PRIMARY RESEARCH PAPER

Marine intrusion and freshwater discharge as oppositeforces driving fish guilds distribution along coastal plainstreams

Rodrigo Ferreira Bastos • Lauro Julio Calliari •

Alexandre Miranda Garcia

Received: 7 April 2013 / Revised: 25 November 2013 / Accepted: 26 November 2013 / Published online: 6 December 2013

� Springer Science+Business Media Dordrecht 2013

Abstract This work investigated variations in fish

guilds along marine surf zone to freshwater reaches of

coastal plain streams and their relationships with

environmental factors. Fish and abiotic data were

collected monthly during 1 year and an automatic

image-recording system was used to monitor marine

intrusion events. Aside ephemeral salinity gradients

produced by storm surges, freshwater conditions

prevailed inside streams. Despite of that, fish habitat

use guilds were spatially distributed according to their

salinity tolerance, with marine species occurring

mainly in the stream site near the adjacent surf zone

and non-salinity tolerant freshwater fish in the

upstream site. Marine intrusion was the main factor

correlated with the entrance of marine-related fish into

streams during summer. In contrast, higher rainfall

during colder months prevented the dominance of

marine species. This work highlighted that spatial

segregation in fish habitat use guild could occur even in

the absence of long-lasting salinity gradients, since

active colonization by euryhaline fish and sporadic

marine intrusions can lead to the occurrence of marine-

related fish in coastal plain streams. Future studies

should evaluate if this marine intrusion role on fish of

coastal plain streams would be affected by changes in

sea level and rainfall in a global warming scenario.

Keywords Storm surge � Marine surf zone �Floods � Meteorological tide � Habitat use �Functional guilds � Spatial segregation

Introduction

Salinity is one of the main environmental factors

influencing fish assemblage structure at the interface

between marine and freshwater habitats (Garcia et al.,

2003a; Winemiller et al., 2008; Moura et al., 2012).

However, additional factors play a role in habitat

structuring and directly and indirectly influence the

salinity gradient. For instance, high precipitation in

watersheds can increase the freshwater discharge in

bodies of water connecting freshwater and marine

environments, hindering the movement of species from

Handling editor: M. Power

R. F. Bastos (&) � L. J. Calliari � A. M. Garcia

Instituto de Oceanografia, Universidade Federal do Rio

Grande (FURG), Av. Italia, Km 8, PO Box 474, Rio

Grande, Rio Grande do Sul 96203-900, Brazil

e-mail: rfbastos@furg.br

R. F. Bastos � A. M. Garcia

Programa de Pos Graduacao em Biologia de Ambientes

Aquaticos Continentais, Instituto de Ciencias Biologicas,

Universidade Federal do Rio Grande (FURG), Av. Italia,

Km 8, Rio Grande, Rio Grande do Sul, Brazil

Present Address:

R. F. Bastos

Programa de Pos Graduacao em Zoologia, Pontifıcia

Universidade Catolica do Rio Grande do Sul, Av.

Ipiranga, 6681. Predio 12 C. Partenon, Porto Alegre, Rio

Grande do Sul 90619-900, Brazil

123

Hydrobiologia (2014) 726:245–258

DOI 10.1007/s10750-013-1771-7

the sea into freshwater systems (Garcia et al., 2001,

2003b). Additionally, the increase in sea level and the

resulting marine intrusion (e.g., a salt wedge) can limit

the dominance of freshwater species (Whitfield, 1999).

Wind pattern is one of the major abiotic factors

increasing or decreasing marine influence along the

coasts (Boyce, 1954; Castello, 1985; Costa et al.,

1988; Saraiva et al., 2003). Sea spray and marine

intrusions depend primarily on the orientation of the

coast, the strength and direction of the wind, and the

size of the beach backshore (Boyce, 1954; Castello,

1985; Costa et al., 1988). Depending on the direction

and intensity of the wind, marine intrusions and salt

spray represent causal factors that can either promote

or moderate marine influence on coastal plain streams.

In addition to these recognized abiotic patterns,

several types of extreme events can regulate the marine

influence on coastal plain streams. Storm surge events

with large waves and strong winds can cause seawater to

invade the post-dune region, particularly at points where

the foredune ridges are naturally absent due to erosion

throughout the course of the stream. Even wetlands and

water bodies without direct marine connections, but

located near foredune ridges, may suffer marine influ-

ence (Sanchez-Botero et al., 2008). On the southernmost

coast of Brazil a small tidal range (0.5 m) occurs and sea

level increases almost exclusively during storm surges

(meteorological tide), which are strongly associated

with intense SW winds (Castello, 1985; Costa et al.,

1988; Saraiva et al., 2003; Serpa et al., 2011).

Innumerable coastal plain streams or washouts

occur along the southern Brazilian coast. These

streams are distributed along the 620-km coastal plain

of the southermost state in Brazil and emerge through

the coastal foredunes toward the adjacent marine surf

zone. The washouts are formed in ponds and wetlands

located behind the foredune ridges (Silva, 1998;

Figueiredo & Calliari, 2006). Silva (1995) reported

that between 2 and 22 streams occur every 10 km.

These streams are more numerous during months of

higher rainfall and lower evaporation rates and less

common during the dry months (Silva, 1998). The

high variability in the number of streams results from

the formation and disappearance of ephemeral and

intermittent streams (Figueiredo & Calliari, 2006).

Despite the temporal and spatial variability of these

types of streams, permanent streams also occur along

the coast and maintain a year-round connection with

the sea (Figueiredo & Calliari, 2006).

Along the course of permanent coastal plain streams,

we can expect marine and estuarine species to occupy and

to be most abundant in the region near the connection

with the sea. Conversely, the primary freshwater species

(sensu Myers, 1938) must occupy sheltered areas with

less marine influence. This expected pattern of assem-

blages along a spatial gradient may be altered by the main

abiotic factors that enhance marine intrusions (e.g., wind

and storm surges) or freshwater discharge (e.g., precip-

itation). For instance, in the largest estuary found in

southern Brazil, higher precipitation can have negative

effects on the entrance of juvenile forms of marine-

spawning fish species into the estuarine zone (Castello &

Moller, 1978; Moller et al., 2009), especially during

extreme events triggered by El Nino episodes (Garcia

et al., 2004). In contrast, E and SE winds increase the

entrance of saltwater into this estuary and can favor the

entrance of marine organisms (Castello & Moller, 1978).

Accordingly, it is plausible that the variability of

these two factors (wind and rainfall) could also

increase or decrease the marine influence on coastal

streams located in this subtropical coastline and,

consequently, structure their fish assemblages accord-

ing to their abilities to tolerate salinity conditions.

Thus, we hypothesized that marine fishes or species

that have part of its life cycle related to the saline waters

(the marine fish guild) are more abundant and frequent

within the lower reaches of the streams near the

adjacent marine surf zone. In contrast, those freshwater

fish families that, in evolutionary terms, have lost their

ability to withstand salinity (the primary freshwater

fish guild) are abundant and frequent in the upstream

reaches, situated more far away from its connection

with sea. Finally, freshwater fish that tolerate varia-

tions in salinity (the secondary freshwater fish guild)

are evenly distributed along the entire coastal stream.

To test these expected patterns, the present study

investigated the seasonal variation in species compo-

sition and abundance of fish guilds along marine surf

zone to freshwater reaches of coastal plain streams and

their relationships with environmental factors.

Materials and methods

Studied area

The study area includes the southern coast of Rio

Grande do Sul state (RS), the southernmost state in

246 Hydrobiologia (2014) 726:245–258

123

Brazil. The northern limit of this area is the western

jetty of Patos Lagoon. The area extends to Chui Stream,

the southernmost point on the Brazilian coast. Three

permanent streams were studied (S1: 32�17023.500S,

52�15039.200W; S2: 32�21034.900S, 52�18039.900W; and

S3: 32�23014.700S, 52�19026.700W) (Fig. 1a, b). Two

distinct areas of each stream, designated sites A and B

(Fig. 1c), were selected to evaluate the spatial varia-

tions in species composition and abundance of fish

assemblages. The first area (site A) was located on the

foredune barrier and was more strongly influenced by

the adjacent marine environment than site B, which

was located in a region close to freshwater wetlands

(which are common in this region) and which was more

distant from marine influence. Additionally, samples

were collected in the surf zone adjacent to each stream

(site M) (Fig. 1c) to verify the fish composition and

abundance in this zone.

Sampling strategy

Monthly samples were collected at sites A and B in

each of the three streams (S1–S3) from April 2010 to

March 2011. Morphological and physical habitat

measurements were obtained monthly at each sam-

pling site. At each site (A and B), the stream width was

measured at the narrowest point of the section sampled.

The average stream depth (cm) in each fish sampling

site was computed based on measurements of the depth

taken every one meter along a transversal section of the

coastal stream reach. Temperature and salinity were

recorded at all sites including the marine adjacent area

(site M). To detect seawater intrusions during a storm

surge event, salinity was recorded in a stream near the

Marine Aquaculture Facility of the Universidade

Federal do Rio Grande—EMA (Fig. 1a).

Three different sampling techniques were employed

to capture the greatest possible number and diversity of

fish species. Three beach seine hauls (6 m long; with a

13-mm stretch mesh in the wings and a 5-mm stretch

mesh in the center 3-m section) covering an area of

approximately 40 m2 per haul were made at each

sampling site every month studied. Additionally, three

hauls were conducted with a beam trawl. Each haul with

the beam trawl swept an area of approximately 8 m2. The

beam trawl network used has a rigid square PVC frame

(0.8 9 0.8 m) attached to a multifilament mesh bag (5-

mm stretch mesh). In addition, fish was collected with a

dip net (39 cm diameter, 5-mm stretch mesh) that was

operated for 15 min at each sampling site. Additionally,

during winter months, we used dip net at temporary

freshwater ponds adjacent to the streams’ flooded

margins because there was a suspicion that they could

harbor annual killifishes, which are common in similar

habitats along the Brazilian coastal plain. Since these

samples were sporadic and opportunistic they were not

included in the statistical analyses (MDS, Cluster, CCA).

To complement these samples taken inside the

streams, three additional beach seine samples were

collected monthly at the marine surf zone adjacent to

each stream (site M) from April 2010 to March 2011.

Logistical problems prevented the collection of sam-

ples in the marine adjacent area to each stream during

April to June of 2010. In order to fill this sampling gap,

samples collected in these missing months with the

same fish gear (beach seine) by the Brazilian Long

Term Ecological Research program in a surf zone site

distant 12 km north of our studied streams (S1)

(Fig. 1a) were used. All captured specimens were

fixed in 4 % formaldehyde in the field and taken to the

laboratory, where they were identified, counted, and

measured (total length—TL).

Daily data on the SE, E, and SW winds (both

predominant direction and mean intensity), which can

influence and foster advances of the sea toward the

dunes and streams, and rainfall were obtained in a

meteorological station located *25 km of the studied

area. Additionally, the degree of intrusion of the sea

into the streams was monitored using mosaics

(merged) of ‘‘timex images’’ supplied by the Argus

system (Holland et al., 1997).

The Argus monitoring system consists of four video

cameras attached to a tower 14 m in height. The

overlapping images (mosaic) provided by the system

serve to monitor a distance of approximately 300 m

along the beach line and 600 m perpendicular to the

shore. The resulting timex images represent the average

of 600 snapshots captured by each camera every second

for 10 min everyday during each daylight hour. The

average intensity of the brightness of each pixel

corresponding to 600 images acquired is calculated by

generating a long-exposure image (timex) in the visible

spectrum (red–green–blue) (Guedes et al., 2009).

A total of 3,643 mosaics of timex images were

collected from approximately 30 days before the first

data sample (March 29, 2010) through February 12,

2011 to calculate the distance from the beach line to a

fixed landmark within the dunes (Guedes et al., 2009).

Hydrobiologia (2014) 726:245–258 247

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This distance is hereafter referred to ‘‘beach back-

shore.’’ This distance from the beach line was used to

identify the hours, days, and periods at which the sea

was closer to the dune ridges and, therefore, closer to

the streams’ mouth.

Data analyses

First of all, multivariate analyses (non-metric multi-

dimensional scaling and cluster analysis) were used to

evaluate possible differences in environmental data

and fish assemblage attributes (species composition

and abundance) collected among the three sampled

streams (S1–S3) and sampling sites (A and B). The

biological matrix (fish abundance) was composed by

those species that reach at least 0.1 % of total fish

abundance. These analyses did not reveal significant

differences among streams, but only between sam-

pling sites. Hence, in the subsequent analyses (Dom-

inance, ANOVA, and CCA analyses), abiotic and fish

samples collected at each sampling site (regardless of

the stream) were considered as replicates. A similar

approach was employed to pool months into seasons,

as follows: Autumn (April–June), Winter (July–Sep-

tember), Spring (October–December), and Summer

(January–March).

The abundance and patterns of species dominance

were analyzed based on the frequency of occurrence

(FO) and numerical percentage (NP). The FO and NP

were calculated for each species at each sampling

location and season, and represent the frequency of

occurrence and the relative numerical abundance in

percentage, respectively, of a species compared to all

samples made in this period and site. To determine the

species dominance patterns at the sampling sites,

including the marine surf zone, the combination of FO

and NP was used. The values of each species were

compared with the averages of all species (lFO and

lNP) for each situation analyzed (Loebmann &

Vieira, 2005; Garcia et al., 2006). The degree of

species dominance was calculated as described in

Garcia et al. (2006) according to the following four

categories: (1) Frequent and abundant (NP [ lNP and

FO [ lFO); (2) Abundant and infrequent (NP [ lNP

and FO \ lFO); (3).Not abundant and frequent

(NP \ lNP and FO [ lFO); and (4) Not abundant

and infrequent (NP \lNP and FO \ lFO).

Based on the taxonomic classification of the species

and information on the biology and ecology of these

species for the region (Chao et al., 1985; Garcia et al.,

2004), the fishes were classified into three different

habitat use guilds. The Primary Freshwater species

guild (PF) comprised the species belonging to families

that are essentially restricted to freshwater environ-

ments (Helfman et al., 2009). In evolutionary terms,

the majority of these families are those that have lost

the ability to withstand salinity (Myers, 1938). The

Secondary Freshwater species guild (SF) comprised

the species belonging to families that are usually

Fig. 1 Southern region of Rio Grande do Sul state (Brazil)

(a) showing the three permanently connected streams studied

(S1, S2, and S3) and others smaller and ephemerals streams

between S1 and S2 (b). Sample sites at the adjacent marine surf

zone (site M), and near the stream mouth and surf zone (site A)

and at post-dune ridges near freshwater wetlands (site B) (c)

248 Hydrobiologia (2014) 726:245–258

123

restricted to freshwater, but tolerate saltwater due to

the shortest evolutionary course between the marine to

freshwater condition. The species belonging to marine

families or having a certain stage of their life cycle

occurring in the marine environment (e.g., peripheral

freshwater species, Helfman et al., 2009) constituted

the Marine species guild (MA).

A two-way ANOVA was used to test the hypothesis

that the abundance (data log10 (x ? 1) transformed) of

the guilds differed among sites (A and B) and seasons

(Autumn, Winter, Spring, and Summer) and also to

evaluate the variability of environmental variables at

the same spatial and temporal scales. The assumptions

of normality and homoscedasticity were evaluated

with the Kolmogorov–Smirnov and Cochran tests,

respectively (Zar, 1996). A Tukey test was used to

compare average values among treatments. Nonpara-

metric tests (Kruskal–Wallis and Mann–Whitney)

were used when the assumptions of ANOVA were

not achieved (Sokal & Rohlf, 1995). A significant

statistical level of 5 % was used in these tests.

Relationships between the abiotic factors and the

abundance of species in the streams were investigated

with a multivariate direct gradient analysis (Canonical

Correspondence Analysis—CCA) (Ter Braak, 1986).

CCA is a multivariate statistical technique that directly

relates the species abundance to environmental vari-

ables. The technique detects patterns of variation in

species/samples that can be adequately explained by a

matrix of environmental data (Leps & Smilauer,

2003). The CCA ordination technique provides a

diagram showing the variation in species/sample

composition as a function of the environmental

parameters analyzed (Ter Braak, 1986). The CCA

result also indicates the distribution of each species/

sample over the range of variation of the environmen-

tal variables (Ter Braak, 1986).

The species matrix included in the CCA analyses

was constructed after excluding the rare species

(NP \ 0.05) to avoid spurious correlations, resulting

in a matrix of 24 species. The environmental variables

measured at each sampling site (A and B) on the three

streams (S1–S3) and the variables measured at the

meteorological station (rainfall, wind intensity, and

predominant wind direction—E, SE, and SW) were

used in the environmental matrix.

To assess possible cumulative and short-term effects,

the daily data on precipitation and on the intensity of each

wind direction were transformed into several variables.

Each variable represented the accumulation (in the case

of rain) or the average (in the case of wind) for a different

number of days before the sampling date. For each of the

four variables (precipitation, E wind, SE wind, and SW

wind) recorded daily, seven variables were generated,

here termed ‘‘lag variables,’’ which grouped the accu-

mulation/average of 1, 3, 5, 10, 15, 20, and 30 days prior

to the collection date. In this way, 28 ‘‘lag variables’’ were

created as follows: 1—precipitation: 1, 3, 5, 10, 15, 20,

and 30 days; 2—SE wind: 1, 3, 5, 10, 15, 20, and 30 days;

3—E wind: 1, 3, 5, 10, 15, 20, and 30 days; and 4—SW

wind: 1, 3, 5, 10, 15, 20, and 30 days.

Monte Carlo permutation tests were used to evaluate

the statistical significance of the relationships found

between environmental variables and species/samples

(Carmona et al., 1990; Garcia et al., 2003a). The

environmental variables that showed no significant

relationship (P[0.05) were excluded from the subse-

quent steps of the analysis (Leps & Smilauer, 2003). In

the case of the lag variables, the lag variable for each of

the four originally measured variables (precipitation, E

wind, SE wind, and SW wind) which made a significant

contribution in modeling the response variable (P\0.05)

were retained in the analysis, whereas those that did not

were not retained (P[0.05). These procedures were run

on CANOCO package. These selected lag variables were

evaluated seasonally by one-way ANOVA, after testing

the assumptions for normality and homoscedasticity and

statistical significance as described earlier.

Results

Environmental data

The abiotic factors related to system size (width and

depth) showed a seasonal trend, with values ranging

between 0.5 m (January–Summer) and 30 m (July–

Winter) for width and 0.05 and 0.4 m for depth. The

streams were deeper and wider during Winter than

during the other seasons. The average depth (F = 8.66;

P \ 0.01) and width (F = 10.34; P \ 0.01) showed

significant seasonal differences, with higher mean

values in Winter (Tukey; P \ 0.01).

The stream width was spatially variable (F = 5.21;

P \ 0.05), with higher values at the stream mouth

(sites A) than upstream (sites B) (Tukey; P \ 0.05).

No significant differences were observed in average

depth (F = 1.54; P = 0.22). These differences in

Hydrobiologia (2014) 726:245–258 249

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width were observed throughout the study period

(F = 0.3; P = 0.83) (Fig. 2).

The average wind intensity in the SE and E

directions during 30 days prior to each sampling day

showed differences among seasons (SE: H = 39.89,

P \ 0.01 and E: H = 35.91, P \ 0.01), with higher

values in summer and significantly lower values in

winter than in other seasons (Mann–Whitney; P \0.01) (Fig. 2). The SW wind intensity during the 3 days

prior to each sampling day also showed significant

seasonal differences (H = 8.16; P \ 0.05) (Fig. 2).

The higher average SW wind intensity in the autumn

was mainly due to the value observed in April (2.11 m/s).

Even with this high value, the difference was not

significant between seasons (Mann–Whitney; P [0.05).

The accumulated rainfall during 30 days prior to the

sampling day showed two contrasting patterns during

the study: lower values in Spring/Summer and higher

values in autumn/winter (H = 39.89; P \ 0.01)

(Fig. 2). Spring values were significantly lower than

the values in other seasons (Mann–Whitney; P \ 0.01).

The rainfall patterns were inversely related to water

temperature (Fig. 2). Temperature values were signif-

icantly lower in Autumn/Winter than in spring/summer

(H = 55.46; Mann–Whitney; P \ 0.01).

Compared with the adjacent marine areas, which

showed salinity values consistently above 25, the stream

sites showed consistently lower salinity values ranging

between 0 and 2 (Fig. 2). This low range of salinity at the

stream sites did not produce significant differences

between sites A and B (F = 0.77; P = 0.38). However,

differences were observed among seasons (F = 5.33;

P \ 0.01), with higher salinities in autumn (Tukey;

P \ 0.01) and winter (Tukey; P \ 0.05) than in

summer. At the adjacent marine sites, the salinity

ranged significantly (F = 8.41; P \ 0.01) between 8 in

winter and 38 in summer, with higher values in summer

than in other seasons (Tukey; P \ 0.05) (Fig. 2).

Additionally, salinity was recorded in a stream during

a storm surge event (January 12, 2011), when the sea

invaded the foredunes and streams. We recorded a

spatial gradient in salinity during this event, with higher

values in the marine area (35), intermediate values at site

A (26), and the lowest values at site B (21).

The beach backshore size showed statistically sig-

nificant seasonal differences (F = 123.8; P \ 0.01). It

was lower during winter (average 211.96 m), when the

sea was more often near the field dunes and the entrance

of the coastal streams (Tukey; P \ 0.01). For instance,

in July the beach backshore size was only 115.75 m and

corresponded to the highest advance of the sea toward

the dunes (Fig. 3a). In contrast, the beach backshore size

had intermediate values in Autumn (217.36 m) and

Spring (221.01 m), with the former showing statistically

significant lower distance than the latter (Tukey;

P \ 0.01). The higher average value was registered in

Summer (228.16 m) (Tukey; P \ 0.01). For instance, in

December, the sea had its highest distance (267.37 m)

from the dunes and the entrance of the coastal streams

(Fig. 3b). Such highest and lowest peaks in beach back

shore sizes had short time duration, ranging from 1 to

25 h (Fig. 3c).

Temporal and spatial patterns of assemblage

structure

A total of 50,093 individuals of 52 fish species

belonging to 23 families and 9 orders were collected

in the streams and in the adjacent marine surf zone.

The numerical percentage (NP) for each site (A, B, and

M) and the dominance patterns are shown in Table 1.

The mullets Mugil liza and Mugil curema, together

with the plata pompano Trachinotus marginatus, were

the most abundant species. Together, these species

represented 85.45 % of the captures at the adjacent

marine surf zones sites. Eight species were recorded at

the marine sites during autumn, whereas only three

species were recorded in winter. The number of

species recorded at the marine sites increased to 13

species in spring and 16 species in summer. The only

dominant species throughout the study at the marine

sites was the estuarine-dependent mullet M. liza

(Table 1). This species, along with a secondary

freshwater fish, the livebearer Jenynsia multidentata,

was dominant in all seasons and sampling sites within

the streams (sites A and B). Together, these two

species represented 58.36 % of the total number of fish

caught in the streams.

Overall, species of the MA guild showed a gradual

decrease in dominance and occurrence from the

adjacent marine sites (M) to the site near the stream

mouth/connection with the sea (site A) and the site

located farther from the sea and near the wetlands

located back of the foredune ridges (site B). In

addition to this spatial pattern, we also observed a

seasonal trend, with a higher occurrence of marine

species within the streams (sites A and B) in summer

and autumn. The exception was the mullet M. liza,

250 Hydrobiologia (2014) 726:245–258

123

which remained dominant everywhere along the

spatio-temporal gradient (Table 1).

In contrast, the freshwater fish with a higher tolerance

to salinity (the SF guild) and those less tolerant to

salinity (the PF guild) were observed only inside the

streams (sites A and B). The only exceptions were two

species of the SF guild, the livebearers J. multidentata

and Phalloceros caudimaculatus, which were caught in

low numbers (four and two individuals, respectively) at

the adjacent marine sites (M) (Table 1).

The MA and PF guilds showed significant differ-

ences between sites A and B in all seasons (Fig. 4).

The MA guild was more abundant at site A (nearer the

sea connection) than at site B (nearer the freshwater

wetlands) (F = 53.51; P \ 0.01). In an opposite

pattern, the PF guild was more abundant at site B

than at site A (F = 17.28; P \ 0.01) (Fig. 4). The

secondary freshwater fishes (SF guild) did not show

significant differences among sites (F = 0.03;

P = 0.98) (Fig. 4).

Fig. 2 Seasonal

environmental variation

(±95% CI) in the abiotic

factors. Water temperature,

salinity (including site M),

width, and depth were

measured at both sites

(A and B) within the streams,

whereas rainfall and wind

speed information were

obtained from a

meteorological station

distant *25 km of the

studied area. Aut autumn,

Win winter, Spr Spring, Sum

summer

Hydrobiologia (2014) 726:245–258 251

123

Seasonal variation was observed in the PF guild

(F = 35.04; P \ 0.01), with a higher abundance in

spring (Tukey; P \ 0.01) and summer (Tukey;

P \ 0.05) than in autumn/winter. A peak in abun-

dance of PF was recorded in spring and was signif-

icantly higher than in summer (Tukey; P \ 0.01). The

abundance of MA guild had intermediate values in

autumn in relation to the period between spring/

summer and winter and showed no significant differ-

ences from these seasons (Tukey; P [ 0.05). The MA

guild showed lower abundances in winter than spring

and summer (Tukey; P \ 0.05). Otherwise, the SF

guild showed a constant abundance, with an exception

in Summer, where a greater abundance was recorded

(Tukey; P \ 0.01) (Fig. 4).

Correlations between abiotic and biotic factors

The CCA analysis explained 27 % of the total

variability of the data and, together, the first and

second axis explained 16.3 % of the total variance.

A Monte Carlo test showed that the environmental

variables used in the CCA were significantly related to

the species variables (P \ 0.05) (Table 2).

In general, the analyses revealed a marked seasonal

pattern in environmental variation and species abun-

dance. The autumn and winter samples were

associated with higher values of width, depth, and

precipitation, whereas the spring and summer samples

were associated with higher temperature values

(Fig. 5a). The autumn and winter months showed

certain unusual features. The samples from July (7)

were negatively related to temperature, but showed

high variability, with samples more related to precip-

itation and others to width and depth. Unlike the

winter samples, the spring samples were negatively

related to precipitation and depth. As expected, the

summer months were associated with higher temper-

atures, and the months of February (2) and March (3)

were related to the E and SE winds (30 days) (Fig. 5a).

The CCA showed that the dominant species had

different patterns of correlation with the environmen-

tal variables analyzed. With the exception of the

mullet M. liza, all species of the MA guild (e.g.,

Eucinostomus melanopterus, Mugil gaimardianus,

and Mugil curema) were correlated with higher E

and SE wind intensities. In contrast, the SW wind

showed low explanatory power and low correlation

with the variability of the dominant species. Several

species belonging to the PF guild (Mimagoniates

inequalis, Astyanax fasciatus, and Oligossarcus jen-

ynsii) were positively correlated with higher temper-

ature and negatively correlated with the width, depth,

and precipitation. In contrast, the annual fish Aust-

rolebias minuano, which was collected in temporary

Fig. 3 Temporal variation

in beach backshore size

relative to the upper limit at

the automatic image-

recording system (Argus)

reference mark located

inside the foredune ridge.

Images showing an example

of smaller beach backshore

(a) and a larger beach

backshore (b). Variations in

beach backshore size by

daylight hour (c) in autumn,

winter, spring, and summer

252 Hydrobiologia (2014) 726:245–258

123

Table 1 Fish species dominance by sites sampled (Marine sites (M) and two stream sites (A—near the sea, B—sheltered from sea)

and by seasons (Aut autumn, Win winter, Spr spring, Sum summer)

Guilds / Species

Marine (M) Stream (A) Stream (B)

AUT WIN SPR SUM AUT WIN SPR SUM AUT WIN SPR SUM

Marine and estuarine (MA)Mugil liza 1 1 1 1 1 1 1 1 1 1 1 1Mugil curema 4 4 1 1 4 1 4 4 4Trachinotus marginatus 1 4 4 1 4Mugil gaimardianus 4 1 4 4 4Brevoortia pectinata 4 4 3Eucinostomus melanopterus 4 4 3 4 4Menticirrhus littoralis 4 3 3Atherinella brasiliensis 4 3Odontesthes argentinensis 3 4Micropogonias furnieri 3 4 4Platanichthys platana 4Ctenogobius shufeldti 4 4Oncopterus darwinii 4 4Eleotris pisonis 4 4Dormitator maculatus 4 4Lutjanus cyanopterus 4Synbranchus sp. 4Lycengraulis grossidens 4 4Menticirrhus spp. 4 4Anchoa marinii 4Trachinotus carolinus 4Oligoplites saliens 4Pomatomus saltatrix 4

MA species richness 8 3 11 15 9 2 3 6 4 1 2 4Secondary Freshwater (SF)

Jenynsia multidentata 4 4 1 1 1 1 1 1 1 1Phalloceros caudimaculatus 4 3 1 3 3 1 1 1 1Cnesterodom decemmaculatus 4 3 3 3 1 1 3 3Crenicichla lepidota 4 4 4 3 4 4 4Cichlasoma portalegrense 4 4 4 4 4 4Australoheros acaroides 4 4 4 3 4 4 4 4Geophagus brasiliensis 4 4 4

SF species richness 0 0 2 1 7 6 4 7 6 5 7 6Primary Freshwater (PF)

Hyphessobrycon luetkenii 4 4 1 1 1 3 1 1Cheirodon interruptus 3 3 1 3 1 3 1 3Astyanax eigenmanniorum 3 4 3 1 1 4 3 3Mimagoniates inequalis 4 4 4 1 4Characidium rachovii 4 3 3 3 3 1 3 4Hyphessobrycon boulengeri 4 4 4 4 4 4Pimelodella australis 3 4 4 4 4 4Corydoras paleatus 4 4 4 4 4 4 4 4Oligosarcus jenynsii 4 4 4 4 4 4 4Austrolebias minuano 4 4Hyphessobrycon bifasciatus 4 4 4 4 4Heptapterus sympterygium 4 4 4 4 4 4Astyanax aff. fasciatus 4 4 4 4 4Hoplias aff. malabaricus 4 4 4 4 4 4 4 4Hyphessobrycon meridionalis 4 4 4 4Cheirodon ibicuhiensis 4 4 4 4 4 4Rhamdia quelen 4 4 4 4Hoplosternum littorale 4 4Astyanax spp. 4Hyphessobrycon anisitsi 4Trachelyopterus lucenai 4Callichthys callichthys 4

PF species richness 0 0 0 0 10 11 15 13 14 14 17 15

1—abundant and frequent, 2—abundant and infrequent, 3—not abundant and frequent, 4—not abundant and infrequent. See

‘‘Materials and methods’’ section for details of these dominance classification categories

Hydrobiologia (2014) 726:245–258 253

123

ponds on the margins of streams, was correlated with

higher values of width, depth, and precipitation and

lower temperatures.

Discussion

The results indicated that occurrence, abundance, and

dominance of the studied ichthyofauna varied in time

and space over the study period, with the entrance of

marine species into the streams influenced mainly by

marine intrusion events and precipitation. The abun-

dance and distribution of the guilds along the limnetic-

marine axis corresponded to the pattern expected from

the degree of salinity tolerance of the species

comprising the different fish habitat use guilds. The

strictly freshwater species were more abundant at the

sites nearest to the wetlands, which were sources for

the species belonging to the PF guild (PF). Con-

versely, the marine species were more abundant at the

sites nearest to the sea, the source of the MA guild. The

results also confirmed the hypothesis that the salt-

tolerant freshwater species (SF guild) would not differ

in occurrence and abundance between sites under the

influence of sea (site near the surf zone) and freshwater

(site upstream). This spatial pattern of the occurrence

and abundance of fish assemblages along spatial

gradients as a result of the degree of salinity tolerance

of the species has been shown in previous studies. For

example, Moura et al. (2012) showed that salinity is

the main environmental factor structuring the shallow

water fish assemblage along a spatial (marine–estua-

rine–limnetic) gradient in Patos–Mirim lagoon sys-

tem, which is located near the studied coastal stream.

In the current study, however, this overall associ-

ation in fish distribution according with their salinity

tolerance degree was not produced by a pronounced

salinity gradient, since near-zero salinity conditions

were observed throughout the study at both sampling

sites inside the streams. In fact, the observations of the

size of the beach backshore by the remote image-

recording system showed that saltwater intrusions into

these streams are frequent, but of short duration

(1–25 h). One example was the observation on

January 12, 2011 in one of the streams of a marked

salinity gradient during a storm surge event: 35 at sea,

26 at the mouth of the stream, and 21 in a site

upstream. However, this salinity gradient last less than

24 h. This could explain why we did not observe

marked salinity gradients during the monthly field

surveys. Despite their ephemeral nature, such events

may have played a role in colonization of the stream

by strictly marine species (e.g., the plata pompano,

Trachinotus marginatus, and the Cubera snapper

Lutjanus cyanopterus, among others). Studies else-

where have shown that coastal lakes without direct

contact with the sea may harbor estuarine and marine

species. For instance, adults of the silversides Atheri-

nella brasiliensis and catfishes Genidens genidens

were found in Cabiunas Lake, in Rio de Janeiro state,

Brazil (Sanchez-Botero et al., 2008). Since this lake is

not connected to the sea, the authors suggested that

Fig. 4 Seasonal variation in average abundance values of each

fish habitat use guilds (log10 ± 95% CI) at each sampling site

inside the streams (A and B). Aut autumn, Win winter, Spr

spring, Sum summer

254 Hydrobiologia (2014) 726:245–258

123

storm surge events with large waves that wash over the

tops of the dunes would transport these species to the

lake, which is located beyond the foredune ridges.

In addition to patterns in abundance and spatial

distribution of the fish habitat use guilds, several

observations can be made about the occurrence,

abundance, and dominance of particular species.

Together with the estuarine-dependent mullet M. liza,

the one-sided livebearer J. multidentata was one of the

most abundant and frequent species inside the streams

throughout the study. This species is commonly found

in brackish and freshwater systems in southern South

America. For instance, this species is conspicuous in

the estuarine region of Patos Lagoon (Garcia et al.,

2004), but its abundance decreases toward the fresh-

water reaches of this lagoon (Garcia et al., 2003a). The

species is also dominant at Mangueira Lake (Artioli

et al., 2009), which is located in the same coastal plain

of the streams studied here. Although it is not

connected to the sea, this lake gets separated from it

relatively recently (approximately 5,000 years ago)

(Tomazelli & Vilwock, 2005) by a sandy spur that is

currently less than 2 km wide in certain areas. In

addition, Mai et al. (2005) showed that juveniles of J.

multidentata have a higher growth rate and higher

survival under intermediate salinity (16) than in zero

salinity. Although the species is known to occur in

freshwater environments of the region (Tagliani,

1994; Quintela et al., 2007) relatively similar to those

sampled in the present study but sheltered from marine

influence, they are found in low abundance. Thus,

there is evidence that J. multidentata becomes dom-

inant only in shallow environments with abundant

macrophytes (Garcia & Vieira, 1997) and under some

degree of marine influence (Garcia et al., 2004; Artioli

et al., 2009), as is the case of the studied coastal

streams investigated here.

Regarding the marine species found in the streams,

the CCA analysis revealed a significant relationship

among some of them (e.g., the mullets Mugil liza, M.

curema, M. gaimardianus and the Flagfin mojarra

Eucinostomus melanopterus) and the E and SE winds,

which seemed to favor the entrance of these species

into the streams. A similar effect has been previously

described for the nearby Patos Lagoon, where E and

SE winds are know to facilitate the entry of the saline

wedge into the lagoon (Castello, 1985; Costa et al.,

1988). Moreover, the data analyzed in this study

suggest that prior to the April sample, an increase in

sea level brought marine waters toward the streams.

Although it was not higher than other such increases

recorded by the automatic image-recording system,

this sea level increase, combined with a lower stream

discharge (low precipitation), apparently facilitated

Table 2 Canonical Correspondence Analysis (CCA) results performed on the environmental variables and fish abundant species

matrix

Axis 1 2 3 4

Environmental correlation

Temperature -0.729 -0.150 -0.167 0.004

Width 0.441 0.065 -0.152 0.159

Depth 0.381 0.295 -0.408 -0.105

SW wind 3 days -0.036 0.039 0.454 0.134

E Wind 30 days -0.613 0.275 -0.195 -0.153

Accumalated rainfall 30 days 0.351 0.451 0.223 0.147

SE Wind 30 days -0.359 0.295 0.112 -0.372

Eigenvalues 0.110 0.068 0.041 0.030

Species–environmental relation 0.805 0.716 0.678 0.608

Cumulative percentage variance:

Of species 10.1 16.3 20.1 22.9

Of species– environmental relation 37.7 61.0 75.1 85.5

Sum of all Eigenvalues 1.085

Sum of all canonical Eigenvalues 0.291

See ‘‘Materials and methods’’ section for details

Hydrobiologia (2014) 726:245–258 255

123

Fig. 5 Species and sample ordination on the first two Canonical

Correspondence Analysis axes. The species/sample association

with the axis is represented by the score (plotted), and the

correlations among environmental variables and axes are

represented by the length and angle of the vectors. The

association among samples and environmental variables is

shown (a). Each symbol denotes a set of samples made in a

specific month, where numbers indicate months (e.g.,

04 = April), streams (S1, S2, and S3), and sites (A and B) (a).

Each triangle represents the scores for the first two axes for each

species (b). Species name code: ASTEIG—Astyanax eigenman-

niorum; ASTFAS—Astyanax fasciatus; AUSACA—Australoh-

eros acaroides; AUSMIN—Austrolebias minuano; CHARAC—

Characidium rachovii; CHEINT—Cheirodon interruptus; CIC-

POR—Cichlasoma portalegrense; CNEDEC—Cnesterodom

decemmaculatus; CORPAL—Corydoras paleatus; CRELEP—

Crenicichla lepidota; EUCMEL—Eucinostomus melanopterus;

HEPSYM—Heptapterus sympterygium; HOPMAL—Hoplias

aff. malabaricus; HYPBIF—Hyphessobrycon bifasciatus; HYP-

BOU—Hyphessobrycon boulengeri; HYPLUE—Hyphessobry-

con luetkenii; JENMUL—Jenynsia multidentata; MIMINE—

Mimagoniates inequalis; MUGCUR—Mugil curema; MUG-

GAI—Mugil gaimardianus; MUGLIZ—Mugil liza; OLIJEN—

Oligosarcus jenynsii; PHACAU—Phalloceros caudimaculatus;

PIMAUS—Pimelodella australis

256 Hydrobiologia (2014) 726:245–258

123

the active entrance of marine species. The mullet M.

liza show its higher abundance during this month and

the cubera snapper Lutjanus cyanopterus was caught

inside the streams in this period. It is noteworthy that

the occurrence of the cubera snapper in these streams

constitutes the southernmost record in the zoogeo-

graphic distribution of this species (Bastos et al.,

2013).

In summary, the coastal streams in the southern-

most region of the Brazilian coastline shelter a diverse

fish fauna comprised mainly of freshwater fishes and

marine-related fishes, especially mullet juveniles that

move from the adjacent surf zone into these streams in

large shoals. Sea intrusions, driven by E, SE, and SW

winds that are enhanced during storm surges, and

precipitation were the main factors favoring or

hindering the entry of marine-related fish into these

coastal streams, respectively. The daily monitoring

(hour based) of the sea level by the automatic image-

recording system enabled the identification of autumn

and winter as the periods with greater frequency of sea

rises, preventing the dominance of species from PF

guild at the stream site near the sea. On the other hand,

this was also the period with the highest rainfall, which

prevented the dominance of marine species inside the

streams. Other environmental factors, like tempera-

ture, streams’ depth and width, also modeled similar

amounts of variation in the CCA and also influenced

the fish assemblage. However, it is more likely that

they affect seasonal (colder vs. warmer months)

variations in abundance of freshwater species or those

marine-related species after their establishment inside

the streams. Future long-term studies should be

conducted to investigate how variations in sea level

rise and rainfall in a global warming scenario would

affect the role of marine intrusions on the fish fauna of

coastal plain streams at distinct levels (e.g., functional

guilds and species). This could have important impli-

cations to the functioning of ecosystems in these

streams, since recent evidences suggest that mullet

juveniles entering these coastal streams contribute

significant amounts of marine-derived nutrients to its

freshwater food web (Oliveira et al., 2014).

Acknowledgments We thank Fernando Calmon for helping

with image process of ARGUS system; colleagues of the

Ichthyology Laboratory at FURG for helping in field collection

and sample processing; Joao Vieira, Daniel Loebmann and

Nelson Fontoura for reviewing an early version of this paper; the

REUNI (Programa de Reestruturacao e Expansao das

Universidades Federais) and CAPES (Coordenacao de

Aperfeicoamento de Pessoal de Nıvel Superior) for providing

student fellowship for RFB and CNPq (Conselho Nacional de

Desenvolvimento Cientıfico e Tecnologico) for a research grant

for AMG.

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