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Pavés, Héctor; Pequeño, Germán; Bertrán, Carlos; Vargas, Luis

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120

MAR 2005, VOL. 30 Nº 3

Keywords: /

Eleginops /

Eleginopidae / Feeding Shifts / Osmoregulation / South America /

5 Las oro Plata PU 2 EU34 Plano CN33 4 US4 UK2 Casual verano talón mujeres de Otros sandalias Otros Confort 5 Received: 05/10/2004. Modified: 01/11/2005. Accepted: 02/04/2005.

Héctor Pavés.

Marine Biologist and Doctoral Student, Universidad Austral de Chile (UACh).

Germán Pequeño.

Ph.D., Oregon State University, USA. Professor, Instituto de Zoología

“Ernst F. Kilian”, Universidad Austral de Chile. Address: Casilla 567, Valdivia, Chile. e-mail: gpequeno@uach.cl

Carlos Bertrán.

M.Sc., UACh. Doctor, Universidad de Concepción, Chile. Professor, UACh.

Luis Vargas.

Marine Biologist, UACh. Doctoral Student, Universidad de Cadiz, Spain.

LIMNETIC FEEDING IN

Eleginops maclovinus

(VALENCIENNES, 1830)

IN THE VALDIVIA RIVER, CHILE

HÉCTOR PAVÉS, GERMÁN PEQUEÑO,

CARLOS BERTRÁN and LUIS VARGAS

leginops maclovinus

, Va-

lenciennes, 1830 is a

monotypic species of the

family Eleginopidae (Osteichthyes), sub-

order Notothenioidei. The species is

thought to be of Antarctic evolutionary

origin, and is one of the most euryther-

mic, euryhaline and stenobathic represen-

tative of the suborder (Pequeño, 1989).

This species is endemic to southern

Chile, southern Argentina and the Mal-

vinas Islands, where it occurs near oce-

anic beaches, and in large and small estu-

aries. In Chile it is found south of the

Aconcagua River (33ºS) and has been

caught in rivers of southern Chile, several

kilometers offshore of the river mouths

(eg. Valdivia River, this study), and over

20km upstream in low salinity (limnetic)

waters.

Previous observations of

the trophic relations of

E. maclovinus

had

been made on specimens obtained in ma-

rine and estuarine habitats. Although this

species has been generally considered as

an omnivorous predator, the literature re-

flects two contrasting variations on this

point, the first by Guzmán and Cam-

podónico (1973) and Gosztonyi (1979),

who postulated an ontogenetic change

from carnivorous behavior in early juve-

nile stages to a herbivorous one in adults.

The second opinion, held by Pequeño

(1979) and Turner (1988) is that the spe-

cies tended toward a carnivorous behavior

0378-1844/05/03/120-06 $ 3. 00/0

throughout its entire ontogenetic develop-

ment.

In the present study the

trophic relations between juveniles and

adults of

E. maclovinus

within a limnetic

habitat, namely the upper Valdivia River

estuary, are compared. It was also tested

whether

E. maclovinus

, the notothenioid

species that most commonly inhabits

fresh waters, preys upon typical freshwa-

ter species during its residence in this

habitat, and remains carnivorous as ob-

served in specimens studied from brack-

ish and marine waters. Parasitological

evidence obtained from the stomachs of

the fish is also used to evaluate the hy-

pothesis of carnivorous tendency in both

juveniles and adults of this species.

Materials and Methods

Sample collection

Samples of

E. maclovi-

nus

included 114 individuals obtained us-

ing a 1.75×30m gillnet with 32mm open-

ings. Catches were made from 17 to 20

March 2002, at Las Mulatas (39º50'S,

73º15'W), at a distance of about 16km

upstream from the Pacific Ocean, in the

Valdivia River estuary (Figure 1). Tidal

movement in this estuary takes place to

about 20km inland of the river's mouth,

and limits of salt water (salinity= 0.1‰)

reach about 14km inland. All the speci-

mens were measured for total length (TL,

live) and standard length (SL) using a

ruler graduated in millimeters. Weights

were obtained using a field balance

graduated to 0.1g. At the laboratory, the

fishes were initially fixed in 10% river

water formalin for 48h and stored in 70%

ETOH. The stomachs were removed from

each specimen and stored separately for

subsequent contents analysis.

Collection of bottom samples

Sampling of the bottom

fauna of the Valdivia River was carried

out at two stations, including Las Mulatas

and Los Pelúes (Figure 1). At each sta-

tion samples were obtained both near the

EU34 US4 5 Confort Plano 5 Casual Plata Otros Otros de 4 mujeres oro talón Las verano 2 UK2 PU sandalias CN33 shore and at its deepest point, using cor-

ers hand-held by divers. Four replicate

samples were obtained at each sampling

point. These samples were collected on

the same dates as the fishes were.

Macrofauna were ini-

tially separated from the sediments using

a 0.5mm screen, fixed in 10% formalin,

and stored in 70% ETOH. These speci-

mens were subsequently separated under

a stereomicroscope and identified to the

closest possible taxonomic species level

using specialized keys. The species rich-

ness and relative abundance were deter-

mined on each of the samples (Morin,

1999). The samples were finally dried at

60ºC for 48h and weighed to determine

MAR 2005, VOL. 30 Nº 3

121

the approximate biomass per species in

each sample.

Stomach contents analysis

The determination of

stomach contents was made using a ste-

reomicroscope, aided by specialized

taxonomic identification keys (Stuardo,

1961; Yamaguti, 1961; Menzies, 1962;

Retamal, 1981), as well as with the aid

from the specialists from the Institutes

of Zoology and Botany at the Univer-

sidad Austral de Chile. The individuals

from the identified taxa were counted to

obtain the frequency distributions of spe-

cies and proportions of individual taxa

in each analyzed stomach (F: frequency

of occurrence per number of stomachs;

F%: frequency of occurrence expressed

in proportions of stomachs). The abun-

dance of prey items found indicated the

number of individuals of a given taxon

registered in all the samples analyzed

(N: abundance expressed per number of

individuals; N%: abundance expressed in

percentage of individuals).

Results

A total of 114 speci-

mens of

E. maclovinus

were obtained in

the samplings. These had a mean total

length (live) of 26.7cm (18-42cm, sd=

4.6cm) and a mean weight (live) of

224.9g (75-800g, sd= 146.7g). Most

specimens were immature males of 2-4

years of age (Gosztonyi, 1974; Calvo,

., 1992). The by-catch obtained in

sampling for

E. maclovinus

included the

salmoniformes

Oncorhynchus

mykiss

(exotic, introduced),

Galaxias maculatus

and

G. platei

, the smelts

Austromenidia

laticlava

and

Basilichthys

australis

(Atherinopsidae), and the cosmopolitan

mullet

Mugil cephalus

(Mugilidae).

Of all the

E. maclovinus

stomach samples, 103 (90%) could be

analyzed, while the remainder (11) were

in a degraded condition. The analyzed

specimens had mean total length (fixed)

of 25.0cm (18-40.1cm, sd= 3.3cm) and

their mean standard length was 22.0 cm

(15.5-30.2cm, sd= 2.8cm).

Almost all the samples

from which the complete digestive tract

could be extracted (93%, n=96) had

stomach contents present. In these it was

possible to identify species or high taxo-

nomic levels of plant and animal re-

mains. Only 7 (7%) of the stomachs

were empty. A total of 55 (53%) stom-

achs analyzed contained nematode para-

sites.

The analysis of the

stomach contents revealed a broad range

of food items, accompanied by appre-

ciable amounts of detritus such as sand

and rock grains (

. schist, mica). Items

observed included algae, plant material,

gastropods, crustaceans, insects, and

fishes, mostly of estuarine or lacustrine

origin. Of the analyzed stomachs, 96

(93%) contained animal remains, and 89

(84%) contained plant remains (Table I).

The highest frequency group on the

TABLE I

FREQUENCY OF OCCURRENCE IN RELATION TO TOTAL NUMBER OF

STOMACHS ANALYZED (F, F%) AND NUMBER OF ITEMS (N, N%) IN THE

STOMACH CONTENTS OF

Eleginops maclovinus

IN THE VALDIVIA RIVER

Taxa

Crustacea

93.20

Corophiidae (Amphipoda)

59246

97.148

93.20

Tanaidacea (Malacostraca)

104

0.171

13.59

Ciprinidae (Ostracoda)

0.033

9.71

Hemigrapsus crenulatum

0.008

4.85

Idotheinae (Valvifera)

0.005

2.91

Zoea larvae

0.002

0.97

Gastropoda

19.42

Littoridina comingii

0.033

18.45

Bivalvia larvae

0.002

0.97

Insecta

69.90

Chironominae (Diptera:Chironomidae)

918

1.505

67.96

Hygrobatidae (Acarii)

0.003

1.94

Trichoptera (Tubo)

0.003

1.94

Inderminate

0.007

2.91

Teleostei

CN33 EU34 sandalias Casual talón 4 2 oro Otros Plano verano de UK2 5 Plata Las Confort US4 5 PU Otros mujeres 1

0.97

Inderminate

0.002

0.97

Bryozoa

78.64

Indet. ovoid structures

519

0.851

55.34

Filaments

42.72

Plants

46.60

Scirpus californicus

(Cyperaceae)*

139

0.228

28.16

Inderminate

44.66

TOTAL

60985

103

* Seeds

sandalias pescado astilleros boca alto Cómodo femenino con de gruesas tacón de flores grandes dulce blue 4HzA7xw

Figure 1. Geographic location of sampling stations, within the estuarine system of the

Valdivia River, Chile. a: Las Mulatas, b: Los Pelúes.

122

MAR 2005, VOL. 30 Nº 3

stomachs (F%) were the crustaceans

(93.2%), followed by ramose bryozoans

(78.64%), insects (69.9%), lake plants

(46.6%), gastropods (19.42%) and, fi-

nally, a bony fish (0.97%, Table I). In

relation to the number of individuals per

group (N%) the class Crustacea repre-

sented 97%, followed by Insecta (1.5%)

and bryozoans, lake plants, gastropods

and Teleostei, each at proportions below

1% (Table I). A grand total of 98.9%

(N, N%) of the items recorded in the

stomachs were of animal origin, with

less than 1.1% of plant origin.

Taxonomic analysis of the stomach

contents by systematic group

Statistically

significant

differences were observed among the

abundances (N) of the different food

items analyzed (Kruskal-Wallis test:

H(15, N=1599)= 949.94 p<0.01).

The taxa showing the

statistically greatest abundances were 1)

the corophiid amphipods (mostly

Para-

corophium hartmannorum

), 2) Diptera:

Chironomidae, 3) bryozoans, and 4) lake

plants (Multiple Comparison Kruskal-

Wallis test, p<0.01). Each of the preced-

ing groups demonstrated absolute, el-

evated abundances, and distinct tenden-

cies among themselves (Table I).

1) Class Crustacea: In this group the

main taxon in numerical abundance

(N%) as well as in frequency of occur-

rence in stomachs (F%) was shown by

the lacustrine amphipod

Paracorophium

hartmannorum

oro de UK2 PU 5 5 mujeres Otros Casual US4 4 sandalias Otros EU34 Plano verano Las 2 CN33 Confort talón Plata which

represented

97% of the individual prey species,

and was found in 93.2% of the stom-

achs analyzed (Table I). Other crusta-

cean items included Tanaidacea (Ma-

lacostraca), Ciprinidae (Ostracoda),

Hemigrapsus crenulatus

(Decapoda),

and Idotheinae (Isopoda, Valvifera)

which as a group represented less than

1% of the total individuals counted.

The tanaids, ciprinids, and

H. crenu-

latus

gave frequencies of occurrence of

between 2.9 and 13.5%. Finally, a bra-

chyuran zoea larva was encountered,

representing less than 1% both in abun-

dance and frequency.

2) Class Mollusca: Only one species of

gastropod,

Littorina cumingii

g Suave Espuma Mujer Zapatillas piscina Home baño ducha Sandalias YMFIE antislittamento zapatos de Suela FZ6qxxO

, was re-

corded, which had a frequency of occur-

rence of near 18.4%, and an abundance

of less than 1%. A few bivalve veliger

larvae were also observed.

3) Class Insecta: The most important

taxon of this group were Diptera of the

family Chironomidae, with an abundance

of 1.5%, and a frequency of occurrence

of 67.9%, making it the second most

common item eaten by the fish. Also

identified were trichopteran tubes and a

hygrobatid mite, representing less than

1% in abundance and 1.9% in frequency

of occurrence.

4) Subdivision Teleostei: Only one indi-

vidual was recorded, and this was in an

advanced stage of digestion, remaining

unidentified. This represented less than

1% in frequency of occurrence and

abundance among the items analyzed.

5) Ramose invertebrates: Due to their

advanced state of digestion, specific

identification of this material was im-

possible, although its tubular structure,

dichotomous ramification and presence

of ovoidal structures in the external

walls suggested it to be assigned to

“bryozoa”. These remains were found in

78.64% of the stomachs, but with an

abundance near 1%. Quantification of

this material was difficult due to clump-

ing, but undoubtedly represented a fre-

quent item in the stomachs of

maclovinus

6) Lacustrine plants: 46.6% of the

stomachs contained remains of lake

plants, including both vegetal portions

and seeds: the latter were determined

to be seeds of

Scirpus californicus

(Cyperaceae) and had a frequency of oc-

currence of 28.1% and an abundance of

less than 1% (Table I; Ramírez

et al

1976).

7) Nematode parasites (Table II): The

main nematode parasite in the stomachs

of the fish was

verano Otros talón mujeres CN33 5 oro 4 sandalias de US4 UK2 2 Plano Casual Plata Las PU 5 Otros Confort EU34 Ascarophis

sp. (Cystido-

colidae), with both mature males and fe-

males present. This nematode had a fre-

quency of 44.6% and an abundance of

75.7% (n= 87), and was the most nu-

merous of the helminths identified. Also

identified from the stomachs were ma-

TABLE II

FREQUENCY OF OCURRENCE (F, F%) AND NUMBER OF PARASITE

NEMATODS (N, N%) IDENTIFIED WITHIN THE STOMACH CONTENTS

Eleginops maclovinus

IN THE VALDIVIA RIVER

Parasites

N(%)

F (%)

Ascarophis

spp. (Cystidicolidae)

75.7

68.7

Anisakids

24.3

31.3

Total

115

100

Figure 2. Variation in the stomach contents of

Eleginops maclovinus

. a: common items,

b: less common items (lower occurrence and presence).

MAR 2005, VOL. 30 Nº 3

123

ture anisakids, at a frequency of 20.3%.

This group included 15 larvae and 13

adults.

Analysis by size of fish

When the fish samples

were separated into size ranges of 1cm,

to give 13 ranges between 15 and 30cm

TL, no statistically significant differences

were observed in total species abundance

in stomachs from the different size

groups (Kruskal-Wallis test H(12, N=

1599)= 19.21559, p>0.05). However, a

decrease in abundance of the Coro-

phiidae, lacustrine plants (

S. californicus

bryozoan remains, Chironomidae, and Os-

tracoda was observed as total length of

the fishes increased (Figures 2a, b). In

contrast, the Idotheidae,

H. crenulatus

one teleost, and

Unisex Ciclismo de Whisper Negro Catlike Adulto 000 de MTB EU Montaña Zapatillas Azul 45 Negro 2016 4a8RW

L. cumingii

were re-

corded in specimens over 19cm SL, and

increasing in the larger

E. maclovinus

(Figure 2b).

With the nematode para-

sites, greater numbers of anisakids were

found in the smaller fish specimens, con-

trary to the numbers of ascarophites

which were more common in the larger

fishes.

Comparison of the fish stomach

contents and river fauna

Items found in the

maclovinus

stomachs were common at

both stations sampled in the Valdivia

River,

including

hartmannorum

Otros Casual de Las CN33 US4 Plata sandalias EU34 Confort 2 verano Otros PU oro mujeres UK2 5 talón 4 5 Plano ,

Chironomidae, and Trichoptera. (Tables

II, III). There was, however, variation in

abundance and diversity of the four taxa

in relation to the sampling depth in the

river (shore

. depth). Amphipods were

more abundant in shore samples at Las

Mulatas. In mid-river, the polychaetes

Prionospio

sp. and

P. gualpensis

were

more abundant, although they were not

recovered from the stomach contents of

the fish. Lower abundance and biomass

were found at Los Pelúes than at Las

Mulatas, where the oligochaete

Tubifex

sp. inhabited anoxic bottoms rich in or-

ganic matter. This species was not re-

covered from fish stomachs. Thus, some

of the potential preys are not used by

the fishes.

Discussion

Among the large variety

of food items present in the stomach

contents of

E. maclovinus

we found re-

mains of algae, land plants, crustaceans,

insects, mollusks and fishes.

The item with the high-

est frequency of occurrence was

Para-

corophium

hartmannorum

somewhat

similar to that recorded by Pequeño

(1979). It should be noted that Pequeño

(1979) considered specimens between

280 and 880mm TL, to be inhabitants of

marine or mixohaline habitats. In the

present study samples obtained were be-

tween 180 and 400mm TL, and distrib-

uted in areas of strong limnetic affinity

and low salinity (Valdivia River surface

salinity= 0‰, bottom salinity= 5‰;

Wladimir Steffen, personal communica-

tion).

The Las Mulatas station

is at the limit of effect of the estuarine

salt wedge in the Valdivia River estuary,

with freshwater occurring to the head of

the estuary, and tidal motion noted up to

20km inland from the mouth of the estu-

ary (Pers. Comm. Wladimir Steffen).

The

majority

samples

maclovinus

having stomach contents

sandalias Plano de UK2 US4 4 PU Confort mujeres 2 Las CN33 5 Otros 5 oro Plata verano Casual EU34 Otros talón (93%), the low degree of digestion of

the prey, and the similarities between

species ingested and those recorded

from the environment, allow the assump-

tion that Las Mulatas is a feeding area

used by the fishes to exploit resources

located near the rivers edge (Table I,

III).

Various species of poly-

chaetes, including

Perinereis gualpensis

and

Prionospio

were found in the

sediment, but not among the stomach

contents although other investigators re-

corded the presence of polychaete re-

mains as well as remains of the oli-

gochaete

Tubifex

sp. (Ruiz, 1993). This

situation may be explained by the life

style of these annelids (buried, as

endofauna), and with soft body struc-

tures which are easily digested, imped-

ing their identification in the stomachs.

Another possibility is that they may be

negatively selected by the fish, based on

its feeding behavior which includes

grazing over sand or gravel, not appear-

ing to consume species which are in

lime-clay sediments containing decom-

posing organic material as typical of

Prionospio

sp. and

P. gualpensis

. This

situation would reflect a selective behav-

4 sandalias 5 2 Plata UK2 US4 Plano 5 de EU34 talón oro verano CN33 Las mujeres Casual Otros Otros PU Confort ior toward species which inhabit gravel

and sandy areas, or in association with

small filamentous algae where benthic

grazing behavior is possible (

. Tri-

choptera, Chironomidae, and

P. hartman-

norum

). The fish may be an opportunis-

tic predator (Morin, 1999) since it ex-

ploits the resource in major abundance

in the environment (

eg. P. hartman-

norum

The remains assigned to

bryozoa and lacustrine plants observed

in the stomach contents of

E. maclovinus

probably represent items accidentally

consumed during feeding on crustaceans

and/or insects due to the common be-

havior arthropods such as the amphi-

pods, isopods and insects in seeking ref-

uge in filamentous microhabitats such as

algae and other plants, reducing predator

pressure and indirectly increasing the

food offering of the substrate (Schneider

and Mann 1991a, b; Peñaloza, 1993).

Another aspect suggesting the accidental

nature of consumption of the bryozoans

was the low degree of digestion of this

material in the fish stomachs. The same

occurred for

Scirpus

californicus

, where

accidental ingestion of the seeds may be

related to sedimentary grazing on animal

prey, particularly the chironomids. The

accidental consumption of seeds may

lead to probable “ichthyochoria” or seed

dispersal by fishes as found in the Ama-

zon by Gottsberger (1978). This was

also noted by Guzmán and Campodónico

TABLE III

ABUNDANCE AND BIOMASS OF MACROBENTHOS SPECIES IN SECTORS*

OF LOS PELÚES AND LAS MULATAS AT THE VALDIVIA RIVER

Los Pelúes margin

Los Pelúes center

Taxa

Abundance /

Biomass

verano mujeres 5 de EU34 Plata CN33 oro sandalias talón Otros UK2 5 Confort 4 2 Plano Otros US4 Las Casual PU Abundance /

Biomass

(gr/m

)

Prionospio

sp.

63.14

0.006

357.77

0.08

Perinereis gualpensis

168.36

0.59

631.36

1.30

Paracorophium hartmanorum

841.81

0.07

2209.75

0.27

Tubifex

sp.

168.36

0.010

21.04

0.002

Las Mulatas margin

Las Mulatas center

Prionospio

sp.

105.23

0.019

3556.65

0.85

Perinereis gualpensis

526.13

0.73

1452.12

1.85

Paracorophium hartmanorum

2336.02

0.24

589.27

0.06

Trichoptera

21.04

0.09

Chironomidae

21.04

0.006

* The sectors are differentiated according to sampling locations, margin or center.

124

MAR 2005, VOL. 30 Nº 3

(1973) who reported seeds of graminea

E. maclovinus

stomach contents.

The

crustaceans,

in-

sects, and plants observed in the stom-

ach contents in this study, have only

been reported from limnetic or estua-

rine environments (see Stuardo, 1961;

Ramírez

et al

., 1976; Pequeño, 1979;

Artigas

et al

., 1985; Jaramillo

et al

1985; Bertrán, 1989; Ruiz, 1993). This

suggested that the fishes sampled had

not migrated into brackish (Corral Bay,

9.2‰ surface, 33.7‰ bottom salinity)

or marine areas to feed, but rather con-

sumed prey from freshwater, upper

reaches of the river (0‰). This capacity

for tolerating low salinity and feeding

on limnetic species explains catches of

these fishes to more than 21km inland

from the mouth of the Valdivia River.

This aspect is corroborated by the lim-

netic fish fauna associated with the ar-

eas from which present samples were

obtained, such as

Austromenidia laticla-

via, Basilichthys australis, Oncorhyn-

chus mykiss, Mugil cephalus, Galaxias

maculatus, G. platei, Cheirodon

sp.

(Ruiz, 1993; Vila

et al.

, 1999). Of these

only

M. cephalus

is capable of life both

in the sea and in freshwater (Ruiz,

1993).

It has been recognized

that freshwater fishes have a diet simi-

lar to that of

E. maclovinus

in this

study in these habitats. Thus

Oncorhyn-

chus mykiss

and

Cauque mauleanum

feed principally on chironomid larvae

and pupae, Littorinidae, Trichopteridae,

Acarii, and Amphipoda (Artigas

et al.

1985; Klink and Eckmann, 1985).

The data showing that

as the fishes grew in size and weight,

corophiid

crustaceans

(

hartman-

norum

) significantly decreased in the

stomach contents, as also found with

the ostracods, suggested a succession of

species taken by

E. maclovinus

with in-

crease in size, where smaller prey items

are progressively replaced by larger

ones. In spite of these changes in pre-

dation, the fish was observed to be

more of a carnivore than herbivore, in

agreement with Pequeño (1979), Turner

Summer ZHZNVX Canvas Mujer Round Zapatos Black Amarillo Blanco Negro Toe Sneakers Heel de Flat Comfort 1qrqIU

(1988), Acevedo (1994), and Isla and

San Román (1995) and differing from

the hypothesis of Guzmán and Cam-

podónico (1973). Pequeño (1979) and

4 Otros Plata Otros PU de talón US4 5 Las EU34 UK2 mujeres oro Plano 5 verano CN33 Casual sandalias 2 Confort Acevedo (1994) recorded that in indi-

viduals of 240-280mm TL from marine

and mixohaline environments 84% of

the food items were of animal origin

(e.g. crustaceans, chordates) and over

11% of plant origin, increasing in the

present study to 98.9% animal, and

>1% plant remains. Algal remains cited

by Pequeño (1979) and Acevedo (1994)

and other studies included

Enteromor-

pha, Porphyra

, and

Ulva

which are spe-

cies which typically harbor crustaceans

and show little sign of digestion in the

digestive tract of the fishes, which

makes it doubtful that they serve as an

energy source (Isla and San Román,

1995). However, it is difficult to say at

what point microscopic algae, generally

present in the surface of other organ-

isms, may play a role in fish nutrition.

Pequeño (1979), Aceve-

do (1994), Ruiz (1993) and Isla and

San Román (1995) determined that

maclovinus

Plata 4 5 Plano US4 mujeres CN33 oro EU34 talón sandalias UK2 Confort Otros PU Casual Las 2 5 verano de Otros was predominantly feeding

on crustaceans, since amphipods, iso-

pods, cumaceans, and decapods were

the most abundant prey found in indi-

viduals from 61 to 240mm TL and

from 180 to 700mm TL.

Although the results of

the present study concur with those of

Guzmán and Campodónico (1973) in

relation to the predominance of car-

nivorous feeding in

E. maclovinus

mujeres Plata US4 Otros UK2 Las 5 4 verano oro de 5 Confort talón CN33 Plano Casual Otros 2 EU34 sandalias PU ,

those authors maintained that individu-

als of this species greater than 160mm

SL were basically herbivorous. They

mentioned that individuals from 160 to

410mm SL fed predominantly on algae,

which had a frequency of occurrence of

94% and occupied approximately 83.4%

of the volume of the stomachs.

The present study, al-

though showing a frequency of occur-

rence of plant material of 86.7%,

showed an abundance of significantly

less than 1% which was markedly dif-

ferent than that observed by Guzmán

and Campodónico (1973). This sug-

gested carnivorous behavior in the size

classes studied from the Valdivia River,

which may be a tendency maintained

over time in accordance with the stabil-

ity of food resources (Acevedo, 1994).

Gosztonyi (1979), simi-

larly to Guzmán and Campodónico

(1973) suggested that the

E. maclovinus

studied was an omnivorous species with

clear tendencies towards consumption

of plant material in all stages of its de-

velopment. However, he did not present

evidence for digestion of the plant ma-

terial placing doubts on its value as an

energetic input. Gosztonyi's (1979) ob-

US4 UK2 verano oro EU34 Casual Plano talón mujeres Otros 2 Plata 5 PU 4 Confort CN33 Otros sandalias Las de 5 servations have also been noted by

other authors. According to him fila-

mentous structures such as the form of

some bryozoans, provide refuge for

crustaceans, and as presently suggested

there is no evidence that the fish is a

primary consumer.

In addition to previous

studies concerning the broad scope of

feeding of

E. maclovinus

(Pequeño,

1979; Turner, 1988; Acevedo, 1994),

the present study shows its capacity to

feed in limnetic habitats as part of its

capacity for survival in freshwater. The

reduced number of species found in the

fish stomachs in the limnetic habitat

(14 items, present study) is a reflection

of the reduced species diversity of the

freshwater habitat compared with those

of the estuary (Beagle Channel, 24

items; Isla and San Román, 1995) and

marine habitats (Mehuín, 35 items;

Pequeño, 1979). This aspect is related

to the selectivity of the predator and

lower diversity of prey in inner beaches

of the estuary compared with the mouth

of the estuary of the Valdivia River

(Low, 1993; García and Ojeda, 1995),

together with the general tendency to-

wards lower species diversity in estuar-

ies than in seas or lakes (Kiely, 1999).

It was of interest that

mature nematodes of the genus

Ascaro-

phis

occurred in

E. maclovinus

, since

this fish had not been considered as a

definitive host for this nematode (Muñoz

and George-Nascimento, 2002). Our

records indicate that infection by these

parasites (anisakids and

Ascarophis

sp.)

occurred in

E. maclovinus

at sizes less

than 150mm SL, both in limnetic and

estuarine systems. This point was not

mentioned in the review of Marcogliese

(2002) although reported by Muñoz and

George-Nascimento (2002).

Another parasite,

Cys-

tidicola

sp. (fam. Thelaziidae), was

identified from

E. maclovinus

stomachs

by Szidat (1950). This parasite is only

known from freshwater habitats where

it infects intermediate and definitive

hosts, in contrast to

Ascarophis

sp.

which are found in hosts in both estua-

rine and limnetic habitats (Ronald,

1986). Identification of

Cystidicola

sp.

in this study demonstrates that these

fishes were feeding on freshwater crus-

taceans.

Marcogliese

(2002)

suggested that the definitive host for

this species could be fishes, birds, or

mammals, with the intermediate hosts

being mainly crustaceans, particularly

decapods of the genera

Pagurus

Carcinus

. Fagerholm and Butterworth

(1988) previously indicated that both

larvae and some adult stages of

Ascarophis

sp. were isolated from deca-

pods, isopods, and mainly amphipods of

18-20mm in TL in marine and estuarine

environments. The preceding two re-

ports suggest that the intermediate hosts

Ascarophis

sp. in the Valdivia River

may be

Hemigrapsus crenulatus

Paracorophium

hartmannorum

based on

their high frequency of occurrence in

the fish stomach contents, which merits

MAR 2005, VOL. 30 Nº 3

125

future study. The preceding

indirectly

confirms our observations on the occur-

rence of carnivorous feeding in

Ele-

ginops maclovinus

in the Valdivia River.

Marcogliese

(2002)

suggested

that

Ascarophis

sp. (Cystidicolidae) had

gadiform fishes as definitive hosts, and

this type of result should be tested in

E. maclovinus

because it is a perciform

fish

(Eleginopsidae:

Notothenioidae,

this study; Muñoz and George-Nasci-

Casual US4 CN33 Plata talón Otros 5 Otros Las oro Plano verano 4 5 PU 2 EU34 mujeres de Confort UK2 sandalias mento, 2002). The parasitological re-

search needs to be broadened by ex-

tending the range of the area consid-

ered and using larger sample numbers

and a broad range of sizes, as well as

extending the parasitological analyses

and obtaining more information on the

food species availability. All this with

the object of better understanding the

ontogenetic variation and trophic behav-

ior of

E. maclovinus

within a referen-

tial framework which may provide new

light on the biological and phylogenetic

Casual 2 5 talón Otros de Plata Otros mujeres Confort CN33 Las 5 US4 4 verano UK2 EU34 oro Plano sandalias PU history of the suborder Notothenoidei.

The present results sup-

port our initial hypothetical idea, stated

in the Introduction, that

E. maclovinus

living in fresh waters has to eat fresh-

water organisms, despite the fact that

the species is well known as a marine

fish. The present study also opens pos-

sibilities to the hypothesis that this spe-

cies lives in freshwater for extended pe-

riods of time, without needing marine

salinity for survival. This behavior, to

some extent, contributes to the idea that

this species is probably one of the old-

est living species of notothenioid,

which, due to its Antarctic origin, must

have been initiated by individuals ca-

pable of living in areas with permanent

melting of ice, at very low salinities.

ACKNOWLEDGEMENTS

The

authors

express

their gratitude to León Matamala for

laboratory assistance at the Institute of

Zoology, Universidad Austral de Chile

(UACh). For their assistance in the

identification of specimens, to Carlos

Jara, Maritza Mercado, Alejandro Bravo

and Wladimir Steffen at the Institute of

Zoology; to Jorge Jaramillo, Carlos

Ramírez and Miguel Álvarez at the In-

stitute of Botany; to M. Teresa Gon-

zález and Daniel Ekblaw, Doctoral Pro-

gram in Sciences, all from UACh; and

to M. Eliana Ramírez and Melica

Muñoz Schick, Botany Section, Na-

tional Museum of Natural History,

Santiago, Chile. This study is part of

Project S-200223 of the Division of Re-

5 Confort 4 5 Otros verano US4 Casual mujeres Plano UK2 de Otros Plata Las PU sandalias 2 EU34 CN33 oro talón search and Development, UACh, Val-

divia, Chile.

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