jackson J.B.C. (2006) Depletion, degradation, and recovery

potential of estuaries and coastal seas. Science, 312, 1806–

1809.

Maes J., Van Damme P.A., Taillieu A., Ollevier F. (1998) Fish

communities along an oxygen-poor salinity gradient

(Zeeschelde Estuary, Belgium). Journal of Fish Biology, 52,

534–546.

Martino E.J., Able K.W. (2003) Fish assemblages across the

marine to low salinity transition zone of a temperate

estuary. Estuarine, Coastal and Shelf Science, 56, 969–987.

Miranda-Marure M.E., Mart�ınez-P�erez J.A., Brown-Peterson

N.J. (2004) Reproductive biology of the opossum pipefish,

Microphis brachyurus lineatus, in Tecolutla Estuary,

Veracruz, Mexico. Gulf and Caribbean Research, 16, 101–

108.

Neves L., Teixeira T.P., Ara�ujo F.G. (2010) Structure and

dynamics of distinct fish assemblages in three reaches

(upper, middle and lower) of an open tropical estuary in

Brazil. Marine Ecology, 32, 115–131.

Ode P.R., Rehn A.C., May J.T. (2005) Quantitative tool for

assessing the integrity of southern coastal California streams.

Environmental Management, 35, 493–504.

Odum H.T. (1983) Ecological and General Systems (Formerly

Systems Ecology). University Press of Colorado, Niwot: 644.

Orl�oci L. (1978) Multivariate Analysis in Vegetation Research.

Junk, The Hague: 451.

Paiva A.C.G., Chaves P.T.C., Ara�ujo M.E. (2008) Estrutura e

organizac�~ao tr�ofica da ictiofauna de �agas rasas em um

estu�ario tropical. Revista Brasileira de Zoologia, 25, 647–661.

Perez-Ruzafa A.C., Marcos-Diego C., Ros J.D. (1991)

Environmental and biological changes related to recent

human activities in the Mar Menor (SE of Spain). Marine

Pollution Bulletin, 23, 747–751.

R Development Core Team (2005) R: a Language and

Environment for Statistical Computing. R Foundation for

Statistical Computing, Vienna, Austria. http://

www.R-project.org (accessed 5 November 2012).

Reis-Filho J.A., Nunes J.A.C.C., Ferreira A. (2010) Estuarine

ichthyofauna of the Paraguac�u River, Todos os Santos Bay,

Bahia, Brazil. Biota Neotropica, 10, 301–312.

Reis-Filho J.A., Barros F., Nunes J.A.C.C., Sampaio C.L.S.,

Souza G.B.G. (2011) Moon and tide effects on fish capture

in a tropical tidal flat. Journal of the Marine Biological

Association of the United Kingdom., 91, 735–743.

Reis-Filho J.A., da Silva E.M., Nunes J.A.C.C., Barros F. (2012)

Effects of a red tide on the structure of estuarine fish

assemblages in Northeastern Brazil. International Review of

Hydrobiology, 97, 389–404.

Ribeiro J., Bentes L., Coelho R., Gonc�alves J.M.S., Lino P.G.,

Monteiro P., Erzini K. (2006) Seasonal, tidal and diurnal

changes in fish assemblages in the Rio Formosa lagoon

(Portugal). Estuarine, Coastal and Shelf Science, 67, 461–474.

Rowell K., Flessa K.W., Dettman D., Rom�an M.J., Gerber L.R.,

Findley L.T. (2008) Diverting the Colorado River leads to a

dramatic life history shift in an endangered marine fish.

Biological Conservation, 141, 1138–1148.

Searle S.R., Casella G., McCulloch C.E. (1992) Variance

Components. Wiley, Toronto: 501.



Sheaves M., Johnston R., Connolly R.M. (2012) Fish

assemblages as indicators of estuary ecosystem health.

Wetlands Ecology Management, 20, 477–490.

Shervette V.R., Aguirre W.E., Blacio E., Cevallos R., Gonzalez M.,

Pozo F., Gelwick F. (2007) Fish communities of a disturbed

mangrove wetland and an adjacent tidal river in Palmar,

Ecuador. Estuarine, Coastal and Shelf Science, 72, 115–128.

Sparre P., Venema S.C. (1995) Introduction to evaluation of

tropical fisheries resources. Part 1 – Manual, FAO Technical

Paper, 306/1, 339-334.

Teixeira R.L. (1994) Abundance, reproductive period, and

feeding habits of eleotrid fishes in estuarine habitats of

north-east Brazil. Journal of Fish Biology, 45, 749–761.

Thiel R., Sepulveda A., Kafeman R., Nellen W. (1995)

Environmental factors as forces structuring the fish community

of the Elbe estuary. Journal of Fish Biology, 46, 47–69.

Underwood A.J. (1981) Techniques of analysis of variance in

experimental marine biology and ecology. Oceanography and

Marine Biology, 19, 513–605.

Vinagre C., Franc�a S., Cabral H.N. (2006) Diel and semi-lunar

patterns in the use of an intertidal mudflat by juveniles of

Senegal sole, Solea senegalensis. Estuarine, Coastal and Shelf

Sience, 69, 246–254.

Vinagre C., Cabral H.N., Costa M.J. (2010) Relative

importance of estuarine nurseries for species of the genus

Diplodus (Sparidae) along the Portuguese coast. Estuarine,

Coastal and Shelf Science, 86, 197–202.

Whitfield A.K., Elliott M. (2002) Fishes as indicators of

environmental and ecological changes within estuaries: a

review of progress and some suggestions for the future.


Wilber D.H., Clarke D.G. (2001) Biological effects of

suspended sediments: a review of suspended sediment

impacts on fish and shellfish with relation to dredging

activities in estuaries. North American Journal of Fisheries

Management, 21, 855–875.

Wouters N., Cabral H.N. (2009) Are flatfish nursery grounds

richer in benthic prey? Estuarine Coastal and Shelf Science,

83, 613–620.

Supporting Information

Additional Supporting Information may be found in the

online version of this article:

Appendix S1. Disturbed and undisturbed habitats.



O R I G I N A L Effects of substratum type on fish assemblages in shallow areas of a tropical...

Documents

Transcript of O R I G I N A L Effects of substratum type on fish assemblages in shallow areas of a tropical...