ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
COMMUNITY ECOLOGY OF THE METAZOAN PARASITES OF THREE BENTHOPELAGIC FISH
SPECIES (PISCES: ACTINOPTERYGII) FROM THE COASTAL ZONE OF CALLAO, PERU
ECOLOGÍA COMUNITARIA DE LOS METAZOOS PARÁSITOS DE TRES ESPECIES DE PECES
BENTOPELÁGICOS (PISCES: ACTINOPTERYGII) DE LA ZONA COSTERA DEL CALLAO, PERÚ
ABSTRACT
Keywords: ectoparasites – endoparasites – marine fish – parasite ecology – parasite of fish – South America
One hundred and eighteen benthopelagic fish specimens from the coastal zone of the Callao region, Peru,
were necropsied from May 2015 to January 2016 to study their metazoan parasite community: 38
specimens of Cheilodactylus variegatus Valenciennes, 1833 (Cheilodactylidae), 66 of Mugil cephalus
Linnaeus, 1758 (Mugilidae) and 14 of Paralabrax humeralis (Valenciennes, 1828) (Serranidae).
Nineteen taxa of metazoan parasites were collected: 10 in Ch. variegatus, 4 in M. cephalus and 7 in P.
humeralis. Only Cheilodactylus variegatus is a new host record for 7 species. Four species of parasites are
new geographic records. The digeneans were the majority of the parasite specimens collected (37.85%) in
Ch. variegatus. In M. cephalus, the majority of the parasite specimens collected were copepods and
monogeneans which accounted for 77.78% of individuals collected. Five larval stages were found. The
parasites of three host species showed the typical pattern of aggregate distribution observed in many
communities of metazoan parasites of marine fish of Peru. In M. cephalus, the total length was correlated
with the prevalence of 2 species of parasites. In Ch. variegatus, and P. humeralis, no relationship between
the prevalence and abundance versus the length and sex of host was observed.
Neotropical Helminthology
305
Neotropical Helminthology, 2019, 13(2), jul-dic:305-316.
1Laboratorio de Parasitología General y Especializada, Facultad de Ciencias Naturales y Matemática (FCNNM), Universidad
Nacional Federico Villarreal (UNFV), El Agustino, Lima, Perú
2Unidad de Posgrado, Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos, Lima, Perú
3Departamento de Ictiología, Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Perú
4Facultad de Ciencias Biológicas, Universidad Ricardo Palma (URP), Santiago de Surco, Lima, Perú
5Laboratorio de Ecología y Biodiversidad Animal (LEBA), Facultad de Ciencias Naturales y Matemática (FCNNM),
Universidad Nacional Federico Villarreal (UNFV), El Agustino, Lima, Perú
Corresponding author:* E-mail: joseiannacone@gmail.com
1,2 2,3 1 1 4,5
Jhon D. Chero ; Hernán Ortega ; Celso L. Cruces ; Gloria Sáez & José Iannacone *
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Volume13,Number2(jul-dec2019)
Three hierarchical levels in studies of parasite
c o m m u n i t i e s a r e r e c o g n i z e d : ( a )
infracommunities, which that include all
individuals of different species of parasites within a
single host. (b) component communities formed by
all infracommunities within a population or host
and (c) composite communities, that include all
parasite communities in various hosts within an
ecosystem (Bush et al., 1997, 2001).
Community studies form the basis of any
parasitological study and are useful for making
comparisons between host species by their
parasitological descriptors for evaluation of
biodiversity loss or as indicators of pollution
(Lafferty, 2012; Madanire-Moyo et al., 2012;
Madhavi & Lakshmi, 2012). Most studies of these
biological systems consist of interpreting patterns
of distribution and abundance of parasitic taxa as
hosts themselves of variables such as their
ontogenetic stage with samples usually taken in a
lifetime opportunity (Ferrer-Castelló et al., 2007).
One of the most suitable models to study ecological
aspects of parasites is the aquatic system of
metazoan parasites of marine fish (Luque &
Poulin, 2007). For ease of collection of hosts and
306
RESUMEN
Palabras clave: ectoparásitos – endoparásitos – peces marinos – ecología parasitaria – parásito de peces – América del Sur
Ciento dieciocho especímenes de peces bentopelágicos de la zona costera de la región del Callao, Perú,
fueron sometidas a una autopsia de mayo de 2015 a enero de 2016 para estudiar su comunidad de parásitos
metazoos: 38 especímenes de Cheilodactylus variegatus Valenciennes, 1833 (Cheilodactylidae), 66 de
Mugil cephalus Linnaeus, 1758 (Mugilidae) y 14 de Paralabrax humeralis (Valenciennes, 1828)
(Serranidae). Diecinueve taxones de metazoos parásitos fueron recolectados: 10 en Ch. variegatus, 4 en
M. cephalus y 7 en P. humeralis. Solo Cheilodactylus variegatus es un nuevo registro de huésped para 7
especies. Cuatro especies de parásitos son nuevos registros geográficos. Los digeneos fueron la mayoría
de los especímenes de parásitos recolectados (37,85%) en Ch. variegatus. En M. cephalus, la mayoría de
las muestras de parásitos recolectadas fueron copépodos y monogeneos con 77,78% de los individuos
recolectados. Se encontraron cinco estadios larvarios. Los parásitos de tres especies hospedadoras
mostraron el patrón típico de distribución agregada observado en muchas comunidades de parásitos
metazoos de peces marinos del Perú. En M. cephalus, la longitud total se correlacionó con la prevalencia
de 2 especies de parásitos. Ch. variegatus y P. humeralis, no se observó relación entre la prevalencia y la
abundancia versus la longitud y el sexo del huésped.
INTRODUCTION for the possibility of obtaining a large number of
replicas, parasites of fish are the most studied
compared to any other group of vertebrates (Luque,
2008; Luque et al., 2016). Many variables of fish
hosts (intrinsic characteristics) and environmental
(extrinsic) influence parasitic communities
(Cruces et al., 2014, 2015; Chero et al., 2016). The
latter have been used as tools to discriminate host
populations, trophic interactions and to identify
contaminated environments (Muñoz & Cribb,
2006; Pulido & Monks, 2008). The length and sex
of the fish host are considered important ecological
variables that relate to fluctuations in parasitic
communities (Luque & Poulin, 2008; Iannacone &
Alvariño, 2009ab).
In the present study, we report the community
ecology of the metazoan parasites of three
benthopelagic fish species at the component and
infracommunity level from Callao, Peru.
Thirty eight specimens of Cheilodactylus
variegatus Valenciennes, 1833 (Cheilodactylidae),
66 of Mugil cephalus Linnaeus, 1758 (Mugilidae)
and 14 of Paralabrax humeralis (Valenciennes,
Neotropical Helminthology, 2019, 13(2), jul-dic
MATERIAL AND METHODS
Chero et al.
307
1828) (Serranidae) were necropsied between May
2015 and January 2016 from the coast of Callao,
Peru (12° 4'S, 77°10'W) to study their community
of metazoan parasites (Eiras et al., 2006). Fishes
were identified according to Chirichigno &
Cornejo (2001). The average total lengths of the
fishes were: Ch. variegatus 23 ± 4.61 (13–33) cm;
M. cephalus 20.85 ± 5.31 (13–37) cm and P.
humeralis 16.86 ± 0.84 (15–18) cm.
The ecological approximation of the metazoan
parasite community was made to component and
infracommunity levels (Esch et al., 1990). The
analyses included only parasite species with
prevalence higher than 10% (Bush et al., 2001).
The variance-to-mean ratio of parasite abundance
(index of dispersion), computed using the program
Quantitative Parasitology 3.0 (Rózsa et al., 2000),
was used to detect distribution patterns of the
infrapopulations (Poulin, 1993; Amarante et al.,
2015). The dominance frequency and the relative
dominance (number of specimens of one
species/total number of specimens of all species in
the infracommunity) of each parasite species were
calculated according to Rohde et al. (1995). The
parasite species diversity was calculated using the
Brillouin index (H), because each fish analyzed
corresponded to a fully censused community (Zar,
1996). For dominance, the Berger-Parker index
(Bautista-Hernández et al., 2013) was used. The
Pearson's correlation coefficient rp was used to
indicate the relationship between the host's total
length and parasite abundance. Spearman's rank
correlation coefficient rs was calculated to
determine possible correlation between the total
length of host and parasite prevalence, with
previous arcsine transformation of the prevalence
data (Zar, 1996; Bautista-Hernández et al., 2013).
The possible influence of host sex on abundance
and prevalence of parasites was tested using the t-
Student test and the chi-square test, respectively.
Parasite species diversity was calculated using the
Brillouin's index (H) (Zar, 1996). The probable
variation of diversity in relation to host sex (Mann-
Whitney test) and to host total length (Spearman's
rank correlation coefficient) was tested.
The ecological terminology used follows Bush et
al. (1997). Statistical significance level was
evaluated at p ≤ 0.05. Voucher specimens of
metazoan parasites were deposited in the
Helminthological Collection and Related
Invertebrates of the Museum of Natural History at
the San Marcos University (MUSM), 3570-3590,
Lima, Peru.
Ethic aspects
The authors point out that they fulfilled all national
and international ethical aspects.
Component community
Nineteen different species of metazoan parasites
were collected: 2 monogeneans, 4 digeneans, 1
cestode, 3 nematodes, 7 copepods and 2
acanthocephalans. Two species of metazoan
parasites were common in at least two
communities.
Cheilodactylus variegatus. Ten species of
metazoan parasites were collected (1 monogenean,
2 digeneans, 1 cestode, 2 nematodes, 2
acanthocephalans and 2 copepods) (Table 1).
Cheilodactylus variegatus is a new host record for
many of these species except the monogenean
Microcotyle nemadactylus Dillon & Hargis, 1965,
and the copepods Caligus cheilodactyli Krøyer,
1863 and Clavellotis dilatata (Krøyer, 1863). The
monogenean M. nemadactylus was the most
prevalent species and Opecoelidae gen. sp. the
most abundant parasite collected 323 individuals
(37.16% of all parasites). Gonocercella aff.
pacifica was the species with the highest average
value of relative dominance (0.37 ± 0.19), followed
by M. nemadactylus (0.34 ± 0.17) and Corynosoma
sp. (0.14 ± 0.03). Ectoparasite adults account for
42.58% of all collected parasites, endoparasite
adults around 38.78% and larval endoparasites just
18.64%. The dispersion index (ID) showed five
parasites found in Ch. variegatus the typical
aggregation distribution pattern with the following
sequence from highest to lowest: M. nemadactylus
(12.40)> Corynosoma sp. (7.89)> C. dilatata
(3.08)> C. cheilodactyli (2.86)> Dichelyne sp.
(2.60). The type of distribution was not determined
in 5 parasites due to lower prevalence (Table 1).
The total length of the host showed no correlation
with the prevalence and abundance of any parasite.
Sex of host did not influence the prevalence and
abundance of species of parasites.
RESULTS
Neotropical Helminthology, 2019, 13(2), jul-dic
Ecology of the metazoan parasites of three benthopelagic sh
308
Mugil cephalus. Four species of metazoan
parasites were collected (Table 2). The
monogenean Metamicrocotyla macracantha
(Alexander, 1954) was the most abundant and
prevalent and 82 specimens (59.94% of all
parasites) were collected. Metamicrocotyla
macracantha had the highest value of mean
relative dominance (0.57 ± 0.23), followed by
Contracaecum sp. (0.22 ± 0.02) and Bomolochus
nitidus Wilson, 1911 (0.17 ± 0.05). All parasites of
M. cephalus showed the typical pattern of
aggregated distribution observed in many parasites
systems: M. macracantha (4.21)> B. nitidus
(3.97)> Contracaecum sp. (3.01)> N. lizae (1.56).
Specimens of Contracaecum sp. (rs = -1.00; p =
0.000) and B. nitidus (rs = 1.00; p = 0.000) showed
correlation between the total length of M. cephalus
and prevalence. The total length of the host showed
no correlation with the abundance of any parasites.
Host sex did not influence the prevalence and
abundance of any species of parasite.
Paralabrax humeralis. Seven species of metazoan
parasites were collected (3 digeneans, 1
acanthocephalan and 7 copepods) (Table 3).
Paralabrax humeralis is a new host record for the
digeneans Macvicaria sp. and Opecoelidae gen. sp.
The copepod Hatschekia amphiprocessa Castro-
Romero & Baeza-Kuroki, 1986 was the most
prevalent and abundant parasite with 169
individuals (52.81% of all parasites) collected. The
copepod H. amphiprocessa was the species that
had the highest frequency value of relative
dominance (0.53 ± 0.27), followed by Helicometra
fasciata (Rudolphi, 1819) Odhner, 1902 (0.33 ±
0.14) and Hamaticolax paralabracis (Luque &
Bruno, 1990) (0.07 ± 0.05) (Table 2). Adult
ectoparasites represented 63.43% of all collected
parasites, adult endoparasites around 35.31%, and
endoparasitic larvae just 1.25%. The dispersion
index (ID) showed five parasites of P. humeralis
with the typical aggregated distribution pattern
followed by H. fasciata (67.64)> H. paralabracis
(3.99)> H. amphiprocessa (7.84)> C. quadratus
(2.81)> Corynosoma sp. (2.06). The distribution of
2 parasites was not determined due to lower
prevalence of less of 10% (Table 3). The total
length of the host showed no correlation with the
prevalence and abundance of any parasite. The sex
of P. humeralis was positively correlated with the
2
prevalence of the copepod H. paralabracis (X =
4.66; p = 0.03). However, the abundance of the
remaining parasites was not correlated with the sex
of the host (p>0.05).
Infracommunities
Cheilodactylus variegatus. Thirty-six (94.73%)
specimens were parasitized by at least one parasite
species. A total of 869 individual parasites were
collected averaging 22.86 ± 35.04 per host. The
total length of the host was positively correlated
with the abundance (r = 0.42; p = 0.008) and with
the richness of parasites (rs = 0.48, p = 0.002).
Infections with 1 parasite species were found in
five hosts (13.16%), biparasitism in 17 hosts
(44.74%), triparasitism in 11 hosts (28.95%),
tetraparasitism two hosts (5.26%) and
pentaparasitism in a host (2.63%). The dominance
index of Berger-Parker for infracommunities was
0.45 ± 0.19. The average value of Brillouin
diversity index (H) was 1.31 ± 0.27. The average
diversity of parasite species did not correlate with
the total length of the host (rs = 0.21; p = 0.19) and
no significant differences between the diversity of
parasites between male (H = 1.32 ± 0.29) and
female hosts were observed (H = 1.26 ± 0.22) (Z c =
102.5; p = 0.13).
Mugil cephalus. Fifty-eight (80.55%) specimens
were parasitized by at least one parasite species. A
total of 144 individual parasites were collected
averaging 2.83 ± 2.71 parasite / host. Host length
did not correlate with the abundance (r = 0.15; p =
0.22) or with the richness of parasites (rs = 0.12, p =
0.30). Infections with 1 species of parasite were
found in 33 hosts (46%), double infections in 17
(24%) and triple infections in 8 hosts (11%). The
dominance index of Berger-Parker for
infracommunities was 0.44 ± 0.14. The average
value of Brillouin diversity index (H) was 0.80 ±
0.07. The average diversity of parasite species did
not correlate with the total length of the host (rs =
0.05; p = 0.65) and no significant differences
between the diversity of parasites of male (H = 0.80
± 0.06) and female hosts were observed (H = 0.79 ±
0.02) (Zc = 95; p = 0.45).
Paralabrax humeralis. All specimens of hosts
were parasitized by at least one parasite species. A
total of 320 individual parasites were collected
averaging 3.26 ± 7.19. The length of the host did
not correlate with the abundance (r = 0.13; p = 0.64)
or with the richness of parasites (rs = 0.35, p =
0.21). One host (7.14%) showed infection with one
Neotropical Helminthology, 2019, 13(2), jul-dic Chero et al.
309
parasite species and 7 (50%) with 3 (21.43%) and 2
(14.29%), and 1 (7.14%) with multiple infections
of 2, 3, 4 and 5 species, respectively. The
dominance index of Berger-Parker for
infracommunities was 0.52 ± 0.14. The average
value of Brillouin diversity index (H) was 1.09 ±
0.15. The average diversity of parasite species did
not correlate with the total length of the host (r =
s
0.32; p = 0.26) and no significant differences
between the diversity of parasites of male (H = 0.83
± 0.46) and female hosts were observed (H = 0.91 ±
0.43) (Zc = -0.19; p = 0.84).
Table 1. Prevalence, intensity range, mean intensity, mean abundance, and site of infection of metazoan parasites
found in Cheilodactylus variegatus from the coastal zone of Callao, Peru.
Parasites Prevalence
(%)
Intensity
range
Mean
intensity ± SD
Mean
abundance ± SD
Site of
infection
Monogenea
Microcotyle nemadactylus 76.32 2−57 10.28± 2.80 7.84± 3.98 Gills
Digenea
Gonocercella aff. pacica †* 5.26 1−5 3± 7.95 0.16± 1.46 Intestine
Opecoelidae gen. sp. †* 7.89 57−203 107.67± 66.06 8.50± 4.44 Intestine
Cestoda
Adenocephalus pacicus (larvae)* 2.63 1 1± 9.36 0.03± 1.55 Mesenteries
Acantocephala
Corynosoma sp. (larvae)* 50 1−22 6.79± 5.27 3.39± 0.83 Mesenteries
Prolicollis altmani (larvae)* 2.63 27 27± 9.36 0.03± 1.55 Intestine
Nematoda
Dichelyne sp.* 10.53 1−4 2± 8.66 0.21± 1.42 Intestine
Proleptus carvajali (larvae)*
2.63 5 5± 6.54 0.13± 1.48 Intestine
Copepoda
Caligus cheilodactyli 21.05 1−5 2.75± 8.13 0.58± 1.16 Gills
Operculum
Clavellotis dilatata 44.74 1−7 2.94± 7.99 1.32± 0.64 Gills
† New geographical record. *New host record.
Table 2. Prevalence, intensity range, mean intensity, mean abundance, and site of infection of metazoan parasites
found in Mugil cephalus from the coastal zone of Callao, Peru.
Parasites
Prevalence
(%)
Intensity
range
Mean
intensity ± SD
Mean
abundance ± SD
Site of
infection
Monogenea
Metamicrocotyla macracantha
51.39
1−7
2.22± 0.29
1.14± 0.45
Gills
Nematoda
Contracaecum sp. (larvae)
34.72
1−4
1.28± 0.38
0.44± 0.04
Kidney
Copepoda
Bomolochus nitidus
11.11
1−5
3.125± 0.93
0.35± 0.11
Gills
Operculum
Naobranchia lizae 11.11 1 0.63 ± 0.84 0.07± 0.30 Gills
Neotropical Helminthology, 2019, 13(2), jul-dic
Ecology of the metazoan parasites of three benthopelagic sh
310
Table 3. Prevalence, intensity range, mean intensity, mean abundance, and site of infection of metazoan parasites
found in Paralabrax humeralis from the coastal zone of Callao, Peru.
Parasites Prevalence
(%)
Intensity
range
Mean
intensity ± SD
Mean
abundance ± SD
Site of
infection
Digenea
Helicometra fasciata 78.57 1−37 9.73±2.96 7.64±3.10 Intestine
Macvicaria sp. † 7.14 1 1±3.21 0.07±2.26 Intestine
Opecoelidae gen. sp.
† 7.14 5 5±0.38 0.36±2.06 Intestine
Acantocephala
Corynosoma sp. (larvae)
14.28 2 2±2.50 0.29±2.11 Mesenteries
Copepoda
Caligus quadratus 21.42 1−8 3.67±1.32 0.79± 1.75
Gills
Operculum
Hamaticolax paralabracis
50
1−8 3.29±1.59 1.64± 1.15
Gills
Operculum
Hatschekia amphiprocessa 85.71 3−37 14.08±6.04 12.07±6.23 Gills
†New geographical record.
Findings indicate that the ectoparasites are the
main components of parasite community of M.
cephalus, where monogeneans dominance was
observed, and P. humeralis dominance was
with copepods. In the parasitic community of
C. variegatus, digeneans endoparasites were
the dominant.
Parasite community of M. cephalus is
dominated by ectoparasites (copepods and
monogeneans), that has previously been
reported by Luque (1985) and by Iannacone &
Alvariño (2009a) on the marine coast of Lima,
Peru. However, the dominance of
endoparasites in M. cephalus has been reported
by Özer & Kurca (2015) off the coast of
Turkey. These differences in the dominance of
a particular group of parasites (ectoparasites
and endoparasites) may be influenced by the
hydrobiological conditions or regional
DISCUSSION environmental or ecological conditions where
the fish were caught (Ibagy & Sinque, 1995).
The dominance of ectoparasites has been
reported for other parasitic communities in
marine fish from the South Pacific Coast
(Luque, 1994; Oliva & Luque, 1998).
Iannacone & Alvariño (2009a) indicated that
the monogenean parasite M. macracantha and
copepod N. lizae were the most prevalent
species with prevalences of 36.4% and 22.9%,
respectively. However, in the present research
the monogenean M. macracantha and the
nematode Contracaecum sp. were the most
common species with prevalences of 51.39%
and 34.72%, respectively. However, the
copepods B. nitidus and N. lizae presented
prevalence lower than 12%. The behavior of
forming schools in the flathead grey mullet
would probably facilitate the transmission of
M. macracantha, since this species of parasite
has a direct life cycle. The foraging habits
would favor the transmission of the nematode
Neotropical Helminthology, 2019, 13(2), jul-dic Chero et al.
311
Contracaecum sp. when consuming infected free
living copepods.
No correlation between the abundance of each
parasite species and the length in the composition
of the parasite community of M. cephalus was
found. In contrast, only a correlation was found
between the prevalence of Bomolochus sp. and
Contracaecum sp. with the size of the hosts. Luque
(1994) found that both the prevalence and mean
infection intensity of M. macracantha were
positively correlated with host length. However,
Iannacone & Alvariño (2009a) did not find
correlation between the prevalence and the
abundance of each species of parasite with the
length of flathead grey mullet. These differences
may be caused by the influence of regional
ecological disturbances. Poulin & Morand (2004)
mention that larger body size host fish could
provide more space, more nutrients, and possibly a
wider variety of niches for parasitic species.
Our results indicate that there is no effect of host
sex on parasite prevalence and abundance. These
same results were found by Iannacone & Alvariño
(2009a). Iannacone (2004) points out that the
selection of parasites for one of the two sexes of
host fish could be attributed to differences in the
ecological relationships (habitat, behavior and
feeding) of males and females. In this work, the
same pattern was observed in other marine fishes of
the Peruvian coast, where fish showed no
difference in parasite prevalence and abundance in
relation to host sex (Iannacone, 2003, 2004;
Iannacone & Alvariño, 2008).
The parasites B. nitidus and N. lizae showed low
prevalence values (11.11%). In contrast, Iannacone
& Alvariño (2009a) observed low prevalence
values (4.1%) for B. nitidus and relatively higher
values (22.9%) for N. lizae . In a congeneric species
of Brazil Mugil platanus (Günther, 1880), a
prevalence of 30.6% was observed for B. nitidus
(Knoff et al., 1997).
The most prevalent taxa for M. cephalus were not
the samein different years. During 1983-1986, the
most prevalent taxa were N. lizae, M. macracantha
and Contracaecum sp. (Luque, 1994). During
2008, M. macracantha, N. lizae and H. manteni
were more prevalent (Iannacone & Alvariño,
2009a). In contrast, during 2015-2016 (present
study), M. macracantha and Contracaecum sp.
were more prevalent. Also, species richness was
not the same in different years: during 1983-1986,
we recorded a total of 6 parasite taxa, 5 species in
2008, and 4 taxa in the present study (2015-2016).
This could be the result of changes in the
environmental conditions of the collection area,
mainly the abiotic environmental factors of the
Peruvian Fauna Province, the El Niño event and the
upwelling phenomenon in the marine
environment. Iannacone & Alvariño (2009a)
indicate that variation in composition between
years, involving trophic transmition of taxa, could
be explained by the types of prey available and
seasonal fluctuations of the intermediate hosts
(Iannacone et al., 2007). In addition, these authors
point out that another factor that could explain the
results obtained is the sampling period, which
would cause seasonal variations in the parasites of
M. cephalus; as well as in those that present
intermediate hosts (Ñahui, 2006).
With the exception of ectoparasites that have been
previously reported in C. variegatus in Peru by
Oliva & Luque (1998) and Iannacone et al. (2003),
all other species of parasites constitute new records
for this host. On the other hand, most of the species
of parasites that are in the Peruvian morworng have
been previously reported in other hosts that inhabit
the Peruvian sea (Luque et al., 2016).
The results obtained in the present study show the
predominance in numerical abundance and
endoparasite taxa richness over ectoparasites
(copepods and monogeneans) for the parasite
community of C. variegatus. However, Oliva &
Luque (1998) and Iannacone et al. (2003) reported
the dominance of ectoparasites in C. variegatus off
the coast of Chorrillos, Lima, Peru. For other
communities of parasites in fish of the family
Cheilodactylidae, the dominance of endoparasites
has been well documented. Thus, Vooren & Tracey
(2010) reported the dominance of endoparasites in
the coastal zone of New Zealand in Nemadactylus
macropterus (Forster, 1801). Rossin & Timi (2010)
point to Nemadactylus bergi (Norman, 1937) from
the coast of Mar de Plata (Argentina) dominance of
endoparasites. According to Tam et al. (2008)
dominance of endoparasites in the parasitic
community component of marine fish can be
attributed to the trophic behavior of hosts because
they are mainly omnivorous fish, which include a
Neotropical Helminthology, 2019, 13(2), jul-dic
Ecology of the metazoan parasites of three benthopelagic sh
312
wide range of aquatic invertebrates that can act as
intermediate hosts in the life cycle of several
endohelminths. Alves & Luque (2006) attributed
the dominance of endoparasites to the food habit,
the trophic level and the geographical distribution
of fish hosts (Gomez del Prado-Rosas et al., 2017).
Most studies of parasite communities in marine
fishes on the Peruvian coast show a dominance
pattern of endoparasites (Iannacone & Alvariño,
2008; Iannacone et al., 2010; Iannacone et al.,
2012; Ñacari & Sánchez, 2014; Chero et al.,
2014abcd; Iannacone et al., 2015).
Oliva & Luque (1998) and Iannacone et al. (2003)
indicated a low parasite richness in the community
of C. variegatus, registering 4 and 3 species of
ectoparasites, respectively. However, our data
show intermediate parasite richness, registering 10
species (three ectoparasites and seven
endoparasites). These differences in parasite
richness in C. variegatus could be attributed to the
sampling period that may be related to seasonal
variations in species richness. Intermediate
richness of parasitic species have been reported for
other fish communities in the Cheilodactylidae
family (Marcogliese, 2002; Vooren & Tracey,
2010; Rossin & Timi, 2010).
The parasites M. nemadactylus, Corynosoma sp.
and C. dilatata were the most prevalent species,
with prevalences of 76.32%, 50% and 44.74%;
respectively. In this study, these parasites are
considered core species. These results are
consistent with those obtained by Oliva & Luque
(1998) and Iannacone et al. (2003) who point to M.
nemadactylus as the most prevalent species. Rossin
& Timi (2010) found a prevalence of 21%, for M.
nemadactylus while Corynosoma australe was the
most prevalent species.
The digenean Hemiuridae gen. sp., the tapeworm
A. pacificus, the acantocephalan P. altmani and the
nematode Proleptus sp. presented low values of
prevalence (<6%) and are considered accidental
species. Iannacone et al. (2009ab) assign the low
prevalence of marine fish macro-parasite
communities to the environmental conditions of
the collection area, mainly to the abiotic
environmental factors of the Peruvian Fauna, to the
El Niño event, and to the upwelling phenomenon.
They can be attributed to the low number of hosts
analyzed or the narrow range of sizes analyzed
(Oliva & Luque, 1998).
A characteristic found during the sampling period
(May 2015 to January 2016) indicates that 4 larval
forms of endohelminths (A. pacificus, Corynosoma
sp., P. altmani and Proleptus sp.) are part of the
parasite community of C. variegatus. The presence
of endohelminth larvae in the present study can be
considered a reflection of the trophic level of C.
variegatus that would act on an intermediate scale
in the marine food chain, a consequence of a
benthopelagic habitat.
All the parasites showed an aggregated or
contagious distribution. This pattern is common in
most host-parasite systems (Poulin, 2007). This
fact seems to be related to the benthopelagic fish,
because of the three fish species studied, 2 of them:
M. cephalus and P. humeralis have an aggregate
pattern and form large schools with a dominance of
ectoparasites. This pattern of aggregate
distribution (ID> 1) is typical for parasitic marine
fish fauna on the Peruvian coast (Chero et al.,
2014abc). This type of pattern is common in most
host-parasite systems (Poulin, 2007; Amarante et
al., 2015). According to Von Zuben (1997), 3
factors can lead to an aggregated pattern of
distribution: (1) heterogeneity in host
susceptibility to infection; (2) direct playback of
the parasite within the host and (3) heterogeneity in
the ability of the host to eliminate the parasites by
immune response or other response (Amarante et
al., 2015).
In the present study, the total length of the Peruvian
morworng correlated with the abundance and
richness of parasites. According to Poulin & Moran
(2004), larger fish hosts harbor greater parasite
richness because they provide a wide variety of
niches and can sustain a greater number of
parasites. In fact, ontogenic changes in the
composition of parasite communities in fish hosts
are commonly reported in the literature (Rossin &
Timi, 2010). Henríquez & González (2012) point
out that another factor that could explain the results
is the sampling period, which would cause seasonal
variations in M. cephalus parasites; as well as those
presenting intermediate hosts (Gomez del Prado-
Rosas et al., 2017).
The fact that copepods were the most abundant
group in P. humeralis clearly shows that having a
Neotropical Helminthology, 2019, 13(2), jul-dic Chero et al.
313
direct life cycle, which does not involve more than
one host, is an attribute that favors the dispersion
and persistence of this group of parasites (Salgado-
Maldonado & Rubio-Godoy, 2014).
Three species of digeneans, Helicometra fasciata
(Rudolphi, 1819) Odhner, 1902, Macvicaria sp.
and Opecoelidae gen. sp. have been recorded in P.
humeralis. Of these species, H. fasciata presented
high prevalence values in comparison with the
other 2 species. This high prevalence could be
related to fish diet and the availability of infective
stages which depend mainly on the presence of
appropriate mollusk first intermediate hosts and
the crustaceans second intermediate hosts (Keeney
et al., 2008). Helicometra fasciata is a general
species that has been recorded along the coast of
the South Pacific (Peru and Chile) in 11 species of
carnivorous fish hosts (Kohn et al., 2007, Chero et
al., 2014ad; Luque et al., 2016).
Paralabrax humeralis sex was positively
correlated with the prevalence of H. paralabracis
copepod. Iannacone et al. (2012) points out that the
selection of parasites to one of the two sexes of host
fish could be attributed to differences in ecological
relationships (habitat, behavior and feeding) of
males and females.
The Authors would like to thank the Programa
Nacional de Innovación para la competitividad
y Productividad (Innóvate Perú) for the
financial support provided.
ACKNOWLEDGEMENTS
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Journal of Veterinary Parasitology, vol. 15,
pp. 167–181.
Amarante, CF, Tassinari, WS, Luque, JL, Pereira,
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