Neotrop. Helminthol., 8(2), 2014
2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
HELMINTHIC ASSEMBLAGES OF SERIOLELLA POROSA GUICHENOT 1848 (PISCES:
CENTROLOPHIDAE) FROM SAN MATÍAS GULF (ARGENTINA)
ENSAMBLES HELMÍNTICOS DE SERIOLELLA POROSA GUICHENOT 1848 (PISCES:
CENTROLOPHIDAE) DEL GOLFO SAN MATÍAS (ARGENTINA)
1 1 1 2 1
Silvia Guagliardo , Carla Schwerdt , Noelia Galeano , Raúl González & Rubén D. Tanzola
Abstract
Keywords: Fish - helminthic assemblages - parasite ecology - Seriolella porosa.
Suggested citation Guagliardo S, Schwerdt C, Galeano N, González R & Tanzola, RD. 2014. Helminthic assemblages of
Seriolella porosa Guichenot 1848 (Pisces: Centrolophidae) from San Matías gulf (Argentina. Neotropical Helminthology, vol. 8,
n°2, jul-dec, pp. XX-XX.
1Laboratorio de Patología de Organismos Acuáticos- Depto. Biología, Bioquímica y Farmacia, Universidad Nacional del Sur, San Juan 670 (8000) Bahía Blanca,
2
Argentina. Escuela Superior de Ciencias Marinas, Universidad Nacional del Comahue, sede Atlántica, San Martín 247, San Antonio Oeste, Río Negro,
Argentina.
E-mail: rtanzola@uns.edu.ar
No previous studies were carried out on aspects of the helminth assemblages of Seriolella porosa.
The present study aims to analyze the metazoan parasite of S. porosa and establish the relationship
between the parasitic variations and both fish size and sex. A total of 101 specimens of S. porosa
from San Matías Gulf, Argentina were examined between September and October 2006. Thirteen
species were reported with a total of 3366 parasites. Lecithocladium cristatum was the most
prevalent, dominant and abundant species. The average species richness was 3.2 ± 1.20. The
evenness showed an inverse correlation with the total number of parasites and did not reveal
differences between host sexes. None of the parasite species showed interspecific associations
with each other. The average richness of the infracommunity was significantly less than the
component community. The helminth community of the silver warehou shows little diversity with
many satellite species and only two core species (Anisakis sp. and L. cristatum). Further studies,
using parasites as stock indicators, would indicate whether the San Matías population represents a
reproductive aggregation that penetrates the gulf seasonally in winter or whether it is a permanent
stock isolated from the continental shelf.
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Helminthic assemblages of Seriolella porosa
48
Resumen
Palabras clave: Ecología parasitaria, ensambles helmínticos, peces, Seriolella porosa,
Hasta el momento no se llevaron a cabo estudios sobre aspectos de los ensambles de helmintos de
Seriolella porosa. El presente estudio se propone analizar el ensamble de metazoos parásitos de S.
porosa y establecer las interrelaciones entre variaciones en la estructura parasitaria y el sexo y
tamaño del hospedador. Se examinó un total de 101 especímenes de S. porosa capturados entre
septiembre y octubre de 2006 en el Golfo San Matías, Argentina. Trece especies y un total de 3366
parásitos fueron registrados. La especie más prevalente, dominante y abundante fue
Lecithocladium cristatum. La riqueza específica fue de 3.2 ± 1.20. La equitatividad mostró una
correlación inversa con el número total de parásitos y no reveló diferencias entre sexos. Ninguna
de las especies parásitas mostró asociación interespecífica con otras especies del ensamble. La
riqueza promedio de la infracomunidad fue significativamente menor que aquella del
componente comunitario. La comunidad de helmintos del savorín mostró poca diversidad con
varias especies satélites y solo dos especies centrales (core) (Anisakis sp. and L. cristatum). El
presente podría constituir la base para identificar stocks poblacionales, empleando parásitos, para
demostrar si la población del Golfo San Matías es un conjunto reproductivo que penetra
estacionalmente al Golfo en invierno, o si se trata de un stock propio del Golfo y separado física y
reproductivamente de los savorines de la Plataforma Continental Argentina.
INTRODUCTION Ramos Alves & Luque, 2001; Iannacone &
Alvariño, 2008). Seriolella porosa Guichenot
1848 (silver warehou) is an important fish
resource of the Argentine Sea (Sánchez & Bezzi,
2004). Its distribution extends from 35° to 55° S
(Garciarena & Perrotta, 2002). Commercial
landings of this resource underwent a growing
trend over the last 20 years as "by catch" in the
hake fishery (Cousseau & Perrota, 1998). It was
described by Perier & Di Giácomo (2002) as “a
seasonal fish resource which uses the area as a
spawning ground and nursery” in the San Matías
Gulf fishery. Up to the present only two studies
have been made on the parasitological status of
this fish in the South Atlantic Ocean (Guagliardo
et al., 2009, 2010).
It would be expected that S. porosa carries
several parasite species to upper levels of the
food chain because it occupies an intermediate
level in the food web. Since there are no records
of aspects of the helminthic assemblages of the
silver warehou, the aims of this study were to
analyze them at the component and
infracommunity levels and to evaluate the
relationship between the parasitic burden and
fish size and sex.
Knowledge of helminth fish parasite
communities from commercial fisheries reveals
basic information as well as applicable data for
studies on population stocks (Timi, 2007;
Braicovich & Timi, 2008), the health of
ecosystems (Palm & Rückert, 2009) and the
sanitary state of the fish (Valero et al., 2006;
Jakob & Palm, 2006).
In view of recent studies, the parasitic fauna of
fish appears to be governed by the trophic habits
and availability of the hosts, as well as the range
of depth and migration processes (Rhode, 1984;
Kennedy et al., 1986; Poulin, 1995; Klimpel et
al., 2003, 2006a, b). This implies that parasites
are important indicators of the habitat and
trophic status of fish in marine ecosystems
(Klimpel et al., 2003). Many studies consider
that the host size is a factor that influences the
formation of parasitic assemblages (Thoney,
1993; Sardella et al., 1995; Balboa & George-
Nascimento, 1998), being a more influential
parameter than host sex (Luque et al., 1996;
Knoff et al., 1997; González & Acuña, 2000;
86
Neotrop. Helminthol., 8(2), 2014
A total of 101 specimens of S. porosa (68 males,
32 females and 1 undetermined) were examined
between September and October 2006. The area
of capture was the northern sector of San Matías
Gulf (41°00'S, 64°00'W), Argentina. The fish
were caught by commercial fleet trawlers from
San Antonio Oeste port. Host size (cm), weight
(g) and sex were determined. The gonad/somatic
index was estimated as GSI= (gonad
weight/total weight)*100. Parasites were
extracted from the gills, body cavity and
digestive lumen. They were subsequently
relaxed in hot saline solution, fixed in 5%
formalin and stored in 70% alcohol. Part of the
helminth sample was stained with Langeron's
hydrochloric carmine cleared in clove oil and
mounted in Canada balsam. Nematodes and
acanthocephalans were made transparent in hot
alcohol-glycerine. Parasite prevalence,
abundance and the intensity of infection were
calculated following Bush et al. (1997).
Specimens of digenean trematodes were
deposited in the collection of the Museum of La
Plata (Argentina) under the following numbers
of collection: Lecithocladium cristatum
(Voucher MLP 5935), Elytrophalloides oatesi
(Voucher MLP 5936), Gonocerca cfr. phycidis
(Voucher MLP 7937) & Aponurus laguncula
(Voucher MLP 5938).
The community structure was analyzed at the
component community and infracommunity
levels. Species with prevalences 10 % were
considered as component species in the
infracommunities (Bush et al., 1990).
The variance/mean ratio (coefficient of
dispersion) was used to determine the
distribution patterns at the level of
infrapopulations. In order to quantify the
influence of parasite species in the community,
the specific importance (IE = (relative
prevalence + relative abundance) x 100) was
estimated according to Bursey et al. (2001). At
the infracommunity level, the richness, mean
diversity and evenness when richness was
higher than four species (Brillouin based
evenness index) were calculated (Mouillot et al.,
2005). The qualitative association between pairs
of parasite species was estimated by using the
correlation Φ coefficient (Combes, 1983). At the
component community level, the relative
dominance (number of specimens of one species
in respect of the total number of specimens of all
species in the infracommunity) of each parasite
species was calculated according to Morales &
Pino de Morales (1987). The dominance
frequencies and the co-dominances were also
calculated. The ecto/endoparasite ratio was
determined as the number of ectoparasite
species/number of endoparasite species.
The species richness, the total number of
parasites, the Simpson index of diversity
(Pielou, 1975; Krebs, 1989), the Shannon-
Wiener index of diversity and evenness were
calculated after Magurran (1988). The
correlations between the total number of
parasites, richness, diversity and evenness in
relation to host weight and total length were
tested using Spearman's rank correlation
coefficient (Siegel & Castellan, 1995). Evenness
was also correlated with the total number of
parasites. This latter parameter was compared
with host sex using the nonparametric Mann-
Whitney U test (Siegel & Castellan, 1995). The
strategy of colonization, allogenic or autogenic
species, was assessed according to Bush et al.
(2001).
The mean total body length and weight of fish
were 39.60 ± 4.68 and 514.55 ± 264.25
respectively. The mean GSI was 0.052 (0.009 –
0.230) in females. Most of the females (75%)
had not reached the first sexual maturity length
(< 45 cm). A total of 3366 helminths, mostly
endoparasites, were recorded and a total of
thirteen taxa were identified. The ectoparasite
versus endoparasite relationship was low (R=
0.18). The helminth assemblage was highly
dominated by digenean (2309 or 68.6% of the
specimens). All component community species
(prevalence 10%) had an aggregated pattern of
distribution. Table 1 shows that Lecitochladium
cristatum was not only dominant but also the
MATERIALS AND METHODS
RESULTS
87
Guagliardo et al.
Helminthic assemblages of Seriolella porosa
Table 1. Prevalence, abundance, mean intensity and specific importance of the parasitic helminths of Seriolella porosa from the San Matías Gulf
(Argentina). 95% confidence interval. SD: standard deviation.
Species
Developmental
stage
Site
Prevalence
(%) ± CI
Abundance
± SD
Mean
intensity
± SD
Specific
importance
Frequence of
Dominance
single
Frequence of
Dominance
3 species
Previous records from
South Atlantic
Ocean (*)
Nematoda
Anisakis sp.
LIII
Body
cavity
75.25 ±8.5
7.22 ±10.96
9.59 ±11.71
797.25
25
1
1,2,3,4,5,6,7,
8, 9,10
Pseudoterranova sp.
LIII
Body
cavity
1.98 ±8.68
0.02 ±0.14
1 ±0
21.98
0
0
5,6,10,11,
12,13
Hysterothylacium sp.
LIV
Body
cavity
2.97 ±10.57
0.03 ±0.17
1 ±0
32.97
1
0
1,2,3,4,5,6,7,
8,10, 14,15,16
Philometra cf. seriolellae
Adult
Ovary
2.97 ±10.57
0.05 ±0.30
1.67 ±0.58
52.97
0
0
---
Acantocephala
Corynosoma cetaceum
Juvenile
Body
cavity
2.97 ±10.57
0.03 ±0.17
18 ±0
32.97
0
0
1,7,8,10,17,18
Corynosoma australe
Juvenile
Body
cavity
1.98 ±8.68
0.04 ±0.31
2 ±1.41
41.98
0
0
1,3,4,6,7,8,13,
17,18,20,22,23
Cestoda
Nybelinia sp. Plerocercus
Body
cavity 0.99 ±1.95 0.01 ±0.10 1 10.99 0 0 3,6,7,8
Table 1. Continuation.
88
Neotrop. Helminthol., 8(2), 2014
Table 1. Continuation.
Monogenea
Neogrubea seriolellae
Adult
Gills
63.4 ±9.49
2.65 ±3.98
4.19 ±4.32
328.4
6
2
---
Eurysorchis australe
Adult
Gills
28.7 ±8.91
0.42 ±0.80
1.44 ±0.87
70.7
2
0
---
Digenea
Lecithocladium cristatum
Adult
Stomach
80.19 ±7.85
17.90 ±24.63
22.32 ±25.74
1870.2
56
2
7,24
Aponurus laguncula Adult Stomach 19.8 ±7.85 0.40 ±1.08 2 ±1.65 59.8 0 1 7,10,24,25,26
Ellytrophaloides oatesi Adult Stomach 31.68 ±9.16 4.55 ±13.88 14.38 ±21.81 486.68 8 0
7,11,12,15,
24,25,27,28,29,30
Gonocerca. cf. phycidis Adult Stomach 0 ±1.95 0.01 ±0.10 1 0.09 0 0 15,24,28,29,31
(*) References: 1- Guagliardo (2003). 2- Tanzola & Guagliardo (2004). 3- Timi et al. (2005). 4- Timi & Poulin (2003). 5- Sardella et al. (1998). 6- Sardella & Timi (2004). 7- Braicovich (2008). 8-
Braicovich & Timi (2008). 9- Guagliardo et al. (2009). 10- Timi et al. (2008). 11- Gaevskaya et al. (1990). 12- Sardella & Timi (1996). 13- Cremonte & Sardella (1997). 14- Navone et al. (1998). 15-
Mackenzie & Longshaw (1995). 16- Incorvaia & Díaz de Astarloa (1998). 17- Timi & Lanfranchi (2009). 18- Sardella et al. (2005). 19- Tanzola & Guagliardo (2000). 20- Timi et al. (2001). 21-
Zdzitowiecki (1989). 22- Tanzola et al. (1997). 23- Braicovich et al. (2005). 24- Guagliardo et al. (2010). 25- Szidat (1950). 26- Szidat (1961). 27- Brickle et al. (2006). 28- Suriano & Sutton (1981). 29-
Szidat (1955). 30- Szidat & Graefe (1968). 31- Laskowski & Zdzitowiecki (2005).
Species
Developmental
stage
Site
Prevalence
(%) ± CI
Abundance
± SD
Mean
intensity
± SD
Specific
importance
Frequence of
Dominance
single
Frequence of
Dominance
3 species
Previous records from
South Atlantic
Ocean (*)
most abundant and prevalent species and it was
also of greater relative influence in the
community (IE= 1870.2).
Only one fish was free of parasites, five fishes
(4.95 %) harboured a single species while 95
hosts (94.05 %) showed multiple infestations,
with a richness range of two to six parasite
species. The average infracommunity species
richness was 3.2 ± 1.20. Co-dominances were
not frequent. All parasite species were autogenic
in their colonization strategy, completing their
life-cycles in aquatic hosts within the same
ecosystem.
Both the infracommunity and the component
community descriptors are shown in Table 2.
The richness and total number of parasites
showed significant correlation with the size of
the hosts, while only diversity was correlated
with body weight (Table 3). The evenness
showed an inverse correlation with the total
number of parasites.
No significant differences were observed
between males and females (U= 1057, p= 0.82)
in the total parasite burden and none of the
species showed any strong interspecific
associations.
Two species of Seriolella reported from the
Southwestern Atlantic are: S. porosa Guichenot
1848 and S. caerulea Guichenot 1848. Although
there is a latitudinal overlap between these two
species, they are rarely found together as they
live at different levels in the water column
(Cousseau & Díaz de Astarloa, 1993). In the San
Matías Gulf, S. porosa is the species that has
undergone rising and sustained catches, so it is
an important fishery resource in its distribution
area (Garciarena & Perrota, 2002; Perier & Di
Giácomo, 2002).
This study is the first comprehensive approach
on silver warehou helminth assemblages. Our
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Guagliardo et al.
Helminthic assemblages of Seriolella porosa
Table 2. Community descriptors of Seriolella porosa in San Matías Gulf (Argentina).
Component community Infracommunity
Total number of species 13 Mean species per host (±SD) 3.12 ± 1.20
Total number of helminths 3366 Mean helminth per host (± SD) 33.3 ± 27.6
Diversity indices
- Shannon-Wiener
1.28
- Simpson
0.64
Mean diversity (Brillouin) (±SD, rank)
0.23 ± 0.13 [0.00-0.56]
Evenness (Shannon-Wiener)
0.50
Mean evenness (Brillouin) (± SD, rank)
0.40 ± 0.19 [0.127-0.96]
Dominance
(Berger-Parker) 0.53
Percentage of infracommunities dominated by
the dominant species 55.45 %
Tabla 3. Relationships (Spearman correlation) between infracommunities descriptors and the size and weigth of
Seriolella porosa from Golfo San Matías(Argentina). r : Spearman's coefficient; critical p-value = 0.05.
s
Infracommunity descriptor Size Total weigth
rs p
rs p
Total number of parasites
0.31 0.002**
0.18 0.062
Richness 0.23 0.022*
0.18 0.074
Diversity (Brillouin)
0.16 0.098
0.35 0.00**
Evenness (Brillouin) -0.13 0.21 0.04 0.73
DISCUSSION
90
Neotrop. Helminthol., 8(2), 2014
records barely coincide with any previous
studies of Seriolella spp.; in S. violacea
Guichenot, 1848 from the Peruvian coast there
were no species in common with the present
survey. The monogenean Paraeurysorchis
sarmientoi (Tantalean, 1974) Tantalean,
Martinez & Escalante, 1985 and the cestode
Neobothriocephalus aspinosus Mateo &
Bullock, 1966 are the only two species reported
from this South Pacific host (Iannacone 2003).
Additionally, S. porosa showed no similarities
with the endoparasites of S. brama (Günther,
1860) from New Zealand although the
monogenean species were the same (Rhode et
al., 1980). None of the digeneans in this work
were recorded for S. punctata in Tasmania (Bray
& Cribbs, 2003).
According to Cortés & Muñoz (2008)
infracommunity studies constitute the first step
to any parasitological analysis within or between
species of hosts through their parasitological
descriptors. In the present study, all component
species of S. porosa follow the typical
aggregated pattern of distribution. As stated by
several authors, aggregation is common
behavior in parasitic life (Crofton, 1971; Esch &
Fernández, 1993). A wide range of biological
processes generates this type of distribution
(Morales & Pino de Morales, 1987). According
to Janovy (1992) the structures of parasite
populations and their frequency distributions
would be the result of mostly ecological
processes. The prey of the fishes could be
c o n s i d e r e d a s c a r r i e r s o f t h e s e
infracommunities, in agreement with the
concept of "instant infracommunities" (Bush et
al., 1993), perhaps transmiting many parasites
with the intake of few intermediate hosts and
vice versa, thus determining the distribution
pattern of parasites.
In our study ectoparasites species were scarce.
This fact agrees with the parasitism present in
teleosts from the South Atlantic coast (Sardella
& Timi, 1996; Tanzola et al., 1997; Tanzola &
Guagliardo, 2000; Sardella & Timi, 2004; Timi
et al., 2005; Timi & Lanfranchi, 2009). In the
north Bonaerense region of the Argentine Sea,
the dominance of larval parasites, in terms of
parasite prevalence and abundance, seems to be
the rule (Timi & Lanfranchi, 2009). The fact that
we have reported a dominance of adult stages at
higher latitude in our study, probably reflects a
particular biogeographic region where the
ecology component governs the parasitic
assemblages of the silver warehou in a different
way. It was noted that the mean richness of the
infracommunities was significantly less than the
total number of species from the component
community. This situation agrees with the idea
that the infracommunities rarely include all
species present at the component community
level (Poulin, 1998).
Seven species, with prevalences lower than 10%
were not included in the component community
a n a l y s i s ( P s e u d o t e r r a n o v a s p . ,
Hysterothylacium, sp., Philometra cf.
seriolellae, Corynosoma australe, C. cetaceum,
Nybelinia sp. and Gonocerca cf. phycidis).
The average richness of the infracommunities
(3.12 ± 1.20) represents a common value in other
host/parasite systems, ranging from two to five
species per host (Cordeiro & Luque, 2004;
Mouillot et al., 2005; Jacob & Palm, 2006;
Rodríguez-González & Vidal-Martínez, 2008;
Timi & Lanfranchi, 2009). In comparison, it
should be noted that the average richness of S.
porosa was slightly less than the value recorded
for S. violacea in Chilean waters (4.60 ± 1.54)
(Mouillot et al. 2005). In this study, the most
recruited species with prevalence > 50% were L.
cristatum, N. seriolellae and Anisakis sp.
The richness was positively correlated with the
size of the hosts. In larger fish more food is
consumed, so consequently an increase in the
exposure to the infective stages of the parasites is
expected (Poulin, 1995).
When both the Shannon-Wiener and Simpson
indexes were compared in respect of the
Brillouin values, the mean values for the
infracommunities were lower than the
component community.
Until the present time, the most common mean
value of helminth diversity in marine fish
91
Guagliardo et al.
Helminthic assemblages of Seriolella porosa
infracommunities is less than two. Based on
previous records (Ramos Alves et al., 2002;
Cordeiro & Luque, 2004; Sardella & Timi, 2004;
Timi & Lanfranchi, 2009; Palm & Rückert,
2009) the parasite assemblage of silver warehou
shows little diversity, with many satellite species
and only two central ones (Anisakis sp. and L.
cristatum).
The evenness is a measure of the unequal
representation of species in a hypothetical
community in which all species are equally
common (Krebs 1989). In this work, the
evenness was 0.50, while the mean value of
evenness in the infracommunities was lower
(0.40) showing an unequal distribution of the
specific abundance. These values can perhaps be
explained by the high dominance of L.
cristatum. Evenness was not correlated with
either size or weight of the host but showed a
highly significant inverse correlation with the
total number of parasites. We have noted that the
greatest number of helminths were L. cristatum
and Anisakis sp., both of them with the highest
dominances.
None of the species showed any interspecific
association with each other (Table IV). A
common pattern in many host species is the
absence of sexual differences in the prevalence
and/or parasitic intensities (Ramos Alves &
Luque, 2001; Knoff et al., 1997; Luque et al.,
1996; Iannacone, 2003). Accordingly, no
differences in the total number of parasites were
reported here, discarding selective parasitism or
differential trophic behavior between sexes.
In respect of the colonizing ability in the
Argentine Sea of cestodes, nematodes and
acanthocephalans recorded in the silver
warehou, they may be considered as generalists,
as they have previously been recorded in several
hosts in the South Atlantic. It is likely that some
infect S. porosa accidently, especially those with
low prevalences, due to the trophic behavior of
this host (Forciniti & Pérez Macri, 1992;
Sánchez & Prenski, 1996). However it should be
noted that both, monogeneans and digeneans,
have demonstrated selective colonization
strategies in the Atlantic Ocean.
Previous studies on the use of parasites as
biological tags of South Atlantic fish stocks have
been able to discriminate populations of
Merluccius hubbsi Marini, 1933 (Sardella &
Timi, 2004), Scomber japonicus (Houttuyn,
1782) (Cremonte & Sardella, 1997); Engraulis
anchoita HUbbs & Marini, 1935 (Timi, 2003),
Cynoscion guatucupa Cuvier 1830 (Timi et al.,
2005), Eleginops maclovinus (Valenciennes,
1839) Dollo, 1904 (Brickle & MacKenzie,
2007) Percophis brasiliensis Quoy & Gaimard,
1824 (Braicovich & Timi, 2008) and Pinguipes
brasilianus Cuvier, 1829 (Timi et al., 2008). The
only information about seasonal migration in the
area of distribution of the silver warehou in the
Argentine Sea is in the San Matías Gulf (Perier
& Di Giácomo, 2002). Further studies, using
parasites as stock indicators, might show
whether the San Matías Gulf population
represents a reproductive aggregation that enters
the gulf in winter, looking for better
environmental conditions or whether it is a
permanent stock isolated from the continental
shelf.
Authors are grateful to Mrs. Rosemary Scoffield
for her assistance with the English language and
Mr. Paul Osovnikar from the Instituto de
Biología Marina y Pesquera Ate. Storni,
province of Río Negro, Argentina, for his
collaboration in obtaining the samples of S.
porosa.
ACKNOWLEDGEMENTS
Balboa, L & George-Nascimento, M. 1998.
Variaciones ontogenéticas y entre años en
las infracomunidades de parásitos
metazoos de dos peces marinos de Chile.
Revista Chilena de Historia Natural, vol.
71, pp. 27 - 37.
Braicovich, PE, González, RA & Tanzola, RD.
2005. First record of Corynosoma
a u s t r a l e ( A c a n t h o c e p h a l a ,
Polymorphidae) parasitizing seahorse
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