Composition and abundance of invertebrate benthic fauna in Farfantepenaeus paulensis culture pens...

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Composition and abundance of invertebrate benthic fauna in Farfantepenaeus paulensis culture pens (Patos Lagoon estuary, Southern Brazil) R. Soares a, * , S. Peixoto b , C. Bemvenuti c , W. Wasielesky b , F. D’Incao a , N. Murcia a , S. Suita a a Laborato ´rio de Crusta ´ceos Deca ´podos, Departamento de Oceanografia, Fundac ßa ˜o Universidade Federal do Rio Grande-(FURG), C.P. 474, Rio Grande (RS), CEP 96201-900, Brazil b Laborato ´rio de Maricultura, Departamento de Oceanografia, Fundac ßa ˜o Universidade Federal do Rio Grande-(FURG), C.P. 474, Rio Grande (RS), CEP 96201-900, Brazil c Laborato ´rio de Ecologia de Invertebrados Bento ˆnicos, Departamento de Oceanografia, Fundac ßa ˜ o Universidade Federal do Rio Grande-(FURG), C.P. 474, Rio Grande (RS), CEP 96201-900, Brazil Received 17 November 2003; received in revised form 24 May 2004; accepted 27 May 2004 Available online Abstract Annual Farfantepenaeus paulensis landings in Patos Lagoon are highly variable, and pen culture in shallow estuarine areas has been developed as an alternative for artisanal fishermen. However, there is a concern about the impact of this system in the natural environment. This study was conducted to evaluate macrobenthos occurrence and variation in relation to rearing cycle and production characteristics of pen culture in Patos Lagoon estuary. Macrobenthic invertebrates, organic matter and mud content were sampled inside and outside pens (control). Six major groups (Polychaeta, Tanaidacea, Isopoda, Gastropoda, Amphipoda and Bivalvia) were observed and 11 species were identified. After 21 days of culture, benthos abundance inside pens dropped by around 86%, but no differences between the stocking densities were detected. Benthic species showed different responses to the shrimp culture, and the impact (predation and/or disturbance) on abundance of the macrobenthic invertebrate community was noted. Mud and organic matter content did not differ across sampled areas during culture period. Shrimp attained higher average weight in lowest stocking density. Although the impact of the pen culture is apparently limited to the fenced area and restricted to a short period (3 – 4 months), the expansion of this method of culture in the 0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2004.05.041 * Corresponding author. Tel.: +55-53-2336538; fax: +55-53-2336741. E-mail address: [email protected] (R. Soares). www.elsevier.com/locate/aqua-online Aquaculture 239 (2004) 199 – 215

Transcript of Composition and abundance of invertebrate benthic fauna in Farfantepenaeus paulensis culture pens...

www.elsevier.com/locate/aqua-online

Aquaculture 239 (2004) 199–215

Composition and abundance of invertebrate benthic

fauna in Farfantepenaeus paulensis culture pens

(Patos Lagoon estuary, Southern Brazil)

R. Soaresa,*, S. Peixotob, C. Bemvenutic, W. Wasieleskyb,F. D’Incaoa, N. Murciaa, S. Suitaa

aLaboratorio de Crustaceos Decapodos, Departamento de Oceanografia, Fundac�ao Universidade Federal do

Rio Grande-(FURG), C.P. 474, Rio Grande (RS), CEP 96201-900, BrazilbLaboratorio de Maricultura, Departamento de Oceanografia, Fundac�ao Universidade Federal do

Rio Grande-(FURG), C.P. 474, Rio Grande (RS), CEP 96201-900, BrazilcLaboratorio de Ecologia de Invertebrados Bentonicos, Departamento de Oceanografia, Fundac�ao Universidade

Federal do Rio Grande-(FURG), C.P. 474, Rio Grande (RS), CEP 96201-900, Brazil

Received 17 November 2003; received in revised form 24 May 2004; accepted 27 May 2004

Available online

Abstract

Annual Farfantepenaeus paulensis landings in Patos Lagoon are highly variable, and pen culture

in shallow estuarine areas has been developed as an alternative for artisanal fishermen. However,

there is a concern about the impact of this system in the natural environment. This study was

conducted to evaluate macrobenthos occurrence and variation in relation to rearing cycle and

production characteristics of pen culture in Patos Lagoon estuary. Macrobenthic invertebrates,

organic matter and mud content were sampled inside and outside pens (control). Six major groups

(Polychaeta, Tanaidacea, Isopoda, Gastropoda, Amphipoda and Bivalvia) were observed and 11

species were identified. After 21 days of culture, benthos abundance inside pens dropped by around

86%, but no differences between the stocking densities were detected. Benthic species showed

different responses to the shrimp culture, and the impact (predation and/or disturbance) on

abundance of the macrobenthic invertebrate community was noted. Mud and organic matter content

did not differ across sampled areas during culture period. Shrimp attained higher average weight in

lowest stocking density. Although the impact of the pen culture is apparently limited to the fenced

area and restricted to a short period (3–4 months), the expansion of this method of culture in the

0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved.

doi:10.1016/j.aquaculture.2004.05.041

* Corresponding author. Tel.: +55-53-2336538; fax: +55-53-2336741.

E-mail address: [email protected] (R. Soares).

R. Soares et al. / Aquaculture 239 (2004) 199–215200

shallow waters areas of the Patos Lagoon must be monitored to ensure that greater than expected

impacts do not occur.

D 2004 Elsevier B.V. All rights reserved.

Keywords: Farfantepenaeus paulensis; Shrimp pen culture; Natural food; Benthic macroinvertebrates; Patos

Lagoon

1. Introduction

The pink shrimp Farfantepenaeus paulensis is one of the most commercially

important species exploited in Patos Lagoon estuary (D’Incao and Reis, 2002), which

is regarded as the world’s largest choked lagoon (Kjerfve, 1986). Annual shrimp

landings from artisanal fisheries in Patos Lagoon are highly variable as the entrance

of post-larvae into the estuary depends on sea water inflow (Castello and Moller, 1978;

Reis and D’Incao, 2000). To alleviate the effect of this variable recruitment has on

shrimp landings, F. paulensis pen culture has been developed as an alternative for

artisanal fishermen in this region (Wasielesky et al., 2003). In pen enclosures, shrimp are

reared in their natural habitat for 3–4 months (summer/autumn), which presents some

benefits compared to traditional pond culture, such as low cost and constant water

renewal (Wasielesky et al., 2003). Furthermore, during pen culture, F. paulensis have

access to a variety of natural food items present in sediment, including detritus, plant

material and animal prey.

Previous studies on penaeid feeding behavior in earthen ponds have indicated that

natural food can comprise a significant part of the diet of shrimp, even when pelleted

food is provided (Allan et al., 1995; Nunes et al., 1997; Focken et al., 1998; Nunes and

Parsons, 1999). In nursery ponds of Litopenaeus vannamei, Anderson et al. (1987)

estimated that between 53% and 77% of shrimp growth was due to the grazing on pond

biota. Reports from gut contents analysis have indicated that amongst the natural food

available, benthic fauna is an important food source in shrimp ponds (Allan and

Maguire, 1992; Allan et al., 1995; Nunes et al., 1997; Focken et al., 1998; Shishehchian

and Yusoff, 1999). In addition, some studies reported that benthic fauna declined as

shrimp density and grazing pressure increased (Ordner and Lawrence, 1987; Allan and

Maguire, 1992; Nunes and Parsons, 2000).Therefore, the impact of shrimp predation on

macrobenthic community might be the main factor controlling its abundance in

enclosures.

Although the estuarine macrobenthic invertebrate community from Patos Lagoon has

been well described (Capitoli et al., 1978; Bemvenuti et al., 1978; Bemvenuti, 1987;

Jorgensen, 1998), the interaction between shrimp pen culture and potential prey

abundance has not been studied. Therefore, this study aimed to describe macrobenthos

occurrence and variation in relation to the rearing cycle of F. paulensis and production

characteristics of pen culture in Patos Lagoon estuary. This knowledge may contribute to

the better management of this production system avoiding negative impacts on the

environment.

R. Soares et al. / Aquaculture 239 (2004) 199–215 201

2. Materials and methods

2.1. Experimental facilities and procedures

This study was carried out in a shallow estuarine area in the Patos Lagoon, Rio Grande

do Sul State, Brazil (32j03V55WS, 052j12V30WW) over 63 days.

Six 50 m2 pens (8 m diameter and 2 m height) made of polyester net covered by PVC (5

mm mesh) were used as experimental units. To test the influence of stocking density on

benthos availability, pens were randomly stocked with 10 or 26 juveniles/m2 (three pens

for each density).

The effect of the artifact (pens without shrimp) was not measured since it is considered

small in sheltered areas (Reise, 1985). Besides, previous experiments (Bemvenuti, 1987,

1988, 1994) found no negative impact of these structures on macrobenthos abundance in

the same experimental area.

Juvenile shrimp (f 1 g body weight) were obtained from reproduction of wild

broodstock according to the procedures described by Cavalli et al. (1997) and Peixoto

et al. (2003). Shrimp were fed twice daily (09:00 and 21:00 h) with commercial pelleted

food (Camaronina Purina, Sao Lourenc�o da Mata, PE, Brazil). Initial feeding rate was 15%

body weight/day, from day 18 through to the end of the experiment this was decreased to

5% body weight/day. Shrimp growth measurements were conducted on D10 (i.e., 10 days

after shrimp stocking), D21, D32, D42, D52 and D63, when 50 shrimp were sampled from

each pen, weighed and returned to the pens. After growth measurements, feeding amounts

were adjusted based on average shrimp body weight. Survival and final biomass were

known at the end of the experiment when all organisms were harvested, counted and

weighed. Temperature and salinity were monitored daily during the culture period.

2.2. Macrobenthos

Macrobenthic fauna sampling began on the first day of the experiment (D0), just prior

to shrimp stocking. Further samples were obtained on D4, D10, D21, D32, D42, D52 and

D63. Three cores of sediment (10 cm diameter, 25 cm deep) were taken from each pen

(fenced areas). Another three cores were taken from adjacent area (outside pens) to

evaluate the organisms occurrence in natural conditions (control). Samples were sieved

through a 300-Am screen to separate macrofauna and detritus from sediment. Samples

were preserved in a 10% formalin solution and stained with Bengal Rose for further

analysis. Organisms were counted and identified using a binocular microscope. Inverte-

brate densities from the three cores per site were pooled and used as an observation

(replicate) in the statistical analysis.

2.3. Sediment

A sediment sample (10 cm diameter, 10 cm deep) was taken from each pen enclosure

and in the adjacent area on the same days as benthos sampling. Samples were dried at 60

jC, sieved through series of screens (500, 250, 125 and 62.5 Am) and weighed. The mud

fraction ( < 62.5 Am) was used for organic matter analysis. Aliquots of mud (2F 0.5 g)

R. Soares et al. / Aquaculture 239 (2004) 199–215202

were weighed, incinerated at 600 jC for 3 h and reweighed. The organic matter content

was estimated by differences in weight before and after incineration.

2.4. Statistical analysis

Statistical analyses were performed with the software Statistica 5.0 version. A two-way

analysis of variance (ANOVA) (local� time) was used to detect differences among locals

(control area, pens with 10 shrimp/m2, pens with 26 shrimp/m2) over time in abundance of

benthic species, shrimp growth and sediment characteristics. Homogeneity of variances

was examined for all data using Cochran’s test. To satisfy the assumptions of normality

and/or homogeneity of variance the following transformations were performed prior to

statistical analysis: shrimp weight (log(x)); survival (arcsin x0.5); abundance of benthic

organisms (log(x + 1)).

3. Results

3.1. Shrimp growth

Average shrimp weight was affect by time and stocking density, higher values were

obtained in the lowest density (Fig. 1). At the end of the experimental period, average

shrimp weight reached 7.1 and 5.4 g in the densities of 10/m2 and 26/m2, respectively.

Survival was not significantly different (P>0.05) between densities, but final biomass was

significantly superior (P < 0.05) in the higher stocking density (Table 1).

Fig. 1. Mean body weight (F S.E.) of F. paulensis reared in pen culture system at two different densities (10 and

26 shrimp/m2) during culture cycle (days). Common superscripts denote non-significant differences ( P >0.05) in

body weight between stocking densities within a sample day.

Table 1

Initial body weight (IW), final body weight (FW), survival (S) and final biomass (FB) of F. paulensis stocked at

densities of 10 and 26 shrimp/m2

Density IW FW S (%) FB (g/m2)

10/m2 0.96F 0.03a 7.11F 0.18a 93.7a 66.74F 2.04a

26/m2 0.90F 0.02a 5.42F 0.09b 94.9a 133.94F 1.57b

Data represent mean values (F S.E.). Common superscripts denote non-significant differences ( P >0.05) between

stocking densities.

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Average temperature and salinity were 23.1 jC (range 17–29 jC) and 5.4x (range

3–9x), respectively. Water temperature decreased during the experiment and salinity

remained low during entire rearing cycle (Fig. 2).

3.2. Macrobenthos

A total of 168 samples were analyzed for composition and abundance of macrobenthos.

Analysis revealed the presence of six major groups: Polychaeta, Tanaidacea, Isopoda,

Gastropoda, Amphipoda and Bivalvia. Within these groups, 11 species were identified and

their percent occurrence within samples were recorded (Table 2).

On the first day (D0 or stocking day), no significant differences (P>0.05) were found

between composition of benthic community in control and fenced areas, mean values

were: Polychaeta 35.4%, Tanaidacea 30%, Isopoda 29.6%, Gastropoda 4.3% and Others

0.7% (Amphipoda +Bivalvia).

Likewise, mean values of total benthos abundance on D0 were similar (P>0.05)

between control and fenced areas. The total abundance was significantly affected by time

of sampling and presence of the pens, but no significant differences (P>0.05) were found

between total benthos abundance in the two shrimp stocking densities during culture

period (Fig. 3). After 10 days of culture, benthos abundance significantly (P < 0.05)

Fig. 2. Daily physical water quality parameters (i.e., temperature and salinity) of shrimp pen enclosures over the

rearing cycle of F. paulensis in Patos Lagoon estuary.

Table 2

Total benthic community composition and percent occurrence (%) of species from samples (n= 168) in control

area and inside pens stocked with 10 and 26 shrimp/m2

Taxa Occurrence (%)

Control 10/m2 26/m2

Polychaeta

Heteromastus similis 100 100 100

Nephtys fluviatilis 100 90.47 87.5

Laeonereis acuta 70.83 71.43 70.83

Tanaidacea

Kalliapseudes schubartii 100 42.86 41.67

Tanais stanfordi 66.67 33.33 25

Isopoda

Munna peterseni 75 47.61 66.67

Cassidinidea fluminensis 25 23.81 33.33

Gastropoda

Heleobia australis 83.33 47.62 37.50

Amphipoda

Melita mangrovi 25 23.81 25

Bivalvia

Erodona mactroides 4.16 0 4.16

Tagelus plebeius 0 4.76 4.16

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dropped inside and outside pens. However, abundance increased again in control areas on

D21 reaching similar values to D0, whereas the abundance inside the pens kept low during

the entire cycle (Fig. 3). On D32 and D52, there were statistical differences between

macrobenthos abundance inside and outside pens (P < 0.05) (Fig. 3).

Fig. 3. Mean values of total benthos abundance (individuals/m2) (� S.E.) during rearing cycle in control and

fenced areas stocked with 10 and 26 shrimp/m2.

Fig. 4. Abundance means (individuals/m2) (�S.E.) of the polychaete species H. similis, L. acuta and N. fluviatilis

during experimental period (days) in control and fenced areas stocked with 10 and 26 shrimp/m2.

R. Soares et al. / Aquaculture 239 (2004) 199–215 205

R. Soares et al. / Aquaculture 239 (2004) 199–215206

The Bivalvia group was not considered for species abundance analysis due to its very

low occurrence and abundance. All other benthos species were analyzed separately and

their abundances were similar between the stocking densities (10 and 26 shrimp/m2).

However, the comparison between abundance in control area and fenced area (pens)

showed differences in several species along the rearing period.

Fig. 5. Abundance means (individuals/m2) (� S.E.) of the Tanaidacea species K. shubartii and T. stanfordi during

experimental period (days) in control and fenced areas stocked with 10 and 26 shrimp/m2.

3.2.1. Polychaete analysis

The polychaete Heteromastus similis occurred in 100% of the samples (Table 2), and it

was the most abundant species reaching densities above 60,000 individual/m2 on D0. Time

and local of sampling were found to affect the abundance of this polychaete. A significant

(P < 0.05) decrease in abundance was recorded on D10 and significant differences between

abundance inside and outside pens (P < 0.05) were detected only on D52 (Fig. 4).

R. Soares et al. / Aquaculture 239 (2004) 199–215 207

Fig. 6. Abundance means (individuals/m2) (� S.E.) of the isopod species C. fluminensis and M. peterseni during

experimental period (days) in control and fenced areas stocked with 10 and 26 shrimp/m2.

R. Soares et al. / Aquaculture 239 (2004) 199–215208

Nephtys fluviatilis abundance was affected by time and local of sampling. During the

first 21 days, the numbers of organisms in control and fenced areas decreased similarly

(Fig. 4). On D32, a peak in N. fluviatilis density was related to natural population

recruitment in control area (90% of juveniles). After D32, abundance in control area

was higher until the end of the experiment, but statistical differences were observed only

on D32 and D52 (P < 0.05) (Fig. 4).

Laeonereis acuta abundance was affect by the time of sampling and became signifi-

cantly (P < 0.05) lower than initial abundance on D32 (Fig. 4). There was no statistical

Fig. 7. Abundance means (individuals/m2) (� S.E.) of the gastropoda and amphipod species H. australis and

M. mangrovi during experimental period (days) in control and fenced areas stocked with 10 and 26 shrimp/m2.

R. Soares et al. / Aquaculture 239 (2004) 199–215 209

difference (P>0.05) between pens and control areas during the entire culture cycle.

Recruitment of juveniles inside the pens resulted in the high abundance observed on D63

(Fig. 4).

3.2.2. Tanaidacea analysis

The tanaids Kalliapseudes schubartii and Tanais stanfordi were affected significantly

by local of sampling but only K. schubartii was affected by time factor. K. schubartii

abundance was significantly reduced (P < 0.05) inside the pens after 21 days, and this

species did not occur in pen samples after D42 (26 shrimp/m2) and D52 (10 shrimp/m2).

Except by a very low abundance registered on D63, T. stanfordi disappeared inside the

pens after D32 (Fig. 5).

3.2.3. Isopoda analysis

The isopods species showed different performances during the culture cycle. The

occurrence of Cassidinidea fluminensis was irregular, and its abundance was not affected

significantly (P>0.05) by time and local sampling (Fig. 6). Munna peterseni occurred

during the entire culture period, and its abundance was affected significantly by time and

local of sampling. The abundance of this species inside the pens tended to be higher in the

beginning of the rearing period but after D10 (26 shrimp/m2) and D21 (10 shrimp/m2), it

dropped significantly (P < 0.05). Significant differences (P < 0.05) in abundance between

control and fenced areas and were recorded only on D32 and D52 (Fig. 6).

3.2.4. Gastropoda and amphipod analysis

The density of the gastropod Heleobia australis was affected significantly by time

and local of sampling. The abundance was higher (P < 0.05) in fenced areas on D0 (Fig.

7). After D4, density significantly (P < 0.05) decreased inside the pens and after D21

became higher in control areas; after D32, the organisms tended to disappear inside pens

(Fig. 7).

Mellita mangrovi did not show any occurrence pattern and its abundance oscillated

among analyzed areas and was not affected significantly by time and local of sampling

(Fig. 7).

Table 3

Percent mean values (F S.E.) of mud and organic matter content (OM) of sediment during experimental period

(days) in control and fenced areas stocked with 10 and 26 shrimp/m2

Days

0 20 30 41 52 61

% mud Control 0.6F 0.5 3.2F 2.2 0.8F 0.6 4.1F 2.5 3.0F 0.2 3.2F 0.7

10/m2 1.2F 0.4 1.7F 0.5 1.5F 0.3 2.5F 0.0 1.6F 3.2 2.9F 1.3

26/m2 1.0F 0.1 1.5F 0.2 2.3F 0.9 4.5F 0.6 2.1F 3.7 1.5F 1.1

% OM Control 2.4F 0.5 0.5F 0.2 2.0F 0.7 0.7F 0.0 1.6F 0.3 0.7F 0.3

10/m2 2.1F 0.5 1.0F 0.4 1.6F 0.3 0.9F 0.3 1.6F 1.1 0.9F 0.3

26/m2 2.2F 0.5 0.8F 0.2 1.0F 0.5 0.8F 0.3 1.7F 0.8 1.2F 0.6

3.3. Mud and organic matter

The mud fraction ( < 62.5 Am) fluctuated during the experimental period in control

and fenced areas without significant differences between sites (P>0.05) (Table 3). Thus,

there was no evident effect of the shrimp pen culture on sediment resuspension and

transport.

The organic content of the sediment changed during the rearing time in all areas, but

there were no significant differences (P>0.05) between control and culture areas (Table 3).

R. Soares et al. / Aquaculture 239 (2004) 199–215210

4. Discussion

4.1. Environmental parameters and shrimp growth

In the Patos Lagoon, estuary-wide and abrupt variations of salinity are usual due to

precipitation and inflow of sea water caused by southern winds. Under these conditions,

growth and survival of shrimp in pen culture systems might be affected by additional

energy requirements for osmoregulation processes (Wasielesky et al., 2000). The high

rainfall rate during the culture period kept mean salinity values low and well below the

values required for best growth. Wasielesky et al. (2000) recorded high survival rates for F.

paulensis reared at salinities from 5x to 40x, but growth tended to be higher between

20x and 30x. The water temperature was within normal levels recommended for F.

paulensis culture (Wasielesky, 2000).

Shrimp growth rates were lower than expected in the present study. Peixoto et al.

(2001) reported final body weights of approximately 11 and 10 g after 63 days using 10

and 25 shrimp/m2, respectively, for F. paulensis pen culture in Patos Lagoon. Similarly, F.

paulensis reached around 7.2 g after 60 days in pen culture with 30 shrimp/m2

(temperature 25.1 jC, salinity 18.2x) (Wasielesky et al., 2001). The lower growth

performance observed in present study might be related to low salinity levels during the

rearing period.

4.2. Natural food

Penaeid shrimps are predators of benthic invertebrates, this has been demonstrated by

analysis of gut contents from different species such as Penaeus esculentus and Penaeus

semisulcatus (Wassenberg and Hill, 1987), Farfantepenaeus aztecus (McTigue and

Zimmerman, 1998), Farfantepenaeus duorarum (Nelson and Capone, 1990), Farfante-

penaeus subtilis (Nunes et al., 1997), Penaeus monodon (Focken et al., 1998) and F.

paulensis (Asmus, 1984; Silva and D’Incao, 2001).

Regardless of the direct predatory action of shrimps on benthic invertebrates, they may

also disturb the substrate searching for food and burrowing themselves. Nevertheless, to

distinguish these two features (predation and disturbance), it would be necessary to

perform separate laboratory experiments. Thus, this study did not determine whether

observed reductions in benthos abundance were a consequence of predation and/or

disturbance.

R. Soares et al. / Aquaculture 239 (2004) 199–215 211

Previous studies observed that in semi-intensive pond culture of Marsupenaeus

japonicus (Reymond and Langardere, 1990) and F. subtilis (Nunes et al., 1997) benthic

prey were the major food source despite inputs of commercial feed. In shrimp ponds with

low stocking densities ( < 10/m2) natural food could sustain shrimp growth for several

weeks with small or no supplementary feed input (Rubright et al., 1981; Wyban et al.,

1987; Lanari et al., 1989).

Benthic invertebrates density generally decrease to a low level after approximately

8 weeks in intensive culture ponds, which has been associated with natural population

fluctuation, predation and pond bottom deterioration (Allan et al., 1995; Shishehchian and

Yusoff, 1999; Shishehchian et al., 2001). Similarly, the present study indicated that the total

benthos abundance inside pens reduced approximately 86% after 21 days of culture. As the

benthic fauna availability decreases as shrimp stocking density and grazing pressure

increases (Maguire and Leedow, 1983; Ordner and Lawrence, 1987; Allan and Maguire,

1992; Nunes and Parsons, 2000), a faster reduction in abundance of benthic invertebrates

should be expected inside the pens with higher stocking density, but there were no

differences between densities used in the present study. This probably reflects an increase

in the grazing rates due to the larger body sizes attained in the lower stocking density. It is

suggested that the higher density tested could be used for shrimp pen culture in Patos

Lagoon estuary as the lower density caused similar impacts on the benthic community.

Notable declines occurred in density of macrofauna living inside pens in contrast with

natural habitat. Benthos abundance in control area fluctuated during the experiment, but

after 21 days of culture, it became higher than inside the pens and remained higher until

the end of rearing period. Bemvenuti (1987), working in the same experimental area,

determined that main predators of macrobenthos invertebrates are fishes (four species),

crabs (two species) and shrimp (F. paulensis), especially during the summer when high

recruitments usually occur. Additionally, the author documented three dominant macro-

benthic species (K. schubartii, H. similis and N. fluviatilis) showing highest densities

during summer and early autumn, whereas epifaunal peracarids were more abundant

during autumn and winter when density of predators were reduced. Despite the presence of

other predators in natural habitat, the predation pressure inside pens was probably higher

due to the elevated density of F. paulensis in the fenced areas.

Macrobenthic species recorded during this experiment showed different responses to

the presence of the culture system. Since many estuarine benthic invertebrates are

frequently patchily distributed, high variances tend to be associated with estimates of

their natural densities, often making it difficult to detect experimentally induced changes in

density with statistical precision (Nelson, 1981; Kneib, 1985). This is the probable reason

why noticeable differences in abundance of some species did not differ significantly

between control and fenced areas.

4.2.1. Polychaetes

The densities of N. fluviatilis and H. similis recorded in the present study were similar

to the densities previously observed in Patos Lagoon estuary of 1000 and 5000

individuals/m2, respectively (Bemvenuti, 1997). The polychaete H. similis is a sedentary

deposit feeder and deep burrower living at depths up to 15 cm, hence promoting protection

against predation by epifaunal organisms like F. paulensis (Bemvenuti,1988). Likewise

R. Soares et al. / Aquaculture 239 (2004) 199–215212

Heteromastus filiformis appeared not to be consumed by shrimps, crabs or fishes, and

therefore is not strongly regulated by predation (Reise, 1979; Virnstein, 1979). The

abundance of H. similis inside pens after D21 tended to be lower than control areas, which

could be associated with shrimp perturbation or impact by the infaunal predator N.

fluviatilis (Bemvenuti, 1994).

N. fluviatilis is not a deep burrower and moves vigorously inside sediment feeding on

meiofauna and deposited material, this species is frequently recorded in gut contents of

fishes and crustaceans captured in Patos Lagoon estuary (Bemvenuti, 1988). Accordingly,

this polychaete species tended to be less abundant inside the pens after D21 as shrimps

probably attained sufficient body size to handle with a large preys like N. fluviatilis.

Adults of the deposit feeder L. acuta are deep burrowers (20 cm), but juveniles keep on

substrate surface and are exposed to intense predation (Bemvenuti, 1992, 1997). Although

this polychaete can reach high densities (5127 individuals/m2) and biomass (28.26 g/m2)

in Patos Lagoon estuary (Bemvenuti, 1997), in this present study, lower densities were

observed. This species has been found in gut contents of captured F. paulensis in Patos

Lagoon (Asmus, 1984; Silva and D’Incao, 2001) and predation probably occurred inside

pens but the effect of shrimp culture on L. acuta was not evident.

4.2.2. Tanaidacea

K. schubartii is a suspension feeder and inhabits U-shaped tubes, whereas T. stanfordi

is an epifaunal grazer. Both tanaids species were severely affected by the culture system

and almost disappeared from the sediment inside pens after D32. This fact is probably

related to shrimp predation since tanaids are an integral part of fish and decapods diets and

are exposed to high predation impact in shallow waters on Patos Lagoon estuary

(Bemvenuti, 1987, 1997; Silva and D’Incao, 2001).

4.2.3. Isopods, gastropods and amphipods

These small and slow organisms inhabit sediment surface and are particularly sensitive

to predation specially when there is low vegetation availability (Virnstein, et al. 1984;

Reise, 1985; Bemvenuti, 1987). A negative effect of culture can be observed on H.

australis and M. peterseni abundance, but not for C. fluminensis and M. mangrovi.

Although H. australis and C. fluminensis have been observed in F. paulensis gut contents

(Asmus, 1984; Silva and D’Incao, 2001), C. fluminensis was not severely affected by

predation inside pens probably due to its low occurrence.

4.3. Organic matter

Accumulation of organic matter in shrimp culture ponds is usual and results in active

microbial decomposition, which could lead to oxygen depletion in the sediment. Compar-

ing the organic matter content in sediments from shrimp culture pens and surrounding areas

in Patos Lagoon, Esteves et al. (1999) recorded lower values inside pens due to shrimp

grazing on submersed vegetation. Accordingly, in the present study, there was no increase

in organic matter or mud content in the sediment inside pens. It is suggested that the water

circulation through the pens was adequate to maintain these parameters at similar levels to

those observed in the control area. Cavalli (personal communication), observed in the same

R. Soares et al. / Aquaculture 239 (2004) 199–215 213

experimental area, a water renewal rate from 20.6 to 72.0 times a day in pen enclosures.

Thus, meshes used in the structure of the pens did not represent a major barrier to the water

flow and, consequently, the granulometry of the sediment is not modified.

4.4. Pen culture

F. paulensis pen culture has been analyzed as an alternative for artisanal fishermen,

especially in years when fisheries yields are low. Concerns exist about the consequences

that this system could generate in the natural environment. In the present work, the impact

of shrimp culture on the abundance of macrobenthic invertebrate community was showed,

however, the culture did not modify the sediment properties even in the higher stocking

density. Furthermore, several macrobenthic species analyzed in our study have been

previously found in F. paulensis gut contents suggesting that predation might be the main

impact factor on benthos abundance inside pens. Moreover, shrimp possibly were not so

attracted by the artificial food when prey items were available, this must be considered

when managing feeding to avoid overfeeding and consequent eutrophication in the initial

stage of culture.

Although the potential impact of the pen culture is apparently limited to the fenced area

and restricted to a short period of the year (3–4 months), the increasing of this activity in

the Patos Lagoon estuary must be supervised to avoid exceeding the capacity of this

system to support pen culture. In addition, the present study may contribute to the

development of management strategies for natural food in pen culture systems reducing

the supplemental feed input.

Acknowledgements

We would like to thank the staff from Estac�ao Marinha de Aquacultura who worked in

the shrimp production, pens construction, sampling and experiment maintenance, and the

staff from Laboratorio de Ecologia de Invertebrados Bentonicos for their assistance on the

taxonomic identification of the macrofauna. Thanks to Frank Coman (CSIRO Marine

Research) for his revision and comments on this manuscript. This study was financed by

FAPERGS (Fundac�ao de Amparo a Pesquisa do Estado do Rio Grande do Sul, RS, Brazil).

The first author was supported by a doctorate scholarship from CNPq (Conselho Nacional

de Desenvolvimento Cientıfico e Tecnologico) of the Ministry for Science and Technology

of Brazil.

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