Feeding of Acetes paraguayensis (Nobili)(Decapoda: Sergestidae) from the Parana River, Argentina

Hydrobiologia 493: 1–6, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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Feeding of Acetes paraguayensis (Nobili) (Decapoda: Sergestidae) from the Parana River, Argentina Pablo A. Collins∗ & Veronica Williner ´ J. Maci´a 1933, 3016 Santo Tom´e, Argentina Instituto Nacional de Limnologia, (∗ Author for correspondence) Received 11 October 2001; in revised form 5 August 2002; accepted 11 September 2002

Key words: Acetes, Sergestidae, shrimp, feeding, wetlands, Paran´a River

Abstract Feeding habits of Acetes paraguayensis (Hansen) were studied by examining the stomach content of specimens from two lakes. A. paraguayensis is omnivorous, feeding mainly on members of littoral-benthic and lotic communities. Algae, rotifers and microcrustaceans (copepods and cladocerans) are the more frequent items in the bulk of the stomach content. Oligochaeta and Diptera larvae were an alternative food source when available. Shrimp feeding habits difference between the two lakes may be due to the resource availability. A. paraguayensis are trophic linkers between limnetic and lotic habitats with an important role in the transportation of energy from the floodplain to the principal channel in the Paraná Rivers System.

Introduction Sergestid shrimp are abundant in coastal and marine waters but are exceptional in freshwater environment. There is only one species of Acetes that inhabits Neotropical rivers, that is A. paraguayensis. It is an endemic species of Sergestidae which lives in South America mainly in rivers, lakes or ponds at Paraná and Paraguay rivers and their tributaries and Amazons river (Omori, 1975; Boschi, 1981; Morrone & Lopretto, 1995). Moreover it is the unique species in the Sergestidae family that inhabits freshwater environments (Manning & Hobbs, 1977). This shrimp is a singular member of littoral communities and lotic environment of the Middle Paraná River floodplain; its presence is sporadic during the year. The reasons of the variation have not yet been analysed but they are closely related to migratory events. A. paraguayensis diet has not been studied but Boschi (1981) mentioned its position in the food web of the planktonic community in the Paraná river and made the comment that this shrimp could have a planktonic feeding habit.

This paper reports on the trophic biology of A. paraguayensis with a special emphasis given to the regular patterns of food items occurrence.

Materials and methods The study took place in two lakes, No. 1 Los Sapos Island (meander lake) and Alejandra lake (oxbow lake) located on the floodplain of Paraná River close to Salado River, a tributary, and Coronda River a secondary branch directly connected to the main channel (Santa Fe, Argentina, South America) (Fig. 1). Study area ‘Laguna No. 1’ is an abandoned meander scroll lake (31◦ 39 S; 60◦ 41 W) (Fig. 1) with a 0.55 m average depth during the isolated phase (Collins, unpublished) located close to the Salado river (a river with high dissolved salt contents). Its volume changes depending on the input of water flow from the Salado and Santa Fe rivers. ‘Alejandra’ lake is a shallow lake situated in the floodplain of the Paraná Medio river close to the

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Figure 1. Location of study area.

Coronda river, a secondary branch directly connected to the main channel (31◦ 45 S; 60◦ 31 W) (Fig. 1). This oxbow lake changes its volume depending on the input of water flow from the Coronda River. Its maximum and mean depth is 2 m and 0.66 m, respectively. No. 1 Lake and Alejandra Lake have different Limnological characteristics (Table 1) but the littoral zones for both lakes have a similar floating and emergent flora (Eichhornia crassipes, Hydrocotyle ranunculoides, Nimphoides humboldtiana, Paspalum repens, Salvinia herzogii, Pistia stratiotes and Azolla filiculoides). Method Samples of A. paraguayensis were taken from a limnetic–littoral transitional zone (mid-vegetated and open water zones) during the morning (8–10 am). Populations of A. paraguayensis were collected with a 8 m2 bottom net (1 mm mesh). Samples were preserved in 10% formalin. Juveniles and adults were identified according to presence or absence of secondary character sexual. Cephalothorax lengths (CL) were measured to the nearest 0.01 mm using a calliper under a stereomicroscope and the alimentary tracts were removed. Individual stomach fullness was estimated according to a

subjective scale, ranging from 0 to 5 (empty; less than half stomach with food; half stomach with food; more than half stomach with food; stomach-fullness without its distension; stomach-fullness with distension). The stomachs were opened and their contents extracted and mounted in a drop of glycerol (50%). Food items were sorted to taxonomic groups, measured, and counted under a compound microscope at 150× to 600×. The identified remains were classified into 13 groups (items): unicellular algae, filamentous algae, Bacillariophyceae, pieces or macrophytes, fungi, Protozoa, Rotifera, Cladocera, Copepoda Calanoidea, Copepoda Cyclopoidea, Chironomid larvae, other Insect larvae and Oligochaeta. The subsample for the feeding analyses was defined by the minimum number of specimens (Collins, 1999). This was determined by the mean of cumulative trophic diversity using Shannon–Wiener and Simpson indexes (Legendre & Legendre, 1979) (Fig. 2). The number of specimens for all stomach fullness categories analysed was 20 per lake. Food items volume and potential food organisms were determined by approximation to regular geometric shapes or converting them to volume data of weight from literature (Edmonson & Winberg, 1971; Dumont et al., 1975; Ruttner-Kolisko, 1977).

3 Table 1. Mean values and standard deviation during the samples in ‘No. 1’ and ‘Alejandra’ lakes, Santa Fe, Argentina for water temperature, oxygen, conductivity, pH and Secchi disc Lake

No. 1 Alejandra

Oxygen mg/l

Conductivity uohms/cm

pH

◦C

T

Secchi disc cm

26.0 ± 1.50 25.3 ± 2.05

7.5 ± 1.00 6.5 ± 1.17

3200.0 ± 100.00 161.7 ± 37.04

8.2 ± 0.20 6.8 ± 0.25

10.0 ± 2.29 31.7 ± 14.3

Figure 2. Mean of cumulative trophic diversity calculated after Simpson index (—— ‘No. 1’ lake; - - - - ‘Alejandra’ lake).

Figure 3. Frequency distribution of cephalothorax lengths of Acetes paraguayensis (Black: ‘No. 1’ lake; white: ‘Alejandra’ lake). CL ranged between 2.2 and 7.1; No. 120.

Statistical analysis Cephalothorax length differences of shrimp from the two lakes were analysed with ANOVA (Zar, 1996) Wilcoxon paired–sampled test was used to determine the difference significance in stomach contents between juveniles and adult, from ‘No. 1’ lake and ‘Alejandra’ lake. Variation in stomach fullness was analysed using Friedman ANOVA (Sneath & Sokal, 1973). The most important food items in shrimp for all stomach fullness categories were identified using the Index of Relative Importance, IRI = (Cv + Cn ) x Fo (Pinkas et al., 1971), where Cv is the volumetric content of prey, Cn is the numeric content of prey, and Fo is the frequency a prey item occurred.

Results A. paraguayensis densities observed in ‘No. 1’ and ‘Alejandra’ lakes were 41.6 ± 3.18 ind./m3and 37.0 ± 2.9 ind./m3 , respectively. Shrimp size (CL) ranged from 2.2 to 7.1 mm in ‘No. 1’ lake and 2.6 to 6.6 mm in ‘Alejandra’ lake. CL mean did not vary

Figure 4. Percentage of male and female shrimps at the both lakes. (White: males, black: females) (No. 120).

between the sergestid shrimps samples from both lakes (ANOVA, F(120,2,0.05): 0.48, p = 0.4895) (Fig. 3). Males/females ratios were 0.92 and 1.27 in each pond, respectively (Fig. 4). High categories of stomach fullness (3,4, plus 5) were dominant, from 75% and 70% of total shrimp (Fig. 5). Empty stomachs were not observed. Fullness index variation was not statistically significant among

4 Table 2. List of food items recorded in A. paraguayensis from ‘No. 1’ lake (A) and ‘Alejandra’ (B) lake Items

Figure 5. Stomach filling index of Acetes paraguayensis. Ranging from 0 (empty) to 5 (stomach fully distended with food). (No. 120).

the shrimps from both lakes (χ r 2 (0.05,2,5): 7.4, p > 0.05). In A. paraguayensis, algae, rotifers and microcrustaceans (Cladocera, principally) (Table 2) were the most frequently eaten prey in the lakes but they did not contribute in great volume to the diet (Fig. 6). Among microcrustaceans, Cladocera was the most frequently eaten prey (45% in ‘No. 1’ and ‘Alejandra’ lakes) being the second in volumetric importance (14.6% and 14.9%, respectively). When Chironomid larvae were present, they contributed to the largest volume of the diet (Fig. 6). The remaining items consisted of mains of macrophyte, fungi, Protozoa, other larvae insects and Oligochaeta (Table 2). Sand (mainly) and unidentified organic matter formed a high proportion of the stomach volume. Diet composition of juveniles and adults was not significantly different (Table 3). However, it differed significantly among shrimps from ‘No. 1’ and ‘Alejandra lakes’ (T (0.05,2,13): 0.666, p > 0.05). Major differences corresponded to the presence of filamentous or unicellular algae, the former was more recurrent in stomachs from ‘No. 1’ lake and the latter in stomach contents from ‘Alejandra’ Lake (Table 2; Fig. 6).

Discussion A. paraguayensis is omnivorous, grazing the phytoplankton (Ankistrodemus sp., Oedogonium sp., Bulbo-

ALGAE Cyanophyceae Rivularia sp. Hapalosiphon sp. Euclorophyceae Ankistrodesmus sp. Rizoclonium sp. Carteria sp. Chlamydomonas sp. Chlorogonium sp. Euglenophyceae Phacus sp. Zygophyceae Closterium sp. Bacillariophyceae Diatoma sp. Navicula sp. Diatomella sp. Gomphonema sp. Synedra sp. Desmidiaceae Micrasterias sp. Closterium sp. Ulotricophyceae Oedogonium sp. Bulbochaeta sp. Microsporas sp. HYPHOMICETES VEGETAL REMAINS SAND UNIDENTIFIED ORGANIC MATTER

A

B

Items

X X X X X X

X X X

PROTOZOA Rhizopoda Arcella sp. Diflugia sp. Actinopoda Chaos sp. Chlamidaster sp. ROTIFERA Lecane sp. Brachionus sp. Keratella sp. Polyarthra sp. Proales sp. Bdelloidea OLIGOCHAETA CRUSTACEA Cladocera Diaphanosoma birgei Bosminopsis sp. Bosmina sp. Ilyocryptus spiniger Macrothrix sp. Chydorus pubescens Camptocercus sarsi Camptocercus sp. Copepoda Cyclopoida Copepoda Calanoida INSECTA (larvae) Diptera Chironomus sp.

X

X

Others Insecta larvae

X X

X

X

X X X X X X X X X

X

X

X X X X X X X

X

A

B

X X

X

X X X X X X X X X

X X X X X X X X X

X X X X X

X X X X

X

X

X

X

X

chaeta sp., Navicula sp., mainly) and predates rotifers (Keratella sp., Brachionus sp., Lecane sp.) and microcrustaceans (Macrotrix sp., Camptocercus sp., Bosmina sp.) which are the predominant animal item. This trophic spectrum agrees with that recorded by Figueras (1986) who showed that algae and small crustaceans are the most important food resource for Palaemon adspersus and P. serratus. Kensley & Walker (1982) mentioned the same observations in Pseudopalaemon chryseus and P. amazoniensis from the Amazon basin. Other items such as Chironomid larvae and Oligochaeta are consumed when available. Moreover this fact may probably explain changes in the diet (Guerao, 1994). Two prawns of the Paraná River, Macrobrachium borellii and Palaemonetes argentinus, were determined to be omnivorous but the animal elements from the littoral – benthic communities are more frequent

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Figure 6. Index of relative importance (IRI) of major food items found in Acetes paraguayensis (No. 40). Vertical scale indicates numerical composition (upper panel) and volumetric composition (bottom panel). Numbers indicate values of IRI (upper panel), and frequency of occurrence (bottom panel). Table 3. Wilcoxon paired-sample test applied to the juveniles and adults data of Acetes paraguayensis

No. 1 lake Alejandra lake Total

Number

Juveniles (LC 2.2–4.0 mm)(%) (%)

Adults (LC 4.0–7.1 mm) (%)

T(0.05,2,13)

p-value

20 20 40

30 40 35

70 60 65

21 11 15

0.938 0.852 0.918

and important (Collins & Paggi, 1998; Collins, 1999). In the same position several species of prawn from Amazon river such as M. inpa, M. nattereri (Kens-

ley & Walker, 1982) were recognised but the authors mentioned that these species are also scavengers. According to the observations done in A. paraguayensis and the marine congeneric shrimp A.

6 siboga australis (Mcleay & Alexander, 1998) they showed the use of four principal feeding modes to capture a wide size range of prey as an opportunistic feeder mechanisms. Diets of sergestid shrimp populations at both lakes were composed by elements recognised as integrating the littoral – benthic communities (Paggi, 1980; Paporello de Amsler, 1987; Paggi & José de Paggi, 1990; Poi de Neiff & Carignan, 1997) and lotic communities (Paggi & José de Paggi, 1974; Paggi, 1975; José de Paggi, 1980, 1981). Unicellular and filamentous algae are the main food resource indicating some preference for them. Differences in A. paraguayensis diet at ‘No. 1’ and ‘Alejandra’ lakes were mainly in the proportion of unicellular and filamentous algae which may be due to the resource availability in each lake. Summarising, stomach contents of A. paraguayensis indicate that this species feeds on a variety of items from littoral and lotic environment. The shrimps are trophic linkers between limnetic and lotic habitat. Within the Paraná River, it has an important trophic role in the transportation of energy to a higher consumer level and from the lake, ponds (floodplain) to river (principal channel). Some works (Pringle et al., 1993; Pringle, 1996) mention that decapod crustaceans such as omnivorous and detritivorous shrimps were dominant faunal components of many tropical streams, but their role as organisers of lotic community structures remains relatively unexplored.

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