PRIMARY RESEARCH PAPER

Spatial variability of the infauna adjacent to intertidal rockyshores in a subtropical estuary

Joao B. L. Gusmao-Junior • Paulo C. Lana

Received: 10 December 2013 / Revised: 3 July 2014 / Accepted: 30 July 2014

� Springer International Publishing Switzerland 2014

Abstract Negative responses of infauna close to

rocky substrates are well known to subtidal bottoms,

but there are few studies addressing similar intertidal

habitats. We tested the hypothesis that the proximity to

rocky shores negatively affects the density and

richness of intertidal infauna of tidal flats by assessing

infaunal variation across the increasing distances from

rocky shores in two tidal flats (Pasto and Limoeiro) of

a subtropical estuary in southern Brazil. Total density

decreased significantly with the proximity to rocks

only in Pasto due to density variations in the two

numerically dominant species, the bivalve Anomalo-

cardia flexuosa and the polychaete Armandia hoss-

feldi. Richness decreased significantly with the

proximity to the rocky shores only in Limoeiro.

Multivariate analyses revealed significant differences

in species and functional groups composition between

assemblages near and far from the rocky shores.

Assemblage variability patterns were mostly

explained by sediment variables. Our hypothesis was

partially refuted because negative effects on the

infauna were spatially inconsistent, due to differences

in species composition between tidal flats, and to

distinct responses of individual taxa. Even with the

absence of consistent response patterns, the proximity

to the rocky shores emerged as a relevant structuring

factor of the surrounding intertidal infauna.

Keywords Macrofauna � Tidal flat � Soft sediments �Infauna � Rocky shores

Introduction

Ecological boundaries between different ecological

systems are common features in heterogeneous land-

and seascapes. These boundaries are frequently related

to contrasts that are reflected in steep environmental

gradients at the interface between different ecosys-

tems (Gosz, 1993; Strayer et al., 2003; Farina, 2010;

Erdos et al., 2011). The extension and amplitude of

these gradients can affect species distributions across

the boundaries (Attrill & Rundle, 2002; Strayer et al.,

2003). However, responses to the boundaries vary

among species. Most species are relatively neutral and

display no abundance variation across the boundaries

(Barros et al., 2001; Dangerfield et al., 2003). How-

ever, population densities may also increase or

decrease along the boundary extension (Summerson

& Peterson, 1984; Kim, 1992; Posey & Ambrose Jr.,

1994; Dangerfield et al., 2003).

Handling editor: Stuart Jenkins

Electronic supplementary material The online version ofthis article (doi:10.1007/s10750-014-2004-4) contains supple-mentary material, which is available to authorized users.

J. B. L. Gusmao-Junior (&) � P. C. Lana

Centro de Estudos do Mar, Universidade Federal do

Parana, Pontal do Parana, Parana 83255-976, Brazil

e-mail: gusmao.jb@gmail.com

123

Hydrobiologia

DOI 10.1007/s10750-014-2004-4

Studies addressing the effects of boundaries on

species distribution provide information on the inter-

action between different ecosystems, such as energy

and matter transport (Strayer et al., 2003; Kruitwagen

et al., 2010), and interspecific interactions (Summer-

son & Peterson, 1984; Langlois et al., 2005, 2006a, b).

The assessment of ecological boundaries can also

provide relevant information for environmental man-

agement, to maintain habitat heterogeneity for biodi-

versity conservation (Hewitt et al., 2005), analysis on

the impact of land- and seascape changes in local and

regional communities (Bostrom et al., 2011), and to

establish the extent of buffer zones in protected areas

(Alexandre et al., 2010).

The contact zone between different substrates

represents a boundary between habitat types in marine

benthic environments. A notable example is the

boundary between hard and soft substrates, such as

reefs and surrounding soft sediments. The presence of

hard substrates tends to affect the surrounding sedi-

ments due to changes in the physical and biological

factors which regulate the adjacent infauna (Ogden

et al., 1973; Kim, 1992; Posey & Ambrose Jr., 1994;

Barros et al., 2001). Hard substrates can affect the

local hydrodynamics by modifying the sedimentation

patterns and the adjacent sediment characteristics

(Davis et al., 1982; Nowell & Jumars, 1984; Cusson &

Bourget, 1997). Hard substrates can also affect the

adjacent infauna by intensifying or reducing biolog-

ical interactions. Small predators and herbivores that

use hard substrates as a refuge can forage on the

surrounding soft substrates, feeding on the associated

plants and animals (Langlois et al., 2005, 2006a, b).

This foraging activity is possibly associated with the

formation of ‘haloes’ in the surrounding sediments,

i.e. zones of reduced organismal abundance and

diversity in the vicinity of hard substrates (Ogden

et al., 1973; Posey & Ambrose Jr., 1994; Sweatman &

Robertson, 1994). The bioturbation activities of some

large animals can also affect the infaunal assemblages

adjacent to hard substrates (Dahlgren et al., 1999).

However, there are situations where the ecological

interactions alone do not explain the observed patterns

in infaunal distribution in such boundaries (Kim,

1992; Barros, 2005).

The influence of hard substrates on the infaunal

assemblage structure has been mostly assessed for

subtidal bottoms (Posey et al., 1992; Barros et al.,

2001; Langlois et al., 2006a; Galvan et al., 2008). In

contrast, studies focusing on the same topic in intertidal

environments are rare (Cusson & Bourget, 1997;

Guichard & Bourget, 1998; Kelaher et al.,

1998). Intertidal ecosystems are exposed to different

physical stress sources during tide variation, such as

flow variability and desiccation (Raffaelli & Hawkins,

1999). Moreover, the associated organisms can also be

affected by the alternating foraging activity of aquatic

and terrestrial organisms during high and low tide

(Wilson, 1991; Morrison et al., 2002). These physical

and biological factors coupled with the proximity of an

entirely different ecosystem such as rocky shores could

promote or intensify any negative effects on the

infaunal assemblages of tidal flats. In this study, we

have assessed the distributional patterns of infaunal

assemblages along the boundary between rocky shores

and tidal flats. Since negative infaunal responses to the

proximity of reefs or hard bottoms are a recurring

pattern in subtidal environments, we predict that

similar responses will be expected in intertidal envi-

ronments. We hypothesized that the proximity to hard

substrates negatively affects infaunal abundance,

richness and diversity in intertidal flats. To test this

hypothesis, we have assessed variations in infaunal

structure according to their distance from rocky shores

in two subtropical tidal flats of the Paranagua Estuarine

Complex (PEC), Brazil, in the south-western Atlantic.

Methods

Study area

Sampling was carried out on two tidal flats bordered

by rocky shores in the PEC: the inlet of the Pasto

Beach in the Laranjeiras Bay (25�24.5840S;

48�25.1070W) and Saco do Limoeiro in the Ilha do

Mel Island (25�33.6150S; 48�18.9610W) (subsequently

referred to as Pasto and Limoeiro, respectively). The

tides of the PEC have a semidiurnal pattern with

diurnal inequalities, and maximum amplitudes vary-

ing between 1.7 m in the outer and 2.7 m in the inner

sector of the bay (Marone & Jamiyanaa, 1997). The

rocky shores of both tidal flats are discontinuous and

approximately perpendicular to the shoreline, and

bivalves and balanid barnacles are the main fouling

animals (Fig. 1).

Pasto is located in the innermost area of the

euhaline sector of the PEC, at the entrance of the

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123

Laranjeiras Bay. The tidal amplitude is approximately

2 m. Declivity is low (maximum 1.3%), and the

sediments are dominated by highly to moderately

selected fine sand (Rosa & Borzone, 2008). Dense

shell deposits of the bivalve Anomalocardia flexuosa

Linnaeus, 1767 (=Anomalocardia brasiliana Gmelin,

1791) increase the complexity of sediment texture,

mainly near the rocky shores.

The Ilha do Mel Island is located at the mouth of the

PEC. It is under oceanic influence at its most easterly

part, and the tidal amplitude is less than 2 m. Tidal

flats’ declivity is also low (maximum 0.6%), with

sediments ranging from highly to poorly selected, and

dominated by fine and very fine sand (Couto et al.,

1995; Couto & Savian, 1998). The structure of the

benthic macrofauna is primarily influenced by numer-

ically dominant species such as the tanaidacean

crustacean Monok alliapseudes schubarti Mane-Gar-

zon, 1949, dense patches of the rhodophyte algae

Acanthophora spicifera (M.Vahl) Børgesen, 1910 and

empty valves of A. flexuosa, which increases sediment

heterogeneity (Couto et al., 1995; Couto & Savian,

1998).

Sampling and laboratory procedures

Samples were collected in November 2011, corre-

sponding to the end of the austral spring. Two

30 m 9 30 m areas separated by a distance of

100 m were delimited alongside the rocky shores in

each tidal flat. At each area, three transects perpen-

dicular to the rocks and 10 m from each other were

established. When establishing transects, we avoided

tide pools and points with abrupt declivity changes.

Along each transect, six sampling points at increasing

distances from the rocky shores were defined: D1 at

approximately 10 cm, D2 at 1 m, D3 at 2 m, D4 at

4 m, D5 at 8 m and D6 at 16 m. Three infaunal

samples were collected at each point, using a corer

15 cm in diameter and 10 cm in height. The samples

were taken to the laboratory, washed through a

0.5-mm sieve, fixed in 7% formalin, stained with

Rose Bengal and preserved in 70% ethanol. A sample

of about 150 g of sediment was collected at each point

to determine sediment texture, carbonate and organic

matter contents. Dry weight of shells, macro-debris of

plants and pebbles was estimated from sediment

subsamples.

Organisms were identified to species whenever

possible, under a stereomicroscope. Infauna was

further classified into functional groups, taking into

account locomotion strategies (M, motile; D, dis-

cretely motile; S, sessile) and feeding habits (Car,

carnivore; Her, herbivore; Omn, omnivore; Fil, sus-

pensivore; Sur, surface deposit feeder; Bur, subsurface

deposit feeder; Ind, indeterminate). This classification

was based on the primary literature (e.g. Fauchald &

Jumars, 1979; Arruda et al., 2003; Pagliosa et al.,

2012).

Sediment analysis was conducted with a particle

size analyser Microtrac Bluewave�. Organic matter

content was determined by weight variation, after

burning 5 g of sediment at 550�C for 60 min.

Carbonate content was estimated by weight variation

after acidification of 10 g of sediment in 20 ml of 10%

HCl.

Data processing

Trends in the variability of environmental parameters

were analysed using principal component analysis

(PCA). These included carbonate and organic matter

content (percentage), dry weight (g) of pebbles, shells

and plant macro-debris, sorting coefficient and sand

Fig. 1 Images of Pasto

(a) and Limoeiro (b) tidal

flats, showing the contact

areas between rocky shores

and unconsolidated bottoms

Hydrobiologia

123

and mud percentages. The results discriminated tidal

flats, areas and distances.

Analysis of variance (ANOVA) was used to test for

significant differences among the average values of the

total density of individuals, richness (S) and density of

numerically dominant taxa and functional groups. The

normality of data was assessed by the Shapiro–Wilk

test and the heterogeneity of variances by the Cochran

test (a = 0.05). Data were transformed (square root,

fourth root or log) when necessary. The factors

considered were Area (random, two levels) and

Distance (fixed, six levels, orthogonal to area). Tran-

sects were used only to demark the sampling points

along the distances from the rocky shores. Thus, for

each area, samples of a same distance were pooled

together (i.e. summing nine replicates for each dis-

tance). Pairwise comparisons a posteriori were made

using the Student-Newman–Keuls test (a = 0.05).

Differences between infaunal assemblages, factor-

ing in taxonomic and functional groups, were tested by

permutational multivariate analysis of variance (PER-

MANOVA), using the software PERMANOVA 1.6

(Anderson, 2005). The data were square-root trans-

formed. Comparisons were made between tidal flats

using the two-factor model of univariate analyses

(a = 0.05). Trends in variation of assemblages were

visualized in non-metric multidimensional scaling

ordinations (nMDS).

To analyse the variability of infaunal assemblage

composition within each level of distance, we per-

formed a permutational analysis of multivariate dis-

persions (PERMDISP) with the software PERMDISP

(Anderson, 2004). In this analysis, the mean distances

of multivariate dispersions in relation to the centroid

of the cluster were compared using ANOVA, in which

the P value was estimated by permutations. The model

applied was the same as the two factors from the

univariate analyses.

The relationship between environmental variables

and the structure of the infaunal assemblages,

factoring in taxonomic and functional groups, was

analysed by the multivariate ordination technique

canonical correspondence analysis (CCA). Collin-

earity and stepwise regression analyses were

employed for selection of the environmental vari-

ables used in CCA. The reduced model used

considered weight of shells and percentage of sand.

The significance of the ordination axes was tested

by ANOVA (a = 0.05).

PERMANOVA, PERMDISP and nMDS analyses

were based on the Bray–Curtis dissimilarity coeffi-

cient. All analyses (except PERMANOVA and

PERMDISP) and graphical visualizations were gen-

erated in R 2.15 (R Development Core Team, 2009),

using the packages GAD (Sandrini-Neto & Camargo,

2010), vegan (Oksanen et al., 2009) and sciplot

(Morales, 2012).

Results

Trends in the variability of environmental parameters

of each tidal flat are shown in the PCA plots (Fig. 2).

In Pasto (Fig. 2a), the first two components accounted

for 54.2% of the total variability. The variability on the

first axis was associated mainly with weight of shells

and pebbles, percentages of sand and mud and content

of organic matter. The variability on the second axis

was associated with weight of shells, percentages of

sand and mud and contents of organic matter and

CaCO3. The major differences among distances were

observed along the first axis between the nearest and

the farthest points from the rocky shores. Nearest

points tended to have a higher amount of shells

(146 ± 19.2 g), pebbles (17.2 ± 8.5 g) and mud

(33.6 ± 14.9%) in the sediment matrix compared to

the farthest points ( 38.1 ± 12.5, 7.8 ± 3.8 g and

64 ± 17.4%, respectively). Weight of macro-debris

and sorting coefficient contributed little to the vari-

ability of the environmental parameters in this tidal

flat. In Limoeiro (Fig. 2b), the first two components

accounted for 56.6% of the total variability. The

variability on the first axis was associated mainly with

percentages of sand and mud, content of organic

matter and sorting coefficient. The second axis

variability was associated with weight of shells,

pebbles and macro-debris. Notable differences

between the nearest and farthest points were only

observed for area 2 which were related to the second

axis. Nearest points tended to have higher amount of

shells (38.1 ± 12.5 g) and pebbles (7.8 ± 3.8 g)

compared to the farthest points ( 8.6 ± 2.4 and

1 ± 0.5 g, respectively). Weight of macro-debris

and contents of organic matter and CaCO3 contributed

little to the variability of the environmental parameters

in this tidal flat. In both tidal flats, the nearest points

had a higher variability of environmental parameters

in comparison to the most distant points. None of the

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123

environmental variables showed a clear variation

pattern between areas.

A total of 16,373 individuals from 100 taxa belonging

to 15 functional groups were identified (Appendix 1—

Supplementory material). The most common taxa were

the bivalve A. flexuosa (4,445; 27.14%), the polychaetes

Sigambra sp. (1,877; 11.46%), Laeonereis sp. (1,248;

7.62%) and Armandia hossfeldi Hartmann-Schroder,

1956 (939; 3.51%), an unidentified morphotype of a

cumacean crustacean (Cumacea sp. 1; 1,602; 9.78%)

and a sphaeromatid isopod sampled only in Limoeiro

(Sphaeromatidae sp.; 850; 5.19%). The most common

functional groups were D-Fil (4,541; 27.7%), M-Bur

(3,559; 21.7%), M-Sur (2,733; 16.7%), M-Car (2,199;

13.4%), D-Sur (960; 5.9%) and M-Her (879; 5.4%).

In general, the variation patterns of total density,

richness and the density of the most common

taxonomic and functional groups along the distances

from the rocky shores were dependent on the tidal flat

analysed (Table 1; Fig. 3). The total density differed

significantly among distances only in Pasto, where the

farthest points showed higher densities than the

nearest points (SNK, P \ 0.05; Fig. 3a). Average

values of richness differed significantly between

distances in the two tidal flats, but it was dependent

on the area (Table 1). A tendency of richness increas-

ing with distance from the rocky shores was recorded

only in Limoeiro (Fig. 3b). Only two of the six most

common species, Anomalocardia flexuosa (Fig. 3c)

and A. hossfeldi (Fig. 3d), had significantly lower

densities in the points near the rocky shores, when

compared to the farthest points in Pasto (SNK,

P \ 0.05). The densities of the species Sigambra sp.,

Laeonereis sp., Cumacea sp. and Sphaeromatidae sp.

were highly variable between areas and distances in

both tidal flats, and did not show any consistent

variation pattern in relation to the distance from the

rocky shores (Appendix 2—Supplementory material).

Tendencies of decreased densities with proximity

to the rocky shores were also recorded for the

functional groups D-Fil (Fig. 3e) and M-Bur (Fig. 3f)

in Pasto. The D-Fil density was significantly higher in

the farthest points than the nearest points in Pasto

(SNK, P \ 0.05) even with the significant differences

between areas. The M-Bur density was also signifi-

cantly higher in the farthest points in Pasto (SNK,

P \ 0.05), but this pattern was dependent on the

analysed area (Table 1). The densities of the func-

tional groups M-Sur, M-Car, D-Sur and M-Her were

highly variable and showed no gradual or consistent

pattern among areas or distances in either tidal flats

(Appendix 3—Supplementory material). None of the

functional groups showed any consistent variation

pattern across distances from the rocky shores in

Limoeiro.

Pasto and Limoeiro differed significantly in taxo-

nomic and functional composition (PERMANOVA,

P \ 0.05). Multivariate analysis considering taxo-

nomic and functional groups showed that assemblage

compositions were highly variable across areas and

distances from rocky shores in both tidal flats

(Table 2). A clear colour gradient reflecting the

taxonomic and functional turnover across distances

was observed across distances in the nMDS ordina-

tions of both tidal flats (Fig. 4). However, significant

differences in taxonomic and functional composition

across distances were dependent on the analysed area

(Table 2). Pairwise tests a posteriori of the PERMA-

NOVAs considering taxonomic and functional groups

(a) Pasto

(b) Limoeiro

~ 10 cm 1 m 2 m 4 m 8 m 16 m

Area 1 Area 2

sand

mud

pebbles

CaCO3sorting

shells

O.M.

macro-debris

sand

mud

pebbles

CaCO3

sortingshells

O.M.macro-debris

Fig. 2 Principal component analysis (PCA) of the abiotic

variables from the Pasto (a) and Limoeiro (b) tidal flats,

highlighting areas and distances from the rocky shores. OM

content of organic matter; sorting sorting coefficient

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123

showed that the assemblages at the points nearest to

the rocky shores (*10 cm to 4 m) tended to differ

significantly from the assemblages at the most distant

points (16 m), in all areas and tidal flats (Table 2). The

taxonomic and functional composition of assemblages

at the nearest points was significantly more variable

~ 10 cm 1 m 2 m 4 m 8 m 16 m

Pasto LimoeiroArea 1 Area 2 Area 1 Area 2

Pasto LimoeiroArea 1 Area 2 Area 1 Area 2

Ave

rage

val

ues

per

core

r (0

.018

m²)

(c) Anomalocardia flexuosa (d) Armandia hossfeldi

(a) Total density (b) Richness (S)

(e) D-Fil (f) M-Bur

Fig. 3 Average values

(±SE) per core (0.018 m2)

of total density (a), richness

(b), and densities of the

species Anomalocardia

flexuosa (c) and Armandia

hossfeldi (d), and the

functional groups D-Fil

(discretely motile,

suspensivore) (e) and M-Bur

(motile, subsurface deposit

feeder) (f) for each distance,

area and tidal flat analysed

Table 1 Analysis of variance comparing the average values

per core of total density, richness (S), and the densities of the

species Anomalocardia flexuosa and Armandia hossfeldi, and

the functional groups D-Fil (discretely motile suspensivores)

and M-Bur (motile subsurface deposit feeders), for each tidal

flat analysed

df Total densitya Richness Anomalocardiab Armandiaa D-Fila M-Bura

F P F P F P F P F P F P

Pasto

Area (A) 1 30.3 <0.0001 5.55 <0.05 18.88 <0.0001 0.49 0.48 19.03 <0.0001 0.01 0.91

Distance (D) 5 21.66 <0.01 0.25 0.92 14.86 <0.01 8.7 <0.05 15.35 <0.01 3.57 0.09

A*D 5 1.41 0.22 3.96 <0.05 1.97 0.09 2.3 0.05 1.90 0.10 4.06 <0.01

Residue 96

Limoeiro

Area (A) 1 27.31 <0.0001 4.065 <0.05 7.11 <0.01 12.6 <0.001 9.81 <0.01 22.07 <0.0001

Distance (D) 5 1.16 0.43 4.0699 0.07 1.81 0.26 1.1 0.45 0.29 0.89 5.44 <0.05

A*D 5 1.92 0.09 3.458 <0.01 2.86 <0.05 1.73 0.13 4.82 <0.001 0.25 0.94

Residue 96

Significant terms (a = 0.05) are highlighted in bolda Data transformed to the square rootb Data transformed to the fourth rootc Data transformed to ln (x ? 1)

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than those in the farthest points (PERMDISP,

P \ 0.05) for both tidal flats (except for area 1 of

Limoeiro). This pattern can be visualized in the nMDS

ordinations (Fig. 4), in which the farthest points (dark

colours) were more clustered than the nearest (light

colours).

The relationship between environmental variables

and structure of the infaunal assemblages considering

taxonomic and functional groups are shown in the

CCA ordinations (Fig. 5). The first two axes were

statistically significant for the taxonomic and func-

tional group ordinations (p \ 0.05) and accounted for

16.2 and 24.8% of the total variability, respectively.

The relationship between environmental variables and

the first two ordination axes in the ordinations

considering taxonomic and functional groups were

similar to each other. Differences between tidal flats

were associated with the first axis, which showed a

high correlation with weight of shells. On the other

hand, differences among distances were related to the

second axis, which showed a high correlation with

percentage of sand. In the ordination considering

taxonomic groups (Fig. 5a), we observed a clear

distinction between taxa associated with sediments

with high quantities of shells in Pasto (e.g. A. hossfeldi

and A. flexuosa), and taxa associated with muddy

sediments and without shells in Limoeiro (e.g. Cum-

acea sp. 1). The ordination considering the functional

groups (Fig. 5b) showed similar patterns to the

taxonomic groups ordination (Fig. 5a). The relation-

ships of the six numerically dominant functional

groups with the environmental variables were clus-

tered to the centre of the ordination, but two reflected

the relationship observed for two of the numerically

dominant taxa: D-Fil and A. flexuosa; and M-Her and

Sphaeromatidae sp.

Discussion

Infaunal structure differed among distances from the

rocky shores in both Pasto and Limoeiro tidal flats.

However, variation patterns in the total density,

richness and density of the numerically dominant taxa

and functional groups were dependent on the tidal flat

analysed rather than proximity to hard substrates,

partially refuting our working hypothesis. These

inconsistent patterns result from differences in the

species composition between tidal flats, and by the

individual responses of each taxon or functional group

to the proximity to the rocky shores.

The significantly lower infaunal density near the

rocky shores in Pasto was related to variations in the

numbers of the two numerically dominant taxa, A.

hossfeldi and A. flexuosa. Therefore, gradual variation

in density was influenced by these two species. A

decrease of total infauna densities associated with

formations of infaunal haloes was not recorded in the

Table 2 Permutational multivariate analysis of variance

(PERMANOVA) comparing the trend of variation of benthic

assemblages (9,999 permutations), considering taxonomic and

functional groups of each tidal flat analysed

df Taxonomic groups Functional groups

Pasto Limoeiro Pasto Limoeiro

P P P P

Area (A) 1 <0.01 <0.0001 <0.001 <0.0001

Distance (D) 5 0.7 0.84 <0.05 <0.05

A*D 5 <0.0001 <0.0001 <0.001 <0.0001

Residue 60

Pairwise tests a posteriori (9,999 permutations)

Taxonomic groups Functional groups

Pasto Limoeiro Pasto Limoeiro

A1 A2 A1 A2 A1 A2 A1 A2

D1*D2 * ns ns ns ns * * ns

D1*D3 ns ns * ns ns ** * *

D1*D4 * *** * ** ** ** *** **

D1*D5 ** ** ** ** *** ** *** ***

D1*D6 ** ns ** ** *** ** ** **

D2*D3 ns ** ns ns ns ns ns ns

D2*D4 ns *** ns ** ** ns * ns

D2*D5 ** ** * ** *** ns ** *

D2*D6 ** * * ** ** *** ** ***

D3*D4 ns ** ns ** * ns ns ns

D3*D5 ** ** ns ** * ns * **

D3*D6 ** * ns ** *** *** ns ***

D4*D5 ** * ns ns ns ns * *

D4*D6 ** ** ns ** * *** * **

D5*D6 ns ns ns ns ns * ns ***

Pairwise tests a posteriori compared the levels of the factor

distance in each tidal flat and area. Data transformed to the

square root

Significant terms (a = 0.05) are highlighted in bold

D1 = *10 cm, D2 = 1 m, D3 = 2 m, D4 = 4 m,

D5 = 8 m, D6 = 16 m

* P \ 0.05; ** P \ 0.001; *** P \ 0.0001

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vicinity of rocky shores in Limoeiro. A decrease in

species richness near the rocky shores was observed

only in Limoeiro. Such inconsistent patterns are

related to differences in specific composition and

sediment heterogeneity, as suggested by Davis et al.

(1982), Kelaher et al. (1998) and Barros et al. (2001).

Species or selected groups from an assemblage may

respond differently to boundaries between

environments (Davis et al., 1982; Summerson &

Peterson, 1984; Dangerfield et al., 2003; Langlois

et al., 2005). In boundaries between reefs and soft

sediments, negative infaunal responses to the proxim-

ity of hard substrates are generally attributed to the

interaction of reef organisms with the biota of adjacent

sediments (Dahlgren et al., 1999; Langlois et al., 2005;

Galvan et al., 2008), or with variations in sediment

Pasto A1

stress = 0.10

Pasto A2

stress = 0.11

Limoeiro A2

stress = 0.14

Limoeiro A1

stress = 0.19

~ 10 cm 1 m 2 m 4 m 8 m 16 m

Pasto A1

stress = 0.17

Pasto A2

stress = 0.14

Limoeiro A1

stress = 0.23

Limoeiro A2

stress = 0.15

(a) Taxonomic groups (b) Functional groups

Fig. 4 nMDS ordinations of the benthic assemblages considering the taxonomic (a) and functional (b) groups at each distance in each

area and tidal flat analysed. A1 area 1, A2 area 2

sand

shellssand

shells

~ 10 cm 1 m 2 m 4 m 8 m 16 m

Pasto Limoeiro

(b) Functional groups(a) Taxonomic groups

Sphaeromatidae sp.

A. flexuosa

Cumacea sp.1A. hossfeldiSigambra sp.

Laeonereis sp.

M-Her

D-Fil D-SurM-SurM-Car

M-Bur

Fig. 5 Canonical correspondence analysis (CCA), depicting

the variation trends of assemblages considering taxonomic

(a) and functional groups (b) with weight of shells, and

percentage of mud and sand environmental variables. Codes of

the functional groups indicate locomotion capacity (M motile,

D discretely motile) and feeding habits (Car carnivore, Her

herbivore, Sur surface deposit feeder, Bur subsurface deposit

feeder)

Hydrobiologia

123

texture (Ambrose & Anderson, 1990). Small predators

like the crab Pachygrapsus transversus Gibbes, 1850

(Christofoletti et al., 2010) and fishes of the families

Blenniidae and Gobiidae (Barreiros et al., 2004) are

known to be associated with rocky shores and tidal

pools in southern Brazil. Blue crabs (Callinectes sp.)

and puffer fishes are frequently observed in the region

as the numerically dominant macropredators in tidal

flats. However, none of them was observed in the

study areas. Although we have not evaluated foraging

intensity, the low density of potential predators

suggests that the negative patterns shown by infauna

are not regulated by predation.

Species composition differed significantly and

consistently between the nearest and farthest points

from the rocky shores in both tidal flats. Similar

variation patterns were also recorded for subtidal

bottoms (Barros et al., 2001; Barros, 2005; Langlois

et al., 2005). Much of the variation for both the

taxonomic and functional groups was explained by

sediment texture, such as shell content and percent-

ages of sand. The accumulation of carbonate shells

alters the sediment matrix, directly and indirectly

affecting resource availability (Gutierrez et al., 2003).

Shells can positively affect the macrofauna by creating

microhabitats and supplying material for tube-build-

ing animals and providing hard surfaces for incrusta-

tion, or negatively by inhibiting burrowers (Gutierrez

& Iribarne, 1999; Reise, 2002; Gutierrez et al., 2003).

Significant changes in infaunal assemblage struc-

ture were observed along the increasing distances

from the rocky shores in both tidal flats. This pattern is

an edge effect associated to the boundary between

rocky shores and tidal flats. Similar patterns are known

for subtidal and intertidal habitats (Cusson & Bourget,

1997; Kelaher et al., 1998; Barros et al., 2001), and the

edge effect may be detected even in extensions larger

than 50 m in some subtidal environments (Davis et al.,

1982; Posey & Ambrose Jr., 1994). The edge effect

zone can be temporally variable, and may suffer

seasonal retreats or advances (Farina, 2010). We have

identified an edge effect related to the influence of

rocky shores in tidal flats at a scale of metres. Faunal

assemblages in boundaries between different benthic

systems are indeed defined by spatially short-scaled

processes (Gosz, 1993; Strayer et al., 2003; Erdos

et al., 2011), including microtopography, heterogene-

ity, physical and chemical characteristics of the

sediment, ecological interactions, local currents and

resource availability (Jumars &Nowell, 1984; Cusson

& Bourget, 1997; Langlois et al., 2005; Gartner et al.,

2013).We suggest that any approach to analyse small-

scale spatial patterns of macroinvertebrate distribution

across habitats should consider the edge effect in such

intertidal systems.

Infaunal assemblages were more variable nearer to

than far from the rocky shores. Higher faunal

variability in the surroundings of rocky reefs in

comparison to more distant points may be associated

with varying physical and biological factors (Barros

et al., 2001). Since sediment texture is a determinant

factor in structuring infaunal assamblages (Anderson,

2008), any spatial variation in flow that affects

sediment dynamics could have effects in the local

infauna. Although we have not measured current

direction and speed, high variability of sediment

texture near the rocky shores indicates changes of flow

conditions. Both Pasto and Limoeiro have discontin-

uous rocky shores that are composed of boulders often

isolated from the mainland formations. The irregular

distribution of rocks in the two tidal flats may result in

alternate high and low water flow areas (Jumars &

Nowell, 1984; Bertasi et al., 2007). This may directly

affect benthic-structuring processes, such as growth of

microbial colonies, faunal recruitment and availability

of particulate food (Jumars & Nowell, 1984; Abelson

et al., 1993).

The development of an infaunal halo in Pasto is

clearly associated with the functional structure of the

local assemblage. The negative infaunal response to

the proximity of rocky shores was mainly associated

with variations in the numbers of suspensivores and

subsurface deposit feeders (D-Fil and M-Bur). Marked

variations in the distribution of functional groups are

expected across environmental gradients, since differ-

ent groups display different trait combinations directly

related with their life strategies (Bolam & Eggleton,

2014). Gradients in physical factors related with the

rocky shores’ proximity, such as flow velocity and

sediment texture, can have sensible effects on the

settlement of suspensivores and deposit feeders (Qian,

1999; Rosenberg, 2001). We therefore suggest that the

development of an infaunal halo in Pasto results from

the responses of the local dominant functional groups,

D-Fil and M-Bur, to a sharp gradient in physical

characteristics near the rocky shores.

Hydrobiologia

123

Conclusions

Changes in infaunal structure due to proximity to

rocky shores were recorded in all studied sites of

Limoeiro and Pasto, but the development of an

infaunal halo was only observed in the latter. The

inconsistency in faunal patterns reflects differences in

the taxonomic and functional structure of local

assemblages. Although we were not able to detect

linear variation patterns in sediment texture, much of

the infaunal variation was clearly correlated with it.

We conclude that infaunal distribution patterns related

to the edge effect between intertidal habitats are highly

dependent on the local species and functional group

composition and of the species-specific responses to

small-scale gradients of sediment texture. Field

experiments may be helpful in providing further

understanding of the relationships between infaunal

structure and sediment properties in these intriguing

ecological boundaries.

Acknowledgments This study was funded by the Federal

University of Parana (Universidade Federal do Parana—UFPR)

and the Graduate Programme in Oceanic and Coastal Systems

(Programa de Pos-Graduacao em Sistemas Costeiros e

Oceanicos—PGSISCO—UFPR). CAPES (Coordenacao de

Aperfeicoamento de Pessoal de Nıvel Superior) funded the

first author. We thank Mauricio Camargo (UFPR) and Rodolfo

Elias (UNMDP) for reviewing earlier drafts of this manuscript,

Veronica Oliveira (UFPR) for helping with identifications, and

all the students who helped with the fieldwork. We also thank

Stuart Jenkins and an anonymous referee for the valuable

criticisms on an earlier version of this manuscript.

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