Parasite 27, 6 (2020)

Ó J. Violante-González et al., published by EDP Sciences, 2020

https://doi.org/10.1051/parasite/2020001
Available online at:
www.parasite-journal.org

RESEARCH ARTICLE OPEN ACCESS

Interannual variation in the metazoan parasite communities

of bigeye trevally Caranx sexfasciatus (Pisces, Carangidae)
Juan Violante-González1,2,*, Scott Monks3,*, Yesenia Gallegos-Navarro2, Nataly G. Santos-Bustos2,
Princessa J. Villalba-Vasquez2, Jesús G. Padilla-Serrato4, and Griselda Pulido-Flores3
1
Facultad de Ecología Marina, Universidad Autónoma de Guerrero, 39390 Acapulco, Mexico
2
Centro de Ciencias de Desarrollo Regional, Universidad Autónoma de Guerrero, 39630 Acapulco, Mexico
3
Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, 42000 Pachuca, Mexico
4
Conacyt – Facultad de Ecología Marina, Universidad Autónoma de Guerrero, 39390 Acapulco, Mexico

Received 9 September 2019, Accepted 6 January 2020, Published online 31 January 2020

Abstract – Parasite communities in Caranx sexfasciatus were characterized and analyzed to determine any interannual
variations in structure and/or species composition. In total, 422 C. sexfasciatus were collected from Acapulco Bay,
Mexico, between May 2016 and March 2019. Thirty-two taxa of metazoan parasites were identified: five Monogenea,
thirteen Digenea, one Acanthocephala, one Cestoda, three Nematoda, seven Copepoda, and two Isopoda. Monogeneans
were the most frequent and abundant parasite species in all sampling years. Parasite species richness at the component
community level varied significantly from 8 (May 2016) to 25 (March 2019) and was similar to previous reports for
other species of Carangidae. The component communities and infracommunities in C. sexfasciatus were characterized
by low parasite species numbers, low diversity, and dominance of a single species (the monogenean Neomicrocotyle
pacifica). Parasite community structure and species composition varied between sampling years and climatic seasons.
Seasonal or local fluctuations in some biotic and abiotic environmental factors probably explain these variations.

Key words: Parasites, Marine fish, Caranx sexfasciatus, Acapulco, México.

Résumé – Variation interannuelle des communautés de parasites métazoaires de la carangue à gros yeux
Caranx sexfasciatus (Pisces, Carangidae). Les communautés de parasites de Caranx sexfasciatus ont été
caractérisées et analysées afin de déterminer si elles connaissent des variations interannuelles dans la structure et/ou
la composition des espèces. Au total, 422 C. sexfasciatus ont été collectés dans la baie d’Acapulco, au Mexique,
entre mai 2016 et mars 2019. Trente-deux taxons de parasites métazoaires ont été identifiés : cinq Monogenea, treize
Digenea, un Acanthocephala, un Cestoda, trois Nematoda, sept Copepoda et deux Isopoda. Les monogènes étaient
les espèces de parasites les plus fréquentes et les plus abondantes au cours de toutes les années d’échantillonnage. La
richesse en espèces de parasites au niveau de la communauté des composants variait considérablement de 8 (mai
2016) à 25 (mars 2019) et était similaire aux rapports précédents pour d’autres espèces de Carangidae. Les
communautés et infracommunautés de C. sexfasciatus étaient caractérisées par un faible nombre d’espèces de
parasites, une faible diversité et la dominance d’une seule espèce (le monogène Neomicrocotyle pacifica). La
structure des communautés de parasites et la composition des espèces variaient entre les années d’échantillonnage et
les saisons climatiques. Les fluctuations saisonnières ou locales de certains facteurs environnementaux biotiques et
abiotiques expliquent probablement ces variations.

Introduction directly between individual hosts through contact, whereas

endoparasites often use trophic transmission routes [9, 26, 37].
Parasite communities in marine fish consist of ectoparasites Transmission strategies of parasites are linked to host behavior.
(monogeneans, copepods, and isopods) and endoparasites For instance, ectoparasite populations may be more abundant on
(digeneans, cestodes, nematodes, and acanthocephalans). Both species of fish that form large schools than on solitary species
types of parasite exhibit different transmission strategies to infect [23, 29, 31], because the probability of a transmission stage
their hosts; for example, ectoparasites are often transmitted (e.g., eggs, larvae) coming into contact with a host increases
as host density rises.
*Corresponding authors: [email protected]; Studies of parasite communities are conducted mainly
[email protected] at two different hierarchical levels: component community
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
2 J. Violante-González et al.: Parasite 2020, 27, 6

(between locations or host populations) and infracommunity Contents of the digestive tract were examined to identify prey
(between individual hosts) [14, 17, 51]. In recent years, a items consumed by this species. Dietary items were identified
central theme in parasite ecology has been the identification to the family level when possible. Prey item analysis was
of the factors (biotic or abiotic) determining species richness carried out using the frequency of occurrence method [19,
and composition in these communities. However, an under- 30]. Parasites were identified to the lowest possible taxonomic
standing is also needed of how consistent parasite community level and vouchers of the most abundant and best-preserved
richness and species composition are in space and time. For specimens deposited in the Coleccion Nacional de Helmintos
example, spatial or temporal variation in community structure (CNHE), Instituto de Biologia, Universidad Nacional
may indicate how important local environmental factors (abiotic Autonoma de Mexico, Mexico City.
and biotic conditions) are in structuring a parasite community, Infection levels for each parasite species were described
particularly when disparities are found between different host using prevalence (percent of fish infected with a particular
species [1, 24, 46, 50, 53]. There is still no consensus on parasite species); mean abundance (mean number of individual
whether marine parasite communities can exhibit temporal parasites of a particular species per examined fish), expressed as
variations in structure and species composition. Some studies the mean ± standard deviation (SD); and intensity (number of a
suggest that the infection levels of most parasite species do particular parasite species per infected fish), expressed as range
not experience significant changes over time, and that commu- (minimum–maximum) [5, 6, 8]. Possible differences in infec-
nities tend to be generally stable in species composition for long tion levels between sampling years and climatic seasons were
periods of time [4, 12, 16, 43]. Others indicate that even though identified using G-tests [44], and a general linear model
parasite species composition may be relatively stable over time, (GLM) for abundance. The dispersion index (DI = variance
a community can undergo substantial changes in structure due to mean abundance ratio) was applied to describe parasite
to variations in local environmental factors [14, 39, 51]. dispersion patterns. The infracommunity index (ICI) [55],
The bigeye trevally, Caranx sexfasciatus Quoy & Gaimard which describes the frequency of double and multiple infections
1825, is an economically important pelagic fish species dis- by a single species of parasite in a distinct host (affinity level of
tributed widely along the eastern coast of the Pacific Ocean a species of parasite; i.e. species with great tendency to join the
from CA, USA to Ecuador and the Galapagos Islands [2]. infracommunity), was also calculated. Spearman’s correlation
Bigeye trevally often form large stationary daytime schools, coefficient (rs) was used to determine possible relationships
but usually tend to be solitary at night when feeding. Their diet between total host length and abundance or DI values of each
consists mainly of fish, but the species also preys on squids and parasite species.
crustaceans [2]. Despite its ecological and economic impor- Analyses were done at the levels of component community
tance, no information is available to date on its parasite fauna (i.e. total parasite species in all fish collected at a sampling year)
along the Pacific coast of Mexico. The present study objectives and infracommunity (i.e. total parasite species in each individ-
were (1) to characterize the metazoan parasite communities of ual fish). Component community parameters included total
C. sexfasciatus; and (2) to evaluate possible interannual vari- species richness, total number of individuals of each parasite
ability in its parasite communities. species, the Shannon–Wiener Index (H) as a measure of diver-
sity, species evenness (equitability), and the Berger–Parker
Index (BPI) as a measure of numerical dominance [25]. The
Materials and methods qualitative Sorensen index and quantitative percentage of simi-
larity (PS) index were used to evaluate similarity and difference
A total of 422 individuals of C. sexfasciatus were obtained in parasite community species composition between sampling
from commercial fishermen over a four-year period (May dates. Differences between component community parameters
2016–March 2019) from Acapulco Bay (16°510 N; 99° were identified with Student t and v2 tests.
520 W) in Guerrero, Mexico. The tropical Pacific region expe- Infracommunities were described in terms of mean number
riences two distinct climatic seasons: a rainy period from June of parasite species per host, mean number of individuals of each
to November (total precipitation  950 mm), and a dry period species, and the mean Brillouin Diversity Index (H0 ) value per
from December to May (total precipitation < 70 mm). In the host. The multivariate general linear model (GLM) was used to
years 2017 and 2019, a single sampling was carried out, but identify possible differences in infracommunity parameters
in a different climatic season: August (rainy season) and March (dependent variables) between sampling years and climatic
(dry season), respectively. In 2016 and 2017, two samplings seasons (predictor variables); fish body size (total length) was
were carried out per year, which included both climatic seasons: used as a covariate to control for the influence of host body size.
May and October in 2016, and May and November in 2018. The significance of all statistical analyses was established at
Records of surface temperatures of the ocean waters and salin- p < 0.05, unless stated otherwise. A multivariate analysis (prin-
ity per sampling date were obtained from other studies carried cipal component analysis, PCA) was applied to identify factors
out at the same location but not yet published. Multivariate El that influenced parasite infracommunity species richness and
Niño index values (MEI) for each sampling date were obtained diversity. The predictor variables used were: Fulton’s condition
from the National Oceanic and Atmospheric Administration factor (Kn) [13]; host diet diversity (calculated as the diversity
(NOAA: https://www.esrl.noaa.gov/psd/enso/mei/table.html). of items consumed by host populations at each sampled date,
Fish were measured and weighed at the time of collection. through the use of the Shannon–Wiener index at the family
A complete necropsy was made for each specimen and all par- level); number of endoparasite and ectoparasite species; surface
asites were collected from the internal and external organs [52]. temperature; salinity; MEI values; sampling year; and climatic
 J. Violante-González et al.: Parasite 2020, 27, 6 3

season. The Kaiser–Meyer–Olkin (KMO) test of sampling ade- In contrast to the percentage infection results, only five
quacy for each variable in the model, as well as the Bartlett species (N. pacifica [GLM; F3,406 = 7.92, p < 0.05], Ps. selene
sphericity test, which evaluates the possibility that there is [GLM; F3,406 = 3.05, p < 0.05], B. varicus [GLM; F3,406 = 3.10,
redundancy among variables were applied. The variance maxi- p < 0.05], Tetraphyllidea cestode [GLM; F3,406 = 5.49,
mizing rotation method was applied to produce the two ordina- p < 0.05], and Ca. alalongae [GLM; F3,406 = 5.31,
tion axes. Discriminant function analyses based on p < 0.05]) exhibited significant interannual variation in abun-
Mahalanobis distances were used to identify possible differ- dance. Abundance for B. varicus, Ps. selene and Tetraphyllidea
ences in parasite community structure between sampling years. larvae was highest in October 2016. For Ca. alalongae, it was
The probability of correct classification expected by chance highest in 2017, while for N. pacifica it was highest in 2019
alone of fishes to any of the four sampling years was calculated (Table 1). Prevalence values were generally positively corre-
using the proportional chance criterion, which is a simple lated with mean abundance values, indicating that the most
method to account for differences in sample sizes between prevalent species also were the most abundant (rs = 0.946,
the groups being compared [36]. Only parasite species with a p < 0.01).
prevalence >10% in at least one of the sampling years (a com-
ponent species; sensu [7]) were included in this analysis.
Spatial dispersion
The dispersion index (DI) values indicated that at least 10
Results species (31%) exhibited an aggregated dispersion pattern in
one or more sampling years (Table 1). Higher mean aggrega-
Species composition tion values (DI > 8) occurred in several years for the monoge-
Thirty-two taxa of metazoan parasites (23 of helminths and neans N. pacifica and Pr. manteri (Table 1). The DI values of
nine of Crustacea) were recovered and identified (9866 individ- each parasite species correlated positively with its prevalence
ual parasites) from 422 individuals of C. sexfasciatus collected (rs = 0.824, p < 0.01), total number of individuals
from Acapulco Bay, Mexico. Five species of Monogenea (rs = 0.878, p < 0.01), and mean abundance (rs = 0.871,
(adults), 13 Digenea (12 adults and one metacercaria), one p < 0.01) values, but not with host body size or sample size
Acanthocephala (adult), three Nematoda (one adult and two lar- (p > 0.05).
vae), seven Copepoda, and two species of Isopoda were col-
lected (Table 1). Species richness was highest among the
digeneans, representing 37.1% of the total species, followed Host diet composition
by copepods (20%). Based on infection site, 14 species of par- The alimentary spectrum of the fish included twelve prey
asite were classified as ectoparasites and 18 as endoparasites. items, of which smaller fish (36%), crab larvae (24.5%) and
The numbers of species of ectoparasite varied significantly from penaeid larvae (15.6%) represented the largest proportions.
2.02 ± 0.90 in 2016 to 2.41 ± 1.20 in 2019 (ANOVA Additonal prey items accounted for 24% of the diet, and
F3,405 = 3.23, p < 0.05) (Fig. 1). Eleven species, Neomicro- included amphipods, polychaetes, mollusk larvae, isopods,
cotyle pacifica Yamaguti 1968, Protomicrocotyle manteri stomatopods, pistol crabs, and copepods. Diet composition var-
Bravo-Hollis 1966, Pseudomazocraes selene Hargis 1957, ied between sampling years (t = 3.10, p < 0.05). For example,
Bucephalus varicus Manter 1940, Ectenurus virgulus Looss in May 2016 diet composition was less varied (H = 0.68,
1910, Synaptobothrium apharei Yamaguti 1970, Tetraphyllidea Table 2), with crab larvae being the main prey item. Feeding
gen. sp., Anisakis sp., Caligus alalongae Krøyer 1863, Ca. habits also changed with fish body size; larger individuals con-
robustus Bassett-Smith 1898, and Lernanthropus ilishae Chin sumed higher percentages of fish while smaller ones fed on
1948 occurred in the parasite communities of C. sexfasciatus higher percentages of crustaceans and other prey.
in all sampling years (Table 1).

Component community
Interannual variation in infection levels
Species richness of parasite by sampling year (Table 2) var-
For eight of these perennial species (the exceptions were ied widely from eight (May 2016) to 25 (March 2019)
Pr. manteri, S. apharei and Ca. robustus), prevalence varied (v2 = 11.6, p < 0.05). No correlation was observed between
significantly between sampling years, though no clear pattern sample size and species richness at this level, indicating that
was observed in variation. For the parasites B. varicus the different sample sizes used in the analyses had no effect
(G = 35.1, p < 0.05) and E. virgulus (G = 12.9, p < 0.05) infec- on the results. The total number of individual parasites ranged
tion percentages were highest in May 2016. For the Tetraphyl- from 670 (October 2016) to 3465 (March 2019) (v2 = 3,997.2,
lidea cestode, prevalence was highest during October 2016. The p < 0.05). The only dominant species was the monogenean
species N. pacifica (G = 21.8, p < 0.05), Anisakis sp. (G = 12.1, N. pacifica (Table 2), although its degree of dominance varied
p < 0.05) and Ca. alalongae (G = 42.3, p < 0.05) exhibited their significantly between sampling years (t = 4.70, p < 0.01).
highest percentages of infection in 2017. For L. ilishae Shannon–Wiener diversity index values were generally low,
(G = 17.1, p < 0.05), the highest percentage occurred in May ranging from 0.90 (October 2016) to 1.40 (March 2019), but
2018, while for Ps. selene (G = 34.9, p < 0.05), it was in varied between sampling years (t = 3.68, p < 0.01). Similarity
November 2018 (Table 1). between component communities was slightly low overall
4 J. Violante-González et al.: Parasite 2020, 27, 6

Table 1. Parasite infection parameters for Caranx sexfasciatus from Acapulco Bay, Mexico.
Parasite taxa Site on Accession Year nb Prevalence Totalc Abundanced Range of DIf ICIg
host numbera (%) intensitye
Digenea
Bucephalus margaritae Ozaki & Intestine 10,997 2017 97 2.06 3 0.03 ± 0.71 1–2 0.33 0.007
Ishibashi, 1934 2018M 63 4.76 3 0.05 0–1 0.021
2019 110 3.64 10 0.09 ± 2.4 1–6 2.27 0.015
Bucephalus varicush Manter, 1940 Intestine 10,998 2016M 65 40* 81 1.25 ± 2.2 1–9 1.52 0.146
2016O 36 27.78 67 1.86 ± 7.4* 1–25 8.13 0.109
2017 97 24.74 70 0.72 ± 3 1–12 3.04 0.086
2018M 63 14.29 26 0.41 ± 2.8 1–9 2.72 0.064
2018N 51 3.92 2 0.04 0–1 0.016
2019 110 19.09 157 1.43 ± 8.6 1–31 9.89 0.081
Neoapocreadium cf. caranxi Intestine 2017 97 1.03 1 0.01 0–1 0.004
Didymozoid larvae Intestine 2017 97 4.12 6 0.06 ± 0.6 1–2 0.22 0.014
2018N 51 1.96 2 0.04 0–2 0.008
2019 110 2.73 3 0.03 0–1 0.012
Ectenurus virgulush Looss, 1910 Intestine 11,000 2016M 65 29.23* 38 0.58 ± 3 1–14 4.39 0.107
11,001 2016O 36 25.00 35 0.97 ± 3.8 1–13 3.69 0.098
2017 97 20.62 32 0.33 ± 1.1 1–5 0.75 0.071
2018N 51 9.80 10 0.20 ± 1.7 1–5 1.50 0.041
2019 110 13.64 38 0.35 ± 3.2 1–14 4.11 0.058
Hirudinella ventricosa (Pallas, 1774) Intestine 2017 97 5.15 5 0.05 0–1 0.018
Baird, 1853 2018N 51 1.96 1 0.02 0–1 0.008
2019 110 0.91 1 0.01 0–1 0.004
Lecithocladium excisum (Rudolphi, Intestine 2019 110 1.82 3 0.03 ± 0.7 1–2 0.33 0.008
1819) Lühe, 1901
Manteria brachyderus (Manter, Intestine 2018N 51 1.96 1 0.02 0–1 0.008
1940) Caballero & Caballero, 1950
Mecoderus oligoplitis Manter, 1940 Intestine 2019 110 0.91 1 0.01 0–1 0.004
Pseudopecoeloides carangi Intestine 11,002 2018M 63 1.59 1 0.02 0–1 0.007
(Yamaguti, 1938) Yamaguti, 1940
Stephanostomum ditrematis Intestine 2018N 51 1.96 1 0.02 0–1 0.008
(Yamaguti, 1939) Manter, 1947 2019 110 1.82 2 0.02 0–1 0.008
Stephanostomum carangis Intestine 2017 97 1.03 1 0.01 0–1 0.004
(Yamaguti, 1951) Caballero, 1952
Synaptobothrium apharei (Yamaguti, Intestine 11,004 2016O 36 2.78 2 0.06 0–2 0.011
1970) Leon-Regagnon, Perez-Ponce 11,005 2017 97 4.12 8 0.08 ± 1.4 1–4 1 0.014
de Leon & Lamothe-Argumedo, 2018N 51 7.84 6 0.12 ± 1 1–3 0.67 0.033
1997 2019 110 5.45 7 0.06 ± 0.4 1–2 0.14 0.023
Monogenea
Heteromicrocotyla carangis Gills 2019 110 0.91 1 0.01 0–1 0.004
Yamaguti, 1953
Neobenedenia melleni (MacCallum, Gills 2019 110 0.91 1 0.01 0–1 0.004
1927) Yamaguti, 1963
Neomicrocotyle pacificah (Meserve, Gills 10,992 2016M 65 86.15 899 13.83 ± 15.5 1–57 15.06 0.314
1938) Yamaguti, 1968 10,993 2016O 36 44.44 262 7.28 ± 21.2 2–76 27.19 0.174
2017 97 91.75* 2271 23.41 ± 19.5 1–103 14.88 0.317
2018M 63 85.71 589 9.35 ± 10.9 1–61 10.85 0.386
2018N 51 62.75 718 14.08 ± 39.1 1–184 67.98 0.260
2019 110 80.91 2818 25.62 ± 31.4* 1–142 31.10 0.343
Protomicrocotyle manterih Bravo- Gills 10,994 2016M 65 63.08 199 3.06 ± 5.1 1–20 5.26 0.230
Hollis, 1966 10,995 2016O 36 47.22 229 6.36 ± 18.3 1–76 24.98 0.184
2017 97 45.36 114 1.18 ± 2.6 1–13 2.66 0.157
2018M 63 46.03 67 1.06 ± 1.5 1–6 1.02 0.207
2018N 51 56.86 173 3.39 ± 8.4 1–45 11.82 0.236
2019 110 60.00 265 2.41 ± 4.3 1–24 4.62 0.254
Pseudomazocraes seleneh Hargis, Gills 10,996 2016M 65 1.54 1 0.02 0–1 0.006
1957 2016O 36 13.89 13 0.36 ± 3.1* 1–8 3.58 0.054
2017 97 1.03 1 0.01 0–1 0.004
2018M 63 3.17 9 0.14 ± 3.5 1–7 2.78 0.014
2018N 51 19.61* 16 0.31 ± 1 1–4 0.58 0.081
2019 110 12.73 19 0.17 ± 0.5 1–2 0.18 0.054
(Continued on next page)
 J. Violante-González et al.: Parasite 2020, 27, 6 5

Table 1. (Continued)
Parasite taxa Site on Accession Year nb Prevalence Totalc Abundanced Range of DIf ICIg
host numbera (%) intensitye
Cestoda
Tetraphyllidea gen. sp.h Intestine 2016O 36 16.67* 18 0.50 ± 2.7 1–8 2.40 0.065
2017 97 3.09 3 0.03 0–1 0.011
2018N 51 7.84 8 0.16 ± 0.8 1–3 0.33 0.033
2019 110 0.91 1 0.01 0–1 0.004
Acanthocephala
Rhadinorhynchus sp. Intestine 2018N 51 1.96 7 0.14 0–7 0.008
2019 110 1.82 2 0.02 0–1 0.008
Nematoda
Anisakis sp.h larvae Mesentery 2016M 65 4.62 6 0.09 ± 1.7 1–4 1.50 0.017
2016O 36 5.56 3 0.08 ± 0.7 1–2 0.33 0.022
2017 97 16.49* 31 0.32 ± 1.4 1–6 1.06 0.057
2018M 63 6.35 4 0.06 0–1 0.029
2019 110 6.36 10 0.09 ± 0.8 1–3 0.43 0.027
Contracaecum sp. larvae Mesentery 2018N 51 1.96 1 0.02 0–1 0.008
Procamallanus sp. Intestine 2019 110 0.90 1 0.01 0–1 0.004
Copepoda
Bomolochus sp. Gills 123 2016O 36 2.78 1 0.03 0–1 0.011
Caligus alalongaeh Krøyer, Gills 120 2016M 65 9.23 6 0.09 0–1 0.034
1863 2016O 36 8.33 3 0.08 0–1 0.033
2017 97 22.68* 54 0.56 ± 1.8* 1–7 1.39 0.078
2018M 63 3.17 2 0.03 0–1 0.014
2018N 51 1.96 1 0.02 0–1 0.008
2019 110 0.91 1 0.01 0–1 0.004
Caligus chorinemi Krøyer, Gills 121 2017 97 2.06 2 0.02 0–1 0.007
1863 2019 110 8.18 10 0.09 ± 0.3 1–2 0.10 0.035
Caligus robustush Bassett- Gills 122 2016M 65 40.00 41 0.63 ± 0.7 1–4 0.31 0.146
Smith, 1898 2016O 36 44.44 30 0.83 ± 1.3 1–5 0.84 0.174
2017 97 32.99 49 0.51 ± 0.6 1–3 0.21 0.114
2018M 63 38.10 51 0.81 ± 1.8 1–7 1.49 0.172
2018N 51 49.02 44 0.86 ± 1.2 1–5 0.77 0.203
2019 110 50.91 89 0.81 ± 0.8 1–4 0.36 0.216
Caligus mutabilis Wilson, Gills 2017 97 1.03 1 0.01 0–1 0.004
1905
Ergasilus sp. Gills 2016O 36 8.33 4 0.11 ± 0.6 1–2 0.25 0.033
2018N 51 5.88 3 0.06 0–1 0.024
2019 110 1.82 2 0.02 0–1 0.008
Lernanthropus ilishaeh Chin, Gills 124 2016O 36 5.56 2 0.06 0–1 0.022
1948 2017 97 9.28 11 0.11 ± 0.7 1–3 0.36 0.032
2018M 63 17.46* 13 0.21 ± 0.4 1–2 0.14 0.079
2018N 51 1.96 1 0.02 0–1 0.008
2019 110 15.45 19 0.17 ± 0.3 1–2 0.10 0.065
Isopoda
Gnathia sp. Gills 2019 110 2.73 3 0.03 0–1 0.012
2018M 63 1.59 36 0.57 0–36 0.007
Rocinella signata Schioedte & Gills 125 2016O 36 2.78 1 0.03 0–1 0.011
Meinert, 1879 2018N 51 1.96 1 0.02 0–1 0.008
2019 110 0.91 1 0.01 0–1 0.004
a
Specimens deposited at the CNHE (Colección Nacional de Helmintos, Instituto de Biología, Universidad Nacional Autónoma de México).
b
Number of fish examined.
c
Total number of individual parasites collected.
d
Number of parasites per fish (mean ± SD).
e
Minimum to maximum number of parasites present.
f
Variance to mean ratio.
g
Infracommunity index.
h
Component species.
Subscripts to the right of the sampling year indicate the sampling month: M = May, O = October, N = November.
*Significantly different measurements of prevalence (G-test) and abundance (two-way ANOVA) (p < 0.05).
6 J. Violante-González et al.: Parasite 2020, 27, 6

number of species (GLM; F3,406 = 3.95, p < 0.01) and the mean
number of individuals (GLM; F3,406 = 10.72, p < 0.01) were
highest in March 2019 (Table 2), although mean diversity
(H0 ) did not exhibit significant variation between sampling
years (p > 0.05). Dominance of the monogenean N. pacifica
at the infracommunity level was very similar to that at the
component level (Table 2). Considering all samples, the mean
number of species (rs = 0.368, p < 0.01), and the mean diver-
sity (rs = 0.098, p < 0.05) exhibited negative correlations with
host body size of fish, while the mean number of individual
parasites was positively correlated (rs = 0.313, p < 0.01). The
infracommunity index values (ICI) indicated that N. pacifica,
Pr. manteri, and Ca. robustus had the highest number of double
or multiple co-occurrences with other parasite species (ICI
mean > 0.15) in all the sampling years (Table 1).

Multivariate analyses

Figure 1. Box plot of species number of ectoparasites (monogenean The KMO (0.476) and the Bartlett’s tests results
and crustacean), and endoparasites (larvae and adults) in Caranx (v2 = 2,944.2; df = 45, p < 0.001) for the PCA, applied to iden-
sexfasciatus from Acapulco Bay. The bottom and top of the boxes tify the influence of biotic and abiotic factors on parasite infra-
represent the lower and upper quartiles respectively; the median is community structure (Fig. 3), indicated that there is a sufficient
shown as a line through the centre of the boxes; outliers are indicated relationship between the number of variables studied and the
with circles for ectoparasites and asterisks for endoparasites. sample sizes, confirming the relevance of the PCA. The first
three component variables generated by the model explained
61.9% of total variance, contributing 24.9% (eigenvalue = 3.74),
(<65%, Fig. 2) and was higher at the qualitative level 19.8% (eigenvalue = 2.97), and 17.2% (eigenvalue = 2.58). The
(mean = 64.05%) than at the quantitative level first variable suggests that the richest and most diverse infra-
(mean = 56.15%). communities among all the sampled years were characterized
by a significant number of ectoparasite and endoparasite com-
Infracommunity ponent species, with more homogeneous species abundances.
The second variable indicated that both the total number of
The body size of individuals of C. sexfasciatus varied from ectoparasites and the parasite load per infracommunity were
19.0 ± 1.3 cm (October 2016) to 28.8 ± 4.5 cm (August 2017) highest in larger hosts with a more varied diet. The third vari-
(Table 2), and it differed significantly between sampling years able associated host diet with the environmental factors that
(ANOVA F3,402 = 32.3, p < 0.01). Mean species richness of were studied (Table 3). This variable indicated that host diet
parasites ranged from 2.22 ± 1.30 to 2.96 ± 1.54, and the mean was more varied during the dry season when water surface
number of individual parasites per fish from 12.71 ± 11.5 to temperature was slightly cooler (as suggested by the negative
31.50 ± 30.35 (Table 2). The Brillouin diversity index (H0 ) correlations), which occurred mainly during the final sampling
values varied from 0.53 ± 0.48 to 0.71 ± 0.58. The mean year (Tables 2 and 3).

Table 2. Characteristics of the parasite component communities and infracommunities of Caranx sexfasciatus from Acapulco Bay, Mexico.
Year Date SST °C Salinity No. Length Diet Component communities Infracommunities
(ppt) fish (cm)
Species No. of BPI Dominant % of H Mean Mean Mean value
richness parasites species dom. number number of Brillouin
infra. of species of parasites Index
d
2016a May 28 34.9 65 23.9 ± 4.5 0.68 8 1271 0.707 Neom 73.8 0.90 2.70 ± 1.10 19.5 ± 16.79 0.70 ± 0.41
2016b Octr 30 34.4 36 19.0 ± 1.3 0.90 14 670 0.391 Neom 13.9 1.15 2.56 ± 1.83 18.61 ± 27.86 0.71 ± 0.58*
2017 Augr 30 34.6 97 28.8 ± 4.5 0.96 18 2663 0.853 Neom 88.7 1.25 2.89 ± 1.30 27.4 ± 20.1.37 0.56 ± 0.43
2018a Mayd 29 34.8 63 26.7 ± 3.1 0.70 11 801 0.735 Neom 74.6 1.04 2.22 ± 1.30 12.71 ± 11.50 0.53 ± 0.48
2018b Novr 30 33.6 51 24.0 ± 3.5 1.0 18 996 0.721 Neom 47.0 1.25 2.41 ± 1.25 19.53 ± 33.98 0.64 ± 0.44
2019 Mard 28 34.1 110 26.5 ± 5.9 1.1 25 3465 0.813 Neom 64.5 1.40 2.96 ± 1.54* 31.50 ± 30.35* 0.61 ± 0.49

SST = sea surface temperature, Length = total length, Diet = diet variety, BPI = Berger-Parker Index; % of dom. infra = percentage of
dominated infracommunities, H = Shannon-Wiener diversity index, Neom = Neomicrocotyle pacifica.
*Significant at p < 0.05. Letters as superscripts represent codes of assignment ranges of locations and climatic seasons (d = dry, r = rainy) used
in the multivariate statistical analysis.
 J. Violante-González et al.: Parasite 2020, 27, 6 7

tests showed that the four sampling years were significantly

different in both dimensions (v2 = 110.37, df = 15,
p < 0.001). Each fish was correctly assigned to one of the four
sampling years with a 41.1% accuracy, more than double that
achieved by chance alone (16%).
Of the nine component species (i.e. prevalence > 10%),
only five were accepted by the model (Table 4) based on their
lower Wilks’ lambda values. High abundance of the
monogenean Pr. manteri and lower abundance of the digenean
E. virgulus were characteristic of hosts collected in 2016. The
monogenean N. pacifica and the copepod L. ilishae effectively
functioned to identify hosts that were collected in 2019, while
the copepods Ca. alalongae and L. ilishae effectively distin-
guished between hosts collected in 2017 and 2018.

Figure 2. Similarity percentages (Bray-Curtis index) for parasite Discussion

communities of Caranx sexfasciatus between sampling years.
d = dry season, r = rainy season. Parasite community species composition
All the present parasite species records (23 helminths and
nine crustaceans) are new geographical records for C. sexfascia-
tus on the Pacific coast of Mexico (Table 1). Ectoparasites (five
monogeneans, seven copepods, and two isopods) numerically
dominated the parasite communities, representing 92.71% of
the total number of individual parasites recovered. This pre-
dominance is probably due to the monogeneans’ transmission
strategies (direct contact), increasing their transmission proba-
bilities especially in gregarious fish such as C. sexfasciatus
[27, 42]. Eight of the reported monogenean species (including
N. pacifica, Pr. manteri, and Ps. selene) have been recorded
in Carangidae from the Pacific coast of Mexico [32]. Copepods
are a highly diverse group that mainly parasitize marine fish
[22, 28, 45]; however, this crustacean group has received lim-
ited attention in Mexico [14]; in the present study, they were
the second most diverse group and represented 22% of the total
taxa recovered (Table 1).

Interannual variation in parasite infection levels

Figure 3. Scatter plot of the principal component analysis (PCA) of
At least five species of parasite (two endoparasites –
factors that influence the species richness and diversity of the
parasite infracommunities of Caranx sexfasciatus, from Acapulco B. varicus and a tetraphyllidean cestode, and three ectoparasites
Bay. Predictor variables: Year = sampling year, Season = climatic – N. pacifica, Ps. selene and Ca. alalongae) exhibited signifi-
season (dry/rainy), Temp = surface temperature values, Enso = cant interannual differences in infection levels (Table 1).
Multivariate El Niño index, Size = host body size (total length), Endoparasites often are trophically transmitted, so variations
Kn = condition factor, Diet = host diet variety, EndoR = number of in infection levels can be explained by interannual changes in
endoparasite species, EctoR = number of ectoparasite species, host diet and availability of prey harboring infective stages
EndoT = total number of endoparasites per host, EctoT = total [16, 18, 23, 38]. The population density and gregarious behav-
number of ectoparasites per host. Infracommunity parameters: ior (schooling behavior) of C. sexfasciatus [2] may be a better
Richness = number of parasite species per infracommunity, explanation for the annual variation observed in the three
Diversity = Brillouin diversity index values, Load = total number
species of ectoparasites. Fish that form large schools facilitate
of parasites per infracommunity, Evenness = species evenness.
ectoparasite transmission, particularly parasites with a direct
transmission cycle such as monogeneans and copepods [14,
In the model constructed to identify possible interannual 23, 39, 41, 51].
differences in parasite community structure, the first two
discriminant variables explained 86.9% of the total variance, Dispersion pattern
contributing 56.2% (eigenvalue = 0.164) and 30.6% (eigen-
value = 0.090). A significant overall group effect was observed The DI values indicated that at least 31% of the species of
(Wilks’ lambda = 0.759, p < 0.001). Individual fish were parasites exhibited aggregate dispersion in one or more of the
mainly distributed along the first axis (Fig. 4). Dimensionality sampling years (Table 1). Aggregation is considered a typical
8 J. Violante-González et al.: Parasite 2020, 27, 6

Table 3. Summary of the principal component analysis (PCA) on biotic and abiotic factors that influence the diversity and species richness of
the infracommunities of Caranx sexfasciatus. The three principal component axes are indicated by PC1, PC2 and PC3, respectively. Variables
that contribute to the total explained variance in each PC are in bold. Eigenvalues, percentage of variance, and accumulative variance are
shown at the end of the table. Communality = total influence of the variable with respect to all other associated variables.
Uniqueness = percentage of variability that is not predicted by the variable in the model.
Communality Uniqueness
Variables PC1 PC2 PC3 R2 % not predicted
Richness 0.961 0.050 0.045 0.928 0.072
Diversity 0.892 0.355 0.024 0.922 0.078
EctoR 0.709 0.005 0.200 0.543 0.457
EndoR 0.705 0.085 0.167 0.532 0.468
EndoT 0.667 0.075 0.070 0.455 0.545
Evenness 0.594 0.590 0.048 0.703 0.297
EctoT 0.148 0.904 0.095 0.848 0.152
Load 0.244 0.894 0.082 0.865 0.135
Size 0.171 0.633 0.033 0.431 0.569
Kn 0.123 0.351 0.156 0.162 0.838
Diet 0.135 0.339 0.336 0.246 0.754
Temp 0.007 0.102 0.842 0.720 0.280
Enso 0.027 0.066 0.892 0.692 0.308
Season 0.073 0.159 0.785 0.646 0.354
Year 0.016 0.189 0.746 0.592 0.408
Eigenvalue 3.74 2.97 2.58
% total variance 24.9 19.8 17.18
Accumulative variance 24.9 44.7 61.9

Predictor variables: Year = sampling year, Season = climatic season (dry/rainy), Temp = surface temperature values, Enso = Multivariate El
Niño index, Size = host body size (total length), Kn = condition factor, Diet = host diet variety, EndoR = number of endoparasite species,
EctoR = number of ectoparasite species, EndoT = total number of endoparasite per host, EctoT = total number of ectoparasite per host.
Infracommunity parameters: Richness = number of parasite species per infracommunity, Diversity = Brillouin diversity index values,
Load = total number of parasites per infracommunity, Evenness = species evenness.

the digeneans B. varicus and Ectenurus virgulus; and the

nematode Anisakis sp.) suggest the existence of differences in
host exposure rates to parasites. Differing exposure rates could
be due to the influence of local environmental factors [35], or
the differences in host feeding behavior revealed in the diet
analysis. In contrast, some contact-transmitted parasites such
as monogeneans, exhibit high host specificity and can be
more abundant in larger fish that form schools [23, 29], like
C. sexfasciatus. Some studies also suggest that DI values can
be influenced by sample size [33, 35], but there was no positive
correlation between DI values and sample sizes in the present
analysis.

Component communities
The parasite communities in C. sexfasciatus exhibited
similar patterns at the component and infracommunity levels:
low species numbers (2.22–2.96 species on average per host),
Figure 4. Graphic of multivariate discriminant analyses for parasite low species diversity, and dominance by a single species (the
communities of Caranx sexfasciatus. The symbols represent each monogenean Pr. manteri, Table 2). Species richness at the
one of the fish examined in each sampling year. Centroid = mean component level (8–25 species, Table 2) is similar to that
group. reported previously in other Caranx species in the Americas,
such as C. hippos (19 species), C. latus (17 species), and
C. caballus (18 species) [15, 21]. However, overall parasite
dispersion pattern of parasites in marine fish [3, 18, 37]. fauna of C. sexfasciatus included 32 species across the four
However, the widely variable aggregation levels of five hel- sampling years. The broad geographical distribution of
minth species (the monogeneans N. pacifica and Pr. manteri; C. sexfasciatus may explain this greater overall richness since
 J. Violante-González et al.: Parasite 2020, 27, 6 9

Table 4. Discriminant analysis classification showing the numbers and percentages of the Caranx sexfasciatus classified in each sampling year
(rows correspond to group memberships). The bottom of the table shows the matrix of classification coefficient values for parasites that
allowed differentiation among sampling years; coefficient values in bold indicate the importance of each species of parasite in distinguishing
among years.
Sampling year 2016 2017 2018 2019 Percent
2016 22 7 57 10 22.9
2017 5 22 41 28 22.9
2018 3 3 81 19 76.4
2019 8 5 53 42 38.9
Parasite
Protomicrocotyle manteri 0.135 0.030 0.063 0.068
Neomicrocotyle pacifica 0.021 0.044 0.024 0.048
Ectenurus virgulus 0.349 0.112 0.056 0.032
Caligus alalongae 0.214 1.239 0.052 0.089
Lernanthropus ilishae 0.070 0.961 0.982 1.389

hosts with a broad geographical distribution are exposed to total parasite load, as suggest by the global positive correlation
large numbers of parasite species by interaction with myriad (r = 0.633) recorded for this variable in the PCA (Table 3). In
intermediate host species throughout their distribution range marine fish, body size has proved to be the main predictor of
[40]. Species composition similarity between the parasite com- total parasite abundance [23, 39, 40]. A large body size can
munities (Fig. 2) was considered generally low at both levels facilitate parasite colonization, since larger individuals tend to
(qualitative and quantitative levels: <65%), compared to the ingest greater quantities of food and are older and thus have
similarity recorded for parasite communities of other marine had more time to accumulate parasites than smaller individuals
fish examined on the Mexican Pacific coast, such as Caranx [39, 40]. However, the negative correlations registered between
caballus 78.5% [14], Oligoplites altus 85% [39], or Parapsettus host body size and species richness and diversity parameters
panamensis 76% [51]. This low similarity can be attributed to suggest that the richest and most diverse parasite infracommu-
the fact that 47% (15 species: six ectoparasites and nine nities were recorded in smaller rather than larger fish. Onto-
endoparasites) of the identified parasite species occurred only genic changes in the feeding habits [10, 11, 20, 51] of
in one or two sampling years (Table 1). This suggests that C. sexfasciatus can explain the broad dietary diversity in smal-
annual variations in biotic (e.g. diet, body size, availability of ler fish (for example, October 2016 and November 2018 sam-
larva-infected prey) and/or abiotic environmental factors ples, Table 2). This would in turn raise infracommunity species
[14, 23, 39, 49, 51], may have been responsible for the low richness and diversity in these individuals (Table 2), as indi-
similarity between the parasite communities of C. sexfasciatus cated in the diet analysis. Parasites are known to be useful as
observed in the present study. biological tags in distinguishing between fish stocks of the same
species [47, 54], but the parasite fauna method has rarely been
used to quantify possible variations in community structure and
Infracommunities species composition over time. The discriminant analysis
results (Table 4) indicated that the high variation in the infection
Several biotic and abiotic factors are known to strongly
levels of at least five parasite species (the monogeneans N. paci-
influence species richness and diversity in the parasite
fica and Pr. manteri; the digenean E. virgulus; and the cope-
communities of marine fish over time [14, 23, 34, 39, 48,
pods Ca. alalongae and L. ilishae) may generate substantial
51]. The PCA results (Fig. 3) indicated that infracommunity
changes in the parasite community structure of C. sexfasciatus
species richness and diversity depended heavily on the occur-
over time. In other words, even though community species
rence of a distinctive set of component species (both ecto-
composition remains relatively stable, its structure may be less
and endoparasite species). However, these component species’
predictable.
frequency or abundance varied between sampling years
Overall, the parasite communities of C. sexfasciatus were
(Table 1). Temporal variations in parasite infracommunity struc-
characterized by high numerical dominance of ectoparasites,
ture and species composition have been attributed to variations
mainly monogenean species. Community structure and species
in the prevalence and/or abundance of some dominant taxa [4,
composition varied between sampling years and climatic sea-
14, 16, 38, 39, 51]. As the ICI results suggest, the ectoparasites
sons. Despite occurrence of a distinctive set of host-specialist
N. pacifica, Pr. manteri, and Ca. robustus play an important
parasites (monogenean species), similarity between the
role in structuring the parasite infracommunities of C. sexfascia-
component parasite communities was generally low. Seasonal
tus. Due to ease of transmission through direct contact, ectopar-
or local variations in some biotic (e.g. feeding behavior, body
asite populations contribute substantially to the structuring of
size, and infected prey availability) and abiotic environmental
infracommunities in gregarious fish such as carangids [23, 29,
factors are possible sources of the observed interannual
31]. Fluctuations in the infection levels of some endoparasite
variations in C. sexfasciatus parasite community structure and
species (e.g. B. varicus and the Tetraphyllidean cestode) can
species composition.
be attributed mainly to changes in C. sexfasciatus diet or forag-
ing habitat, both between sampling years and climatic seasons Acknowledgements. The authors thank the fishermen who caught
(dry/rainy). Host body size was an important predictor of the the fish at each sampling date, as well as the students of the Marine
10 J. Violante-González et al.: Parasite 2020, 27, 6

Ecology Academic Unit (UAGro) for their assistance with field and 15. Gallegos-Navarro Y, Violante-González J, Monks S, García-
laboratory work. Four anonymous reviewers provided useful com- Ibáñez S, Rojas-Herrera AA, Rosas-Acevedo JL. 2019. Meta-
ments that substantially improved this manuscript. zoan parasite communities of Selar crumenophthalmus and
Decapterus muroadsi (Pisces: Carangidae) from Mexican
Pacific coasts. New Zealand Journal of Marine and Freshwater
Research, 53(3), 377–396.
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Cite this article as: Violante-González J, Monks S, Gallegos-Navarro Y, Santos-Bustos NG, Villalba-Vasquez PJ, Padilla-Serrato JG &
Pulido-Flores G. 2020. Interannual variation in the metazoan parasite communities of bigeye trevally Caranx sexfasciatus (Pisces,
Carangidae). Parasite 27, 6.
12 J. Violante-González et al.: Parasite 2020, 27, 6

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