Effects of environmental gradients on sandy beach macrofauna of a semi-enclosed bay

ORIGINAL ARTICLE

Effects of environmental gradients on sandy beachmacrofauna of a semi-enclosed bayRicardo S. Cardoso1, Gustavo Mattos2, Carlos H.S. Caetano3, Tatiana M.B. Cabrini1, LudmilaB. Galhardo1 & Felipe Meireis1

1 Laboratorio de Ecologia Marinha, Departamento de Ecologia e Recursos Marinhos, Universidade Federal do Estado do Rio de Janeiro (UNIRIO),

Rio de Janeiro, RJ, Brazil

2 Programa de Pos-Graduacao em Ecologia, Departamento de Ecologia, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, RJ, Brazil

3 Laboratorio de Zoologia de Invertebrados Marinhos, Departamento de Zoologia, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio

de Janeiro, RJ, Brazil

Introduction

Community ecology studies have addressed the spatial

variability of species richness (Ricklefs & Schluter 1993),

composition (Patterson & Atmar 1986), interspecific vari-

ability in abundance (Preston 1962), and distribution of

species (Brown 1984). These spatial and temporal varia-

tions in community and population descriptors can occur

in different habitats (Diamond & Case 1986).

In the macrofauna of sandy beaches, large-scale studies

have evaluated the pattern of community descriptors

(Dexter 1992; Ricciardi & Bourget 1999; McLachlan 2001;

Keywords

Beach; exposure rating; intertidal; large-scale;

macrofauna; morphodynamic; Sepetiba Bay,

Brazil.

Correspondence

Ricardo S. Cardoso, Laboratorio de Ecologia

Marinha, Departamento de Ecologia e

Recursos Marinhos, Universidade Federal do

Estado do Rio de Janeiro (UNIRIO), Rio de

Janeiro, RJ, CEP 22290-240, Brazil.

E-mail: [email protected]

Accepted: 13 April 2011

doi:10.1111/j.1439-0485.2011.00457.x

Abstract

Macrofauna of sheltered and pocket beaches located in embayments, estuaries

or landward of protective reefs has not been adequately assessed in beach ecol-

ogy. In this setting, the concurrent role of large-scale morphodynamics and

wave-exposure gradients in shaping biological patterns is still uncertain. To

examine variations in community descriptors and the influence of physical fac-

tors on macrofauna, 12 sandy beaches on five islands within Sepetiba Bay (SE

Brazil) were characterized in terms of beach morphodynamics and dimensions

(length and width), such as geographical position relative to the bay mouth.

A total of 80 species were collected and identified. Community descriptors of

macrofauna responded to morphodynamics and exposure gradients. Increases

in species richness, and abundance, from harsh reflective (coarse sands, steep

slopes) to benign dissipative (fine sands, gentle slopes) beaches, and from the

bay mouth (exposed beaches) towards the inner bay (sheltered beaches) were

observed. Mollusks were the most abundant macrofaunal group, followed by

crustaceans and polychaetes. Crustaceans dominated the beaches near the bay

mouth, whereas mollusks were more abundant on the beaches farther from the

bay mouth. Canonical correspondence analysis showed that the degree of expo-

sure, distance from the bay mouth, beach index, and beach length and width

significantly affected the macrofauna distribution and abundance, creating an

environmental gradient along Sepetiba Bay. Differences in macrofauna compo-

sition among the beaches studied were associated with beach length and width.

In this sense, spatial variation of macrofauna among beaches can be a function

of intertidal area. These results indicate that community characteristics in the

sandy beaches studied are affected by several physical characteristics, but also

by other factors that are affected by coastal processes.

Marine Ecology. ISSN 0173-9565

106 Marine Ecology 33 (2012) 106–116 ª 2011 Blackwell Verlag GmbH

Soares 2003) and the life history of populations (Defeo &

Cardoso 2002, 2004; Cardoso & Defeo 2003, 2004) on a

latitudinal gradient. However, Underwood & Petraitis

(1993) stated that large-scale differences can be better

explained by local differences in physical characteristics

(i.e. wave exposure) than by biogeographical effects.

Several studies have found consistent macrofauna com-

munity patterns in sandy beaches, which could be mainly

explained by variations in physical factors (i.e. grain size,

beach slope, swash processes) (McLachlan 1990; Jaramillo

& Gonzalez 1991; Defeo et al. 1992; Jaramillo & McLachlan

1993; Jaramillo et al. 1993; Veloso & Cardoso 2001; Veloso

et al. 2003). These predictions appear to be valid globally,

where sandy beach communities increase in richness, den-

sity, total abundance, and biomass compared with micro-

tidal reflective beaches (coarse sand and steep slope) to

macrotidal dissipative beaches (fine sand and gentle slope)

(McLachlan 1990; Defeo et al. 1992; McLachlan et al. 1993;

Ricciardi & Bourget 1999).

On the other hand, sandy beaches located in embay-

ments, estuaries or landward of protective reefs have been

neglected in macrofauna studies. Recently, Lercari & Defeo

(2006), and Rosa (2009) studied the salinity gradient in

sandy beaches, and found an increase in the species rich-

ness and total abundance of macrofauna from estuarine to

oceanic sandy beaches. However, the effects of morphody-

namics and physical factors on the macrofauna of sheltered

sandy beaches have not been adequately assessed in studies

of sandy beach ecology (Haynes & Quinn 1995; Amaral

et al. 2003; Arruda & Amaral 2003; Denadai et al. 2005).

The aim of the present study is to describe the composi-

tion and structure of sandy beach macrofauna within Se-

petiba Bay (Brazil) and to clarify the influence of some

rarely tested environmental variables (e.g. distance between

beach–bay mouth, length and width of beach) in these

biological descriptors. We test the hypothesis that the

macrofauna of sandy beaches within inner bays presents

higher values for community descriptors (species richness,

diversity, evenness, density, and biomass of both commu-

nity and most important species) than beaches located in

outer bays. Similar hypothesis were adopted in relation to

(i) beach dimensions (i.e. longer beaches have higher val-

ues for community descriptors than shorter beaches), (ii)

morphodynamics (i.e. beaches towards the dissipative

extreme show higher values of community descriptors).

Material and Methods

Study area

Sepetiba Bay (22�54¢–23�04¢ S; 44�34¢–44�10¢ W) is a sed-

imentary embayment located in Rio de Janeiro State,

Southeastern Brazil, with an area of 520 km2. It was

shaped by an extensive process of sand deposition, which

formed a barrier beach at its southern end. It ends in a

wide confluence with the Atlantic Ocean at its western

boundary (Azevedo et al. 2007). This bay holds one of

the most important commercial ports in the Brazilian

southeast region, with intense touristic, fishing, and

industrial activities.

This bay can be divided into three zones (inner, mid-

dle, and outer) according to environmental characteris-

tics. The islands, and consequently the beaches studied

for this paper, are in the outer zone, where the substrate

is mainly sandy, with a mean salinity of 33 and maximum

depth of approximately 28 m (Pessanha & Araujo 2003).

Twelve microtidal sandy beaches on five islands were

sampled in two periods, summer 2007 (Boi, Flexeiras,

Catita, Escalhau, Bonita, and Jardim) and summer 2008

(Gamboa, Leste, Estopa, Pitangueiras, Sul, and Pier)

(Fig. 1). Sampling was carried out during spring low tides

in the summers of both years to reduce biotic and abiotic

interannual variability linked to the seasonal cycle (Defeo

& Rueda 2002), and we did not consider changes between

years, as we focused only spatial analysis.

Field sampling and laboratory procedures

Biological samples were taken along five transects, equally

spaced perpendicular to the shoreline. On each transect,

10 equally spaced sampling units (SUs) were established,

the first (SU1) at the waterline, second last (SU9) on the

drift line, and the last (SU10) 3 m above the drift line

(supralittoral). One sample was taken with a 0.04 m2

quadrat sampler to a depth of 25 cm.

The collected sediment was sieved through a 0.50-mm

mesh, and the retained material was taken to the labora-

tory, where the organisms were sorted by species,

counted, and fixed in 5% buffered formalin.

Sediment samples for particle-size analysis were col-

lected with a 3.5-cm diameter corer to a depth of 15 cm

at strata 1 (lower), 5 (middle), and 10 (upper) of the cen-

tral transect of each sandy beach. Samples were oven-

dried at 70 �C and passed through a series of sieves

()2.5–4.0 phi) in order of size, to determine the mean

grain size (Folk & Ward 1957). The slope of the beach

face was determined by the height difference (Emery

1961) between the supralittoral and the waterline on the

central transect and expressed in m. The Google Earth�

program was used to determine the distance from the bay

mouth. The beach index (BI) (McLachlan & Dorvlo

2005) was calculated for each beach as a measure of its

morphodynamic state, BI = (mean grain size · tide) ⁄slope. The exposure index proposed by McLachlan (1980)

was used to categorize the beaches in relation to

exposure.

Cardoso, Mattos, Caetano, Cabrini, Galhardo & Meireis Environmental gradients on sandy beach macrofauna

Marine Ecology 33 (2012) 106–116 ª 2011 Blackwell Verlag GmbH 107

Data analysis

Diversity (H¢) and evenness (J¢) were calculated using the

Shannon–Wiener index in loge (Begon et al. 2006) for

each beach, using the total number of individuals per spe-

cies. The relationships between community descriptors

(species richness, diversity, evenness, total abundance, and

biomass), and the physical variables (mean grain size,

slope, beach index, beach length, beach width, and dis-

tance from bay mouth) were modeled by linear or non-

linear fitting procedures, and the model with the best

goodness-of-fit was selected.

A nested ANOVA was used to test significant differ-

ences in the total abundance between islands with more

than one beach studied, and beaches nested within island.

Island was fixed factor with two levels, and beach was a

random factor in the model. This analysis was not real-

ized to main species abundance because it did not fulfill

nested ANOVA assumptions. An one-way ANOVA was

employed to examine differences in the most abundant

(more than 3% of total abundance) and frequent (occur-

ring in more than five beaches) species (Excirolana

armata, Excirolana braziliensis, Atlantorchestoidea brasili-

ensis, Anomalocardia brasiliana, Tellina lineata, Heterodo-

nax bimaculatus, and Cerithium atratum) among beaches,

using each transect as a replicate. Tukey’s honest signifi-

cant difference (HSD) test was used a posteriori to assess

significant differences.

Canonical correspondence analysis (CCA) was per-

formed to explore the relationships among spatial distri-

bution patterns of macrofauna (among beaches) and

environmental factors. CCA was conducted using the

software CANOCO (ter Braak & Smilauer 1998) with

the software options set for forward selection to test the

significance of environmental variables at a level of

P < 0.05. The results of the CCA were drawn on two

biplots: beaches and species were each plotted on a

two-dimensional plot, with the environmental parameters

represented as vectors. For the CCA, we used non-trans-

formed datasets of species abundance (excluding species

with total abundance <1%) and environmental variables

(slope, beach index, exposure rating, beach length and

width, distance between beach and bay mouth, mean

grain size, and silt-clay content) at each beach. There was

no collinearity between the variables analyzed.

Results

Physical characterization

The environmental characterization of the study area is

presented in Table 1. The longest and shortest beach mea-

sured 353 m (Beach 3) and 80 m (Beach 11), respectively.

The widest beach measured 32 m (Beach 12) and the nar-

rowest 11 m (Beach 10). Beach slope ranged from 2.53%

(Beach 1) to 10.53% (Beach 4). Mean grain size varied

from fine (0.12 mm) to coarse (0.97 mm) sands on Pier

(Beach 12) and Escalhau (Beach 7) beaches, respectively.

The beaches of Itacuruca and Jardim islands are located

far from the bay mouth compared to other beaches. The

beach index ranged from 1.29 (Beach 4) to 2.17 (Beach

1). The beaches of Itacuruca, Jardim, and Marambaia

islands are sheltered, whereas beaches located on Bonita

and Jaguanum islands are exposed.

Biological characterization

A total of 7874 macrofaunal organisms were collected,

belonging to 80 taxa, from all the beaches together.

Mollusks were the most abundant macrofaunal group,

Fig. 1. Location map of the 12 beaches

sampling in Sepetiba Bay, also showing the

bay mouth and Atlantic Ocean. 1: Jardim; 2:

Flexeiras; 3: Gamboa; 4: Leste; 5: Boi; 6: Sul;

7: Escalhau; 8: Estopa; 9: Pitangueiras; 10:

Catita; 11: Bonita; 12: Pier.

Environmental gradients on sandy beach macrofauna Cardoso, Mattos, Caetano, Cabrini, Galhardo & Meireis


followed by crustaceans and polychaetes. Other groups

such as cephalochordates, echinoderms, sipunculids, oli-

gochaetes, and insects made only residual contributions

to macrofauna abundance (Fig. 2).

Mollusks were the most abundant animals, represented

mainly by Cerithium atratum (gastropod) and Anomalo-

cardia brasiliana, Heterodonax bimaculatus, Tellina lineata,

and Diplodonta patagonica (bivalves). Crustaceans were

represented mainly by Atlantorchestoidea brasiliensis

(amphipod), Excirolana armata, Excirolana braziliensis

(isopods), and Kalliapseudes schubarti (tanaid). Among

polychaetes, Glycera sp.1 and Scolelepis squamata showed

the highest frequency and abundance. Scolelepis squamata

was most abundant at Pier Beach (Beach 12) (Supporting

information Appendix S1). There was a high frequency of

Excirolana braziliensis, Heterodonax bimaculatus, and

Phaleria testacea, with these species found in 10 of 12

beaches (Appendix S1).

Nested ANOVA indicated significant differences

between islands and beaches nested in islands (Island:

F1,36 = 62.92; P < 0.001; Beaches (Islands): F7,36 = 25.15;

P < 0.001). Total abundance was significantly higher at

Itacuruca Island than at Jaguanum Island. Beaches of

Jaguanum Island did not differ among each other

(Tukey’s HSD; P > 0.05, Fig. 3). However, an inverse

pattern was shown by beaches of Itacuruca Island. Total

abundance was significantly higher at Beach 2 than at

Beach 3, which in turn was higher than at Beaches 4 and

5, which did not differ between each other (Tukey’s HSD;

Fig. 3). Species richness was higher in Boi (Beach 5) and

Gamboa (Beach 3) (Fig. 3a). The highest values of diver-

sity were found in Pitangueiras (Beach 9), Catita (Beach

10), and Boi (Beach 5), while evenness values were high-

est in Pitangueiras (Beach 9), Leste (Beach 4), and Catita

(Beach 10); all these beaches are farther toward the inner

bay (Fig. 3b).

Most of the correlations between physical and biologi-

cal parameters were not significant (P > 0.05). Species

richness did not show significant correlation with physical

parameters. However, diversity and evenness were signifi-

cantly and negatively correlated with slope, BI, and beach

width. Total abundance showed an inverse pattern with

diversity and evenness, being significantly and positively

correlated with slope, BI, and beach width. Evenness also

showed a marginally significant and positive correlation

Table 1. Environmental characterization of the study area, based on variables registered in the 12 beaches located in Sepetiba Bay.

Location Island

beaches

Length

(m)

Width

(m)

Slope

(m)

Grain

size (mm)

Distance

from bay

mouth (km)

Exposure

indexa

Beach

index (BI)

Itacuruca

Boi 95 16 9.8 0.66 (±0.15) 26.5 Sheltered (7) 1.38

Flexeiras 350 25 30.6 0.53 (±0.11) 25.5 Sheltered (8) 1.95

Gamboa 353 19 17.1 0.59 (±0.30) 27.1 Sheltered (7) 1.69

Leste 291 15 9.5 0.79 (±0.20) 28.1 Sheltered (10) 1.29

Jardim

Jardim 180 23 39.6 0.45 (±0.39) 24.6 Sheltered (9) 2.17

Bonita

Bonita 80 11 10.4 0.53 (±0.26) 20.6 Exposed (12) 1.50

Jaguanum

Catita 180 11 7.7 0.59 (±0.07) 17.7 Exposed (11) 1.31

Escalhau 210 20 22.6 0.97 (±0.39) 17.8 Exposed (15) 1.58

Estopa 250 15 11.8 0.50 (±0.49) 19.6 Exposed (12) 1.45

Pitangueiras 140 15 10.1 0.71 (±0.18) 19.8 Exposed (12) 1.37

Sul 200 20 12.5 0.64 (±0.20) 17.4 Exposed (15) 1.50

Marambaia

Pier 130 32 18.7 0.12 (±0.01) 9.6 Sheltered (7) 2.06

aValues in parentheses are derived from the summation of scores (see McLachlan 1980 for details)

0%10%20%30%40%50%60%70%80%90%100%

Jardim

Estopa

Escalhau

Sul

Bonita

Gamboa

Boi

Flexeiras

Leste

Catitia

Pitangueiras

Pier

Abu

ndan

ce (i

nd.m

–2)

Crustacea Mollusca Polychaeta

Fig. 2. Percentage of Crustacea, Mollusca, and Polychaeta abun-

dances in the 12 beaches.



with mean grain size. Biomass was significantly and posi-

tively correlated with beach length (Table 2).

Analysis of variance indicated the existence of signifi-

cant variation in the abundance of the main macrofauna

species among beaches. The abundance of Excirolana

armata was significantly higher (F6,28 = 13.18; P < 0.001)

in Beaches 1 and 11, whereas Atlantorchestoidea brasilien-

sis was significantly higher (F5,24 = 6.24; P < 0.001) in

Beaches 7 and 8. The abundance of Excirolana braziliensis

was significantly higher (F9,40 = 2.14; P < 0.05) in Beach

8. The abundance of A. brasiliana was significantly higher

(F6,28 = 5.63; P < 0.001) for beaches located on Itacuruca

Island (Beaches 2 and 3) than those on Jaguanum

(Tukey’s HSD: P < 0.05). The abundance of Tellina

lineata was significantly higher (F7,32 = 4.54; P < 0.05) in

Beaches 2 and 12, and the abundance of Heterodonax

bimaculatus significantly higher (F9,40 = 30.23; P < 0.001)

in Beach 11. Cerithium atratum was significantly more

abundant (F5,24 = 21.64; P < 0.001) in Beach 2.

Distribution of macrofauna along environmental gradients

Canonical correspondence analysis indicated that of the

eight environmental variables studied, the exposure rating

(F = 2.99; P = 0.002), distance from bay mouth (F =

3.57; P = 0.006), beach length (F = 2.78; P = 0.018), and

beach index (F = 2.34; P = 0.032) were significant, and

the beach width (F = 1.94; P = 0.092) was marginally sig-

nificant. The environmental variables explained 90.26% of

macrofauna data variation among the beaches in CCA.

The first and second axes accounted for 27.6 and 23.0%

of the variance observed in the species data, respectively.

All canonical axes were also assessed as significant using

the Monte Carlo permutation test (F = 3.482; P = 0.004).

On the CCA plot (Fig. 4), beaches located on Jagua-

num, Bonita and Jardim islands were plotted mainly on

the right side, whereas the beaches on Itacuruca and

Marambaia islands were located on the left side or near

the center. These placements indicate that the islands had

different environmental parameters along axis 1 (i.e.

beach index, beach length and width, and exposure rat-

ing). The beach on Marambaia Island was plotted on the

upper part of the plot, suggesting that this beach was dis-

tinguished from the others along axis 2, negatively associ-

ated with the distance from the bay mouth. The CCA

also revealed that beach index and beach length and

width had a strong and positive influence on the mollusks

Cerithium atratum and Anomalocardia brasiliana. The

Fig. 3. Biological descriptors of the 12

beaches studied: (a) total abundance

(indÆm)2) and species richness; (b) diversity

(H¢) and evenness (J¢). Beaches are numbered

following Fig. 1. Note the artificial scale on

the x-axis. Error bars: standard deviation (only

estimated to total abundance).



crustaceans Ruffosius fluminensis, Atlantorchestoidea brasil-

iensis, Excirolana armata, Excirolana braziliensis, and

Sphaeromopsis mourei, as well as the mollusk Heterodonax

bimaculatus and the polychaete Glycera sp.1 responded

positively to the degree of exposure, increasing their

abundances from left to right along the first axis. The

polychaete Scolelepis squamata was associated with Pier

(Beach 12) in the upper part along the second axis.

Discussion

The distribution and abundance patterns of macrofauna

of the beaches of Sepetiba Bay were affected by beach

morphodynamics and exposure degree. Although the

main species occurred in most of the beaches, the rich-

ness and abundance were higher in sheltered beaches

nearest the continent and with the highest silt-clay con-

tent (see results of nested ANOVA). This agrees with the

multicausal environmental severity hypothesis (Brazeiro

2001) that predicts an increase in community descriptors

from harsh reflective (coarse sands, steep slopes) to

benign dissipative (fine sands, gentle slopes) beaches.

Analogously from this hypothesis, we can also associate

sheltered beaches with a benign environment and exposed

beaches with harsh ones. In addition, our results showed

that crustaceans dominated the beaches of Jaguanum and

Bonita islands (near the bay mouth, with steeper slopes

and coarse sand), whereas mollusks were more abundant

in the beaches of Itacuruca Island (farther from the bay

mouth, with fine sands and gentle slopes) (see results of

one-way ANOVA with main species). This pattern is in

agreement with the postulate by Dexter (1983) that

Table 2. Results of linear and nonlinear regression analyses and associated statistics between community descriptors and physical variables.

Variables Model n a b r P

Species richness

Mean grain size (mm) Y = a + bX 12 23.09 )4.11 )0.11 0.74

Slope (1 m)1) Y = a + bX 12 19.09 )0.11 )0.08 0.66

BI Y = a + bX 12 19.12 0.97 0.04 0.91

Beach length (m) Y = a + bX 12 20.02 0.003 0.04 0.91

Beach width (m) Y = a + bX 12 18.69 0.11 0.08 0.66

Distance from bay mouth (km) Y = a + bX 12 9.68 0.52 0.35 0.26

Diversity (H¢)Mean grain size (mm) Y = a + bX 12 0.97 1.45 0.46 0.1354

Slope (1 m)1) Y = aXb 12 25.56 )1.05 )0.84 0.000004

BI Y = aebX 12 11.28 )1.18 )0.85 0.0386

Beach length (m) Y = a + bX 12 2.28 )0.002 )0.31 0.3268

Beach width (m) Y = a + bX 12 2.98 )0.06 )0.56 0.0432


Evenness

Mean grain size (mm) Y = a + bX 12 0.29 0.54 0.55 0.0673

Slope (1 m)1) Y = aXb 12 7.69 )1.19 )0.88 0.000000

BI Y = aebX 12 4.00 )1.20 )0.94 0.000012

Beach length (m) Y = a + bX 12 0.73 )0.0006 )0.26 0.4233

Beach width (m) Y = a + bX 12 1.02 )0.02 )0.64 0.0256


Total abundancea

Mean grain size (mm) Y = a + bX 12 3.15 )0.85 )0.42 0.1839

Slope (1 m)1) Y = aebX 12 2.31 0.69 0.57 0.0481

BI Y = aXb 12 2.00 0.58 0.65 0.0325

Beach length (m) Y = a + bX 12 2.45 0.001 0.21 0.5012

Beach width (m) Y = a + bX 12 2.01 0.03 0.50 0.0969


Total biomass

Mean grain size (mm) Y = a + bX 12 24.76 )13.62 0.07 0.8215

Slope (1 m)1) Y = a + bX 12 56.38 )5.22 0.44 0.1511

BI Y = a + bX 12 )57.48 46.26 0.36 0.2519

Beach length (m) Y = a + bX 12 )39.96 0.28 0.65 0.0242

Beach width (m) Y = a + bX 12 )22.20 2.11 0.33 0.3014

Distance from bay mouth (km) Y = a + bX 12 )45.77 2.95 0.41 0.1865

aTotal abundance were transformed to log(x). Significant values are highlighted in bold.



changes in the contributions of the main taxonomic

groups are also expected along the wave exposure gradi-

ent. Usually crustaceans are dominant organisms on

exposed beaches, being more generalist and adapted to

live on harsh reflective beaches. In contrast, polychaetes

and deposit-feeder mollusks are specialists, and may be

delicate forms and ⁄ or slow burrowers, tending to domi-

nate benign environments such as sheltered beaches,

ultradissipative beaches, and tidal flats. In these environ-

ments, the variations of physical factors are more limited

(Dexter 1983; McLachlan & Brown 2006). Conversely to

the beach exposure gradient, Pier Beach (Beach 12),

located on Marambaia Island, showed similar characteris-

tics to those found in the Itacuruca Island beaches, in

spite of being near the bay mouth, possibly because of

the protection provided by the pier located at the far end

of the beach. This pier creates depositional conditions on

one side of the structure, while causing some erosion on

the opposite side according to the direction of currents

and tide (Nordstrom 2000).

The occurrence of the main species among beaches

and the spatial variations in abundance of these species

respond to local features of the beaches studied. These

species differ in sediment needs and niche requirements.

This allows the development of a mosaic in the spatial

distribution of macrofauna among beaches on islands of

Sepetiba Bay, where these beaches have a set of environ-

mental variables that reflect the morphodynamic and

exposure gradients. Recent studies on sandy beaches

were directed to address the interaction between mor-

phodynamics (e.g. swash features, mean grain size, and

wave height) and estuarine (e.g. salinity) gradients in

aggregate population descriptors of macrofauna, such as

abundance, biomass, recruitment, and body size (Celent-

ano et al. 2010; Lozoya et al. 2010). Lozoya et al. (2010)

observed higher abundances of the isopod Excirolana

armata for high salinities and intermediate ⁄ dissipative

beaches with fine sands (<0.20 mm) and low organic

matter (<0.1%). The higher abundance of this species in

beaches with fine sands is explained by its behavior,

since this isopod is highly substrate-specific, as also

reflected in its range distribution (Defeo et al. 1997;

Veloso & Cardoso 2001; Cardoso & Defeo 2004;

Thompson & Sanchez de Bock 2007). Celentano et al.

(2010) showed that salinity, mean grain size, and swash

width were the most important factors affecting spatio-

temporal variations in abundance of the mole crab

Emerita brasiliensis, and that its abundance and biomass

increased from reflective to dissipative beaches and from

estuarine to oceanic ones.

Canonical correspondence analysis (Fig. 4) indicates

that environmental parameters such as beach index, expo-

sure rating, beach length and width, and distance from

the beach to the bay mouth are the most important fac-

tors, explaining more than 90% of the variability in the

macrofauna. In general terms, there is a positive correla-

tion between macrofauna abundance of beaches of

Itacuruca Island and increases in the beach index, dis-

tance from the beach to the bay mouth, and beach length

a

b

Fig. 4. Canonical correspondence analysis biplots: (a) beaches scores

and (b) species scores. Arrows indicate environmental variables. Spe-

cies represented in plot (b): Cer (Cerithium atratum), Ano (Anomalo-

cardia brasiliana), T.lin (Tellina lineata), Dip (Diplodonta patagonica),

Het (Heterodonax bimaculatus), Tyl (Tylos niveus), Kal (Kalliapseudes

schubarti), Sph (Sphaeromopsis mourei), Pag (Pagurus criniticornis),

Ruf (Ruffosius fluminensis), E.arm (Excirolana armata), E.bra (Excirol-

ana braziliensis), Atl (Atlantorchestoidea brasiliensis), Gly (Glycera

sp.1), Sco (Scolelepis squamata), Pha (Phaleria testacea).



and width. A decrease in beach length together with more

exposed conditions (steeper slope and coarse sand) seem

to positively affect crustacean species such as Excirolana

braziliensis, Excirolana armata, and Atlantorchestoidea bra-

siliensis. However, E. braziliensis and A. brasiliensis were

more abundant in beaches of Jaguanum Island nearer the

mouth of the bay, and E. armata was more abundant in

beaches of Bonita (located behind Jaguanum Island) and

Jardim Island (which is nearer the continent than Ita-

curuca Island). These two beaches have finer sand than

the beaches of Jaguanum Island. Defeo et al. (1997) sug-

gested that E. armata is a highly substratum-specific spe-

cies (fine sands) and capable of displacing E. braziliensis

when in sympatry. The abundances of mollusks (Cerithium

atratum, Anomalocardia brasiliana, and Tellina lineata),

which were found mainly in beaches of Itacuruca Island,

were well explained by long beach length and high silt-clay

content. The higher silt-clay content is a consequence of

proximity to the continent and the high fluvial input to

this region. These morphological characteristics are typical

of benign environments with sedimentary stability, such as

the more sheltered beaches. However, Heterodonax bima-

culatus was more abundant at beaches of Jaguanum and

Bonita islands. It is evident that differences in community

composition were more pronounced between islands than

between different beaches on the same island. Deidun &

Schembri (2008a) suggested that the inter-island obstacles

to macrofaunal recruitment and dispersal are more impor-

tant than the inter-beach ones.

Community descriptors of macrofauna responded to

morphodynamic and exposure gradients. Increases in spe-

cies richness and abundance, from harsh reflective (coarse

sands, steep slopes) to benign dissipative (fine sands, gen-

tle slopes) beaches, and from the bay mouth (exposed

beaches) towards the inner bay (sheltered beaches) were

observed. In an unexpected way, diversity and evenness

showed a different pattern. Diversity and evenness

increased from benign to harsh environments (Table 2).

We suggested that benign and more stable environments

present higher species richness (‘number of species’),

among which there is a prevalence of some species that

correspond to the greatest part of total macrofaunal

abundance dominating the resources available, resulting

in a lower diversity and evenness. In harsh and more

dynamic environments, the species richness is lower and

the contribution of dominant species lower than the total

abundance of macrofauna, as that the resource is shared

by a smaller number of species, consequently increasing

the diversity and evenness. According to the CCA and

regression analyses, differences in macrofauna composi-

tion among the beaches studied are associated with beach

length and beach width. In this sense, spatial variation of

macrofauna can be a function of intertidal area. Recently,

McLachlan & Dorvlo (2007) observed an increase of spe-

cies richness in wider beaches. Brazeiro (1999) postulated

that for pocket beaches the number of species may

increase with beach length, with short and pocket beaches

supporting fewer species than longer ones, although the

relationship between beach length and total species num-

ber is not obvious and may be non-linear and scale-

dependent.

Our results showed that there were higher abundances

of supralittoral species such as the amphipod Atlantor-

chestoidea brasiliensis (r = 0.73; P = 0.10) on shorter

beaches. A similar pattern was observed by Rodil et al.

(2006), who associated beach length with macrofauna

zonation, suggesting that different macrofaunal species

exhibit different responses to increasing beach length.

Whereas species found in the higher beach levels showed

higher densities on shorter beaches (e.g. the polychaete

Ophelia bicornis and the amphipod Talorchestia brito),

most species of the lower beach (e.g. the amphipod

Bathyporeia pelagica, the bivalve Donax trunculus, and

the cumacean Cumopsis fagei) showed an opposite trend.

Our results also showed that a shorter beach was associ-

ated with lower beach index values (r = 0.82; P < 0.01),

which supports the suggestion of McLachlan et al.

(1993) that in fully reflective beaches the harsh swash

climate excludes the establishment of intertidal macrofa-

unal species. This would explain the observed higher

densities of supralittoral species in beaches with reflec-

tive conditions.

Higher biomass was observed in longer beaches. We

also observed that longer beaches were associated with

higher beach indexes, so indirectly we can suggest that

higher biomasses are associated with dissipative ⁄ sheltered

beaches, categorized as a semi-closed ecosystem with

high primary productivity provided by the huge

amounts of diatoms living in the surface zone. Lastra

et al. (2006) suggested that the lower macrofaunal bio-

mass in pocket beaches is associated with the effect of

headlands on the water circulation of small beaches.

This effect increases the rip-current velocity and beach

erosion, thus affecting seaward transport of beach sedi-

ments, nutrients, and organisms (Donn 1987; Short

1996; Brazeiro 1999). This reduced or absent inter-beach

transport induced Deidun & Schembri (2008a) to con-

sider pocket beaches as ecological islands: in the Maltese

Islands where they conducted their study, the lack of

along-shore currents between the beaches and the pau-

city of sandy coastlines results in the few sandy beaches

being separated by long stretches of non-sandy coastline.

This also can presumably hinder inter-beach biotic

recruitment. Such a lack of recruitment to beaches of

smaller length is especially significant when considering

the effect of stochastic events, including severe storms,



and of human disturbance, which might extirpate partic-

ular species from a beach (Deidun & Schembri 2008b).

This confirms the ‘source–sink hypothesis’ for intertidal

sandy beach populations (Defeo & McLachlan 2005),

where sink and source habitats could be explained by

the difference between the reflective and dissipative

extremes of the morphodynamic gradient. We can sug-

gest criteria for identifying source and sink habitats,

mainly that specialist species such as the bivalve Anom-

alocardia brasiliana reach high abundances in some

longer beaches of Itacuruca Island (source habitat) but

do not maintain a population in the shorter beaches of

Bonita and Jaguanum islands (sink habitat). The inverse

pattern is observed for Heterodonax bimaculatus, which

is more abundant in Bonita Beach (Bonita Island) than

in beaches of Itacuruca Island. Thus, our results also

support recent findings that life-history traits (larval or

ovoviviparous) of intertidal species affect macrofauna

composition. Species that reproduce by larvae tend to

expand in response to currents (i.e. the bivalves Anom-

alocardia brasiliana, Heterodonax bimaculata, Tellina line-

ata), whereas ovoviviparous species (i.e. the cirolanid

Excirolana braziliensis) only expand the conditions in

which plasticity is favored, in order to optimize fitness

(Kingsolver et al. 2002). Our future studies will address

these questions.

In summary, the wave exposure gradient shapes the

large-scale spatial distribution of macrofaunal sandy

beach communities of the inner part of Sepetiba Bay: the

species richness and total abundance markedly increased

in the inner bay, where the wave action was minimal.

Sediment variables (e.g. silt-clay content), the distance

from the bay mouth, and the length and width of the

beaches had a stronger influence on community descrip-

tors, even though wave exposure variability also signifi-

cantly explained spatial variations in these descriptors.

Thus, the geographical position of beaches can be consid-

ered an aggregate factor that has different, simultaneous

effects on the macrofauna community. These observations

provide additional support for the perception that sandy

beach macrofauna seems to be controlled by the interac-

tion between different factors operating together.

Acknowledgements

The authors express their deepest gratitude to Dr. Luzia

A.F. Moraes (UNIRIO) for map creation, and Dr. Janet

W. Reid for English language revision. Thanks are also

due to Dr. Omar Defeo (UNDECIMAR), Dr. Mariano

Lastra (Universidad de Vigo) and Dr. Mick Keough

(University of Melbourne) for providing useful comments

on the paper. R.S. Cardoso was supported by the CNPq

(Conselho Nacional de Desenvolvimento Cientifico e

Tecnologico), FAPERJ (Fundacao de Amparo a Pesquisa

do Estado do Rio de Janeiro) and CT-Infra (Fundo

Setorial de Infra-Estrutura) by MCT ⁄ CNPq (nO. E-26 ⁄171.164 ⁄ 2006).

References

Amaral A.C.Z., Denadai M.R., Turra A., Rizzo A.E. (2003)

Intertidal macrofauna in Brazilian subtropical sandy beach

landscapes. Journal of Coastal Research, 35, 446–455.

Arruda E.P., Amaral A.C.Z. (2003) Spatial distribution of mol-

lusks in the intertidal zone of sheltered beaches in southeast-

ern of Brazil. Revista Brasileira de Zoologia, 20, 291–300.

Azevedo M.C.C., Araujo F.G., Cruz-Filho A.G., Pessanha

A.L.M., Silva M.A., Guedes A.P.P. (2007) Demersal fishes in

a tropical bay in southeastern Brazil: partitioning the spatial,

temporal and environmental components of ecological vari-

ation. Estuarine, Coastal and Shelf Science, 75, 468–480.

Begon M., Townsend C.R., Harper J.L. (2006) Ecology: From

Individuals to Ecosystems. Blackwell Publishing, Hong Kong:

740 pp.

ter Braak C.J.F., Smilauer P. (1998) CANOCO Reference Man-

ual and User’s Guide to Canoco for Windows: Software for

Canonical Community Ordination (Version 4). Microcom-

puter Power, Ithaca, NY: 351 pp.

Brazeiro A. (1999) Community patterns in sandy beaches of

Chile: richness, composition, distribution and abundance of

species. Revista Chilena de Historia Natural, 72, 93–105.

Brazeiro A. (2001) Relationship between species richness and

morphodynamics in sandy beaches: what are the underlying

factors? Marine Ecology Progress Series, 224, 35–44.

Brown J.H. (1984) On the relationship between abundance

and distribution of species. The American Naturalist, 124,

255–279.

Cardoso R.S., Defeo O. (2003) Geographical patterns in repro-

ductive biology of the Pan-American sandy beach isopod

Excirolana braziliensis. Marine Biology, 143, 573–581.

Cardoso R.S., Defeo O. (2004) Biogeographic patterns in life

history traits of the Pan-American sandy beach isopod Exci-

rolana braziliensis. Estuarine, Coastal and Shelf Science, 61,

559–568.

Celentano E., Gutierrez N.L., Defeo O. (2010) Effects of mor-

phodynamic and estuarine gradients on the demography

and distribution of a sandy beach mole crab: implications

for source-sink habitat dynamics. Marine Ecology Progress

Series, 398, 1–18.

Defeo O., Cardoso R. (2002) Macroecology of population

dynamics and life history traits of the mole crab Emerita

brasiliensis in Atlantic sandy beaches of South America.

Marine Ecology Progress Series, 239, 169–179.

Defeo O., Cardoso R. (2004) Latitudinal patterns in abundance

and life-history traits of the mole crab Emerita brasiliensis

on South American sandy beaches. Diversity and Distribu-

tions, 10, 89–98.



Defeo O., McLachlan A. (2005) Patterns, processes and

regulatory mechanisms in sandy beach macrofauna: a

multi-scale analysis. Marine Ecology Progress Series, 295,

1–20.

Defeo O., Rueda M. (2002) Spatial structure, sampling design

and abundance estimates in sandy beach macroinfauna:

some warnings and new perspectives. Marine Biology, 140,

1215–1225.

Defeo O., Jaramillo E., Lyonnet A. (1992) Community struc-

ture and intertidal zonation of the macroinfauna on the

Atlantic Coast of Uruguay. Journal of Coastal Research, 8,

830–883.

Defeo O., Brazeiro A., de Alava A., Riestra G. (1997) Is sandy

beach macrofauna only physically controlled? Role of sub-

strate and competition in isopods Estuarine, Coastal and

Shelf Science, 45, 453–462.

Deidun A., Schembri P.J. (2008a) Long or short? Investigating

the effect of beach length and other environmental parameters

on macrofaunal assemblages of Maltese pocket beaches.

Estuarine, Coastal and Shelf Science, 79, 17–23.

Deidun A., Schembri P.J. (2008b) Assessing inter-beach differ-

ences in semi-terrestrial arthropod assemblages on Maltese

pocket sandy beaches (Central Mediterranean). Marine Ecol-

ogy, 29 (Suppl. 1), 108–117.

Denadai M.R., Amaral A.C.Z., Turra A. (2005) Structure of

molluscan assemblages in sheltered intertidal unconsolidated

environments. Brazilian Archives of Biology and Technology,

48, 825–839.

Dexter D.M. (1983) Community structure of intertidal sandy

beaches in New South Wales, Australia. In: McLachlan A.,

Erasmus T. (Eds), Sandy Beaches as Ecosystems. Junk, The

Hague: 461–472.

Dexter D.M. (1992) Sandy beach community structure: the

role of exposure and latitude. Journal of Biogeography, 19,

59–66.

Diamond J., Case T.J. (1986) Overview: introductions, extinc-

tions, exterminations, and invasions. In: Diamond J., Case

T.J. (Eds), Community Ecology. Harper & Row, New York:

65–79.

Donn J.E. (1987) Longshore distribution of Donax serra in two

log spiral bays in the Eastern Cape, South Africa. Marine

Ecology Progress Series, 35, 217–222.

Emery K.O. (1961) A simple method of measuring beach

profiles. Limnology and Oceanography, 6, 90–93.

Folk R.L., Ward W.C. (1957) Brazos River bar, a study in

significance of grain size parameters. Journal of Sedimentary

Petrology, 27, 3–26.

Haynes D., Quinn G.P. (1995) Temporal and spatial variability

in community structure of a sandy intertidal beach, Cape

Paterson, Victoria, Australia. Marine and Freshwater

Research, 46, 931–942.

Jaramillo E., Gonzalez M. (1991) Community structure and

zonation of the macroinfauna along a dissipative-reflective

range of beach category in southern Chile. Studies on Neo-

tropical Fauna and Environment, 26, 193–212.

Jaramillo E., McLachlan A. (1993) Community and population

responses of the macroinfauna to physical factors over a

range of exposed sandy beaches in south-central Chile. Estu-

arine, Coastal and Shelf Science, 37, 615–624.

Jaramillo E., McLachlan A., Coetzee P. (1993) Intertidal zona-

tion patterns of macroinfauna over a range of exposed sandy

beaches. Marine Ecology Progress Series, 101, 105–118.

Kingsolver J.G., Pfenning D.W., Servedio M.R. (2002) Migra-

tion, local adaptation and the evolution of plasticity. Trends

in Ecology and Evolution, 17, 540–541.

Lastra M., de La Huz R., Sanchez-Mata A.G., Rodil I.F., Aerts

K., Beloso S., Lopez J. (2006) Ecology of exposed sandy

beaches in northern Spain: environmental factors controlling

macrofauna communities. Journal of Sea Research, 55,

128–140.

Lercari D., Defeo O. (2006) Large-scale diversity and abun-

dance trends in sandy beach macrofauna along full gradients

of salinity and morphodynamics. Estuarine, Coastal and


Lozoya J.P., Gomez J., Defeo O. (2010) Modelling large-scale

effects of estuarine and morphodynamic gradients on distri-

bution and abundance of the sandy beach isopod Excirolana

armata. Estuarine, Coastal and Shelf Science, 87, 472–478.

McLachlan A. (1980) The definition of sandy beaches in rela-

tion to exposure: simple rating system. South African Journal

of Science, 76, 137–138.

McLachlan A. (1990) Dissipative beaches and macrofauna

communities on exposed intertidal sands. Journal of Coastal

Research, 6, 57–71.

McLachlan A. (2001) Coastal beach ecosystems. In: Lewin R.

(Ed.), Encyclopedia of Biodiversity. Academic Press, New

York: 741–751.

McLachlan A., Brown A.C. (2006) The Ecology of Sandy Shores.

Elsevier, Amsterdam: 373 pp.

McLachlan A., Dorvlo A. (2005) Global patterns in sandy

beach macrobenthic communities. Journal of Coastal

Research, 21, 674–687.

McLachlan A., Dorvlo A. (2007) Global patterns in sandy

beach macrobenthic communities: biological factors. Journal

of Coastal Research, 23, 1081–1087.

McLachlan A., Jaramillo E., Donn T.E., Wessels F. (1993)

Sandy beach macrofauna communities and their control by

the physical environment: a geographical comparison. Jour-

nal of Coastal Research (Special Issue), 15, 27–38.

Nordstrom K.F. (2000) Beaches and Dunes on Developed

Coasts. Cambridge University Press, Cambridge: 338 pp.

Patterson B.D., Atmar W. (1986) Nested subsets and the struc-

ture of insular mammalian faunas and archipelagos. Biologi-

cal Journal of the Linnean Society, 28, 65–82.

Pessanha A.L.M., Araujo F.G. (2003) Spatial, temporal and diel

variations of fish assemblages at two sandy beaches in the

Sepetiba Bay, Rio de Janeiro, Brazil. Estuarine, Coastal and


Preston F.W. (1962) The canonical distribution of common-

ness and rarity: part II. Ecology, 43, 410–432.



Ricciardi A., Bourget E. (1999) Global patterns of macroinver-

tebrate biomass in marine intertidal communities. Marine

Ecology Progress Series, 185, 21–35.

Ricklefs R.E., Schluter D. (1993) Species diversity: regional and

historical influences. In: Ricklefs R.E., Schluter D. (Eds),

Species Diversity in Ecological Communities. Historical and

Geographical Perspectives. The University of Chicago Press,

Chicago: 350–364.

Rodil I.F., Lastra M., Sanchez-Mata A.G. (2006) Community

structure and intertidal zonation of the macroinfauna in

intermediate sandy beaches in temperate latitudes: north

coast of Spain. Estuarine, Coastal and Shelf Science, 67,

267–279.

Rosa R.C. (2009) As praias estuarinas da Baıa de Paranagua

(regiao sul do Brasil): aspectos morfodinamicos e ecologicos.

Ph.D. thesis, Universidade Federal do Rio Grande, Brazil.

Short A.D. (1996) The role of wave height, period, slope, tide

range and embaymentisation in beach classifications: a

review. Revista Chilena de Historia Natural, 69, 589–604.

Soares A.G. (2003) Sandy beach morphodynamics and macro-

benthic communities in temperate, subtropical and tropical

regions – a macroecological approach. Ph.D. thesis, University

of Port Elizabeth, South Africa.

Thompson G.A., Sanchez de Bock M. (2007) Population

dynamics of Excirolana armata (Isopoda: Cirolanidae) in

Buenos Aires beaches, Argentina. Revista de Biologıa Tropi-

cal, 55, 131–140.

Underwood A.J., Petraitis P.S. (1993) Structure of intertidal

assemblages in different locations: how can local processes be

compared? In: Ricklefs R.E., Schluter D. (Eds), Species Diver-

sity in Ecological Communities. Historical and Geographical

Perspectives. The University of Chicago Press, Chicago: 39–51.

Veloso V.G., Cardoso R.S. (2001) The effects of morphody-

namics on the spatial and temporal variation of the macro-

fauna of three sandy beaches on the Rio de Janeiro State,

Brazil. Journal of the Marine Biological Association of the

United Kingdom, 81, 369–375.

Veloso V.G., Caetano C.H.S., Cardoso R.S. (2003) Composition,

structure and zonation of intertidal macroinfauna in relation

to physical factors in microtidal sandy beaches at Rio de

Janeiro State, Brazil. Scientia Marina, 67, 393–402.

Supporting Information

Additional Supporting Information may be found in the

online version of this article:

Appendix S1 Abundance (indÆm)2) of macrofauna at

12 beaches located in Sepetiba Bay.

Please note: Blackwell Publishing are not responsible

for the content or functionality of any supporting materi-

als supplied by the authors. Any queries (other than miss-

ing material) should be directed to the corresponding

author for the article.



Effects of environmental gradients on sandy beach macrofauna of a semi-enclosed bay

Documents

Transcript of Effects of environmental gradients on sandy beach macrofauna of a semi-enclosed bay