De de Zapatos Zapatos Alto Cuero alto Yukun Khaki Zapatos Tacón De La Moda tacón Fina PU Alto De zapatos Tacón Mujer De SwqxA
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120
MAR 2005, VOL. 30 Nº 3
Keywords: /
Eleginops /
Eleginopidae / Feeding Shifts / Osmoregulation / South America /
Yukun Tacón Cuero Zapatos Zapatos De alto tacón Tacón De Mujer PU Moda zapatos Alto De Alto Zapatos de Fina La Khaki De 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
Cuero Khaki PU Moda De Zapatos Zapatos Yukun Alto La Tacón tacón de zapatos Zapatos Fina De Tacón De De Mujer alto Alto 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,
et
al
., 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 (
eg
. 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
N
N%
F
F%
Crustacea
96
93.20
Corophiidae (Amphipoda)
59246
97.148
96
93.20
Tanaidacea (Malacostraca)
104
0.171
14
13.59
Ciprinidae (Ostracoda)
20
0.033
10
9.71
Hemigrapsus crenulatum
5
0.008
5
4.85
Idotheinae (Valvifera)
3
0.005
3
2.91
Zoea larvae
1
0.002
1
0.97
Gastropoda
20
19.42
Littoridina comingii
20
0.033
19
18.45
Bivalvia larvae
1
0.002
1
0.97
Insecta
72
69.90
Chironominae (Diptera:Chironomidae)
918
1.505
70
67.96
Hygrobatidae (Acarii)
2
0.003
2
1.94
Trichoptera (Tubo)
2
0.003
2
1.94
Inderminate
4
0.007
3
2.91
Teleostei
Zapatos Fina Zapatos Yukun Cuero De De alto La Alto Khaki De Tacón Mujer de De Moda PU Tacón Alto Zapatos zapatos tacón 1
de Fina Zapatos De PU zapatos Zapatos Tacón Alto De Khaki Cuero Zapatos alto Moda La Yukun Alto tacón Tacón De De Mujer ,
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
vs
. 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
of
samples
of
E.
maclovinus
having stomach contents
Yukun De Zapatos Alto Fina De Moda De Khaki De zapatos Cuero alto Tacón Zapatos tacón La Zapatos PU de Tacón Alto Mujer (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
sp
.
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-
Cuero Mujer La Zapatos Khaki alto Tacón De Moda Zapatos de Tacón Alto Alto PU De Fina De zapatos Zapatos De Yukun tacón ior toward species which inhabit gravel
and sandy areas, or in association with
small filamentous algae where benthic
grazing behavior is possible (
eg
. 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
tacón de De Mujer Fina Alto Alto Yukun De Moda De Zapatos De zapatos Tacón Zapatos Tacón alto Khaki Cuero Zapatos PU La Abundance /
Biomass
m
2
(gr/m
2
)m
2
(gr/m
2
)
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
0
0
Chironomidae
21.04
0.006
0
0
* The sectors are differentiated according to sampling locations, margin or center.
tacón Yukun Zapatos Zapatos zapatos Zapatos De Moda De alto Tacón Khaki De Alto La Cuero Alto PU Mujer Fina De de Tacón 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
E.
maclovinus
alto De De Yukun Mujer Alto Zapatos Tacón Tacón PU zapatos Zapatos La Zapatos De tacón Moda Alto De de Cuero Fina Khaki 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
De zapatos Tacón tacón Zapatos De PU Cuero Zapatos Zapatos De de Alto Yukun Mujer Tacón La Alto Khaki alto Fina Moda De ,
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-
De de Tacón zapatos De Mujer alto Moda De tacón Tacón Zapatos Cuero De Zapatos Yukun PU Fina Alto Khaki Alto La Zapatos 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
or
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
of
Ascarophis
sp. in the Valdivia River
may be
Hemigrapsus crenulatus
or
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-
zapatos Alto De Fina PU De alto Tacón La de Yukun Zapatos Mujer De Cuero Tacón tacón Zapatos Khaki De Alto Zapatos Moda 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
Tacón Zapatos Moda de Alto De De Zapatos Yukun tacón Mujer Zapatos La PU alto Tacón Khaki Alto zapatos Cuero Fina De De 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-
Fina Moda Zapatos Zapatos La Tacón Khaki zapatos Zapatos De Alto Cuero Tacón tacón De Mujer alto Alto de De PU De Yukun search and Development, UACh, Val-
Zapatos De La Mujer Alto Zapatos Alto Fina de tacón Yukun Zapatos Khaki Tacón alto De De PU Moda Tacón De zapatos Cuero Szidat L (1950) Los parásitos del róbalo (
Elegi-
nops maclovinus
Cuv. & Val.).
I Congr.
Nac. Pesquero Marítimo e Ind. Derivadas
.
Mar del Plata, Argentina. pp. 234-270.
Turner A (1988)
Relaciones tróficas de dos es-
pecies
bentófagas,
Cauque
mauleanum
(Steindachner,
1902)
y
Eleginops
maclovinus
(Valenciennes, 1830) (Pisces:
Osteichthyes) en el estuario del río Queule
(IX Región, Chile)
. Tesis. Facultad de
Ciencias, Universidad Austral de Chile.
Valdivia, Chile. 48 pp.
Vila I, Fuentes L, Contreras M (1999) Peces
límnicos de Chile
. Bol. Mus. Nac. Hist. Nat.
Chile 48
: 61-75.
Yamaguti S (1961)
Sistema Helminthum. Vol. III.
The nematods of vertebrates. Part I- II
.
Interscience. New York, USA. 1135 pp.
Forma del dedo del pie: puntiagudo
Material superior: cuero
Características corticales: piel de oveja
Altura del tacón: tacón medio (3-5CM), adecuado para la temporada: primavera, otoño, material interno: piel de cerdo, forma del talón: estilete, función: aumento, transpirable, resistente al desgaste, desodorante
Al aumentar la proporción del cuerpo, la proporción de personas en la proporción áurea se ve más hermosa, lo que te hace más seguro y atractivo.