Volume11,Number1(ene-jun2017)

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

Lima-Perú

VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

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Neotropical Helminthology, 2017, 11(1), jan-jun: 167-186.

REVIEW ARTICLE/ ARTÍCULO DE REVISIÓN

COMPARISON OF BIODIVERSITY PARASITIC OF PARALABRAX CLATHRATUS

(GIRARD, 1854) AND P. HUMERALIS (VALENCIENNES, 1828) (PISCES: SERRANIDAE)

FROM THE EASTERN PACIFIC

COMPARACIÓN DE LA BIODIVERSIDAD PARASITARIA DE

PARALABRAX CLATHRATUS (GIRARD, 1854) Y P. HUMERALIS (VALENCIENNES, 1828)

(PISCES: SERRANIDAE) DEL PACÍFICO ORIENTAL

1 Laboratorio de Parasitología, Departamento Académico de Biología Marina, Universidad Autónoma de Baja California Sur.

Ap. P. 19-B. La Paz, B.C.S. 23080, México.

2 Departamento de Plancton y Ecología Marina, Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional.

La Paz, B.C.S. 23096, México.

3 Laboratorio de Ecología y Biodiversidad Animal (LEBA), Facultad de Ciencias Naturales y Matemática (FCNNM),

Universidad Nacional Federico Villarreal (UNFV), El Agustino, Lima, Perú.

4 Facultad de Ciencias Biológicas, Universidad Ricardo Palma (URP), Santiago de Surco, Lima, Perú.

mcgomez@uabcs.mx/joseiannacone@gmail.com

Neotropical Helminthology

167

ABSTRACT

Parasite biodiversity of the groupers Paralabrax clathratus (Girard, 1854) and P. humeralis (Valenciennes,

1828) (Pisces: Serranidae) from the eastern pacific, host specificity of the parasites and the role groupers play in

the life cycle of the parasite is presented. The information is a compilation of records generated by various

authors. It was found that the parasite biodiversity of both fish species is grouped into 22 families (helminths

and crustaceans), two orders and one class. Paralabrax humeralis was infested with a richer diversity of

parasites than P. clathratus (n=40 vs n=27): monogeneans (n=3 vs n=3), digeneans (n=10 vs n=10), tapeworms

(n=6 vs n=1), acanthocephalans (n=2 vs n=1), nematodes (n=9 vs n=4), copepods (n=8 vs n=8), isopods (n=1 vs

n=0) and hirudinea (n=1 vs n=0). Of this parasite richness, it was observed that hosts share ten families:

Diclidophoridae and Capsalidae (Monogenea), Hemiuridae and Opecoelidae (Digenea), Polymorphidae

(Acantocephala), Anisakidae and Cucullanidae (Nematoda), Caligidae, Bomolochidae and Hatschekiidae

(Copepoda). Sörensen qualitative index that was used to compare the biodiversity of parasites at the family

level and at the species level for P. clathratus and P. humeralis which showed a value of 57.14% and 11.94%,

respectively. Despite this difference, a similar proportion of larvae and adult parasites were observed, as well as

in the life cycle types and at the site of infection (ectoparasites and endoparasites) between both species of

Paralabrax. On the other hand, parasites showing some host specificity towards groupers are copepods of

family Hatschekiidae and tapeworms Trypanorhyncha that parasitize elasmobranches fish in adult stage. The

remaining parasites are considered generalists. Tapeworms, acanthocephalans and anisakid are registered in the

larval stages indicating that Paralabrax use paratenic as intermediate hosts in their life cycles. Monogeneans,

copepods and digeneans were adult forms suggesting that P. clathratus and P. humeralis are the definitive hosts.

The observed differences in parasite richness of the hosts may be due to specific environmental conditions, the

presence of different intermediate hosts, the feeding behavior of the host and host specificity.

Keywords: crustaceans – host specicity – helminths – Paralabrax clathratus – P. humeralis

1 1,2 3 3,4

María del Carmen Gómez del Prado-Rosas ; Horacio Lozano-Cobo ; Lorena Alvariño & José Iannacone

Neotropical Helminthology, 2017, 11(1), jan-jun

RESUMEN

Se presenta la biodiversidad parasitaria de Paralabrax clathratus (Girard, 1854) y P. humeralis

(Valenciennes, 1828) (Pisces: Serranidae) del Pacífico Oriental, su especificidad hospedatoria y el papel

que desempeñan en el ciclo de vida de los parásitos. La información es una compilación de los registros de

diversos autores durante la revisión de los parásitos de los peces estudiados. Se encontró que la

biodiversidad parasitaria de ambas especies de peces está agrupada en 22 familias (entre helmintos y

crustáceos), dos órdenes y una clase. Paralabrax humeralis presenta mayor riqueza parasitaria que P.

clathratus (n = 40 vs n = 27): monogeneos (n = 3 vs n = 3), digéneos (n = 10 vs n = 10), céstodos (n = 6 vs n

= 1), acantocéfalos (n = 2 vs n = 1), nemátodos (n = 9 vs n = 4), copépodos (n = 8 vs n = 8), isópodos (n = 1

vs n = 0) e hirudineos (n = 1 vs n = 0). De esta riqueza parasitaria, se observó que los hospederos comparten

diez familias: Diclidophoridae y Capsalidae (Monogenea), Opecoelidae y Hemiuridae (Digenea),

Polymorphidae (Acantocephala), Anisakidae y Cucullanidae (Nematoda), Caligidae, Bomolochidae y

Hatschekiidae (Copepoda). El índice de Sörensen cualitativo que sirvió para comparar la biodiversidad

parasitaria a nivel de familia y de especie de P. clathratus y P. humeralis mostró un valor de 57,14% y de

11,94%, respectivamente. A pesar de esta diferencia, se observó una proporción similar de parásitos en los

estadios larval y adulto, así como en los tipos de ciclos de vida y en el sitio de infección (ectoparásitos y

endoparásitos) entre ambas especies de Paralabrax. Por otro lado, los parásitos que muestran cierta

especificidad hospedatoria hacia serránidos son los copépodos de la familia Hatschekiidae y los céstodos

del orden Trypanorhyncha que parasitan a peces elasmobranquios en estado adulto, el resto se consideran

parásitos generalistas. Los céstodos, acantocéfalos y anisákidos registrados son formas larvarias

indicando que utilizan a Paralabrax como hospederos intermediarios o paraténicos en sus ciclos de vida.

Los monogéneos, digéneos y copépodos son formas adultas lo que sugiere que P. clathratus y P. humeralis

son sus hospederos definitivos. Las diferencias observadas en la riqueza parasitaria de los hospederos

pueden deberse a condiciones específicas del ambiente, de la presencia de diferentes hospederos

intermediarios, del comportamiento alimentario y de su posible especificidad hospedatoria.

INTRODUCTION

The species of the subfamily Serraninae have

sedentary behavior and are predators that feed on

fish and benthic invertebrates, mainly crustaceans

(Fischer et al., 1995; Pérez-Matus et al., 2012).

Some species are hermaphrodites, because

individuals function as males and females at the

same time. Other species change sex, from females

to males during their lifetime, but several have

separate sexes (Aburto-Oropeza et al., 2008).

Phylogenetically Serraninae is the basal subfamily

of the Serranidae family.

Paralabrax Girard, 1856 is one of the 13 genera of

the subfamily Serraninae (Nelson, 2006); forms a

monophyletic group of American distribution

(Pondella et al., 2003). Composed of nine valid

species divided into two phylogeographic groups:

1) the group of North America, composed of P.

clathratus (Girard, 1854), P. nebulifer (Girard,

The family Serranidae Swainson, 1839 consisting

of 537 species is one of the eight most diverse

families of teleosteos fish (Nelson, 2006; Froese &

Pauly, 2006; Eschmeyer & Fong, 2015). The

Serranid has great commercial importance for

artisanal, recreational and industrial fishery in the

world and several species are highly valued in the

market aquaristik (Aburto-Oropeza et al., 2008).

These predominantly tropical or subtropical fish of

often demersal behavior live on the continental

shelves, from the shore to moderate depths (rarely

greater than 200 m). Most live associated with

coral reefs and rocky bottoms, although some live

in seagrass beds, and muddy and sandy bottoms

(Fischer et al., 1995; Cisternas & Sielfeld, 2008).

168

Gómez del Prado-Rosas et al.

Palabras claves: crustáceos – especificidad hospedatoria – helmintos – Paralabrax clathratus – P. humeralis

1854), P. auroguttatus Walford, 1936, and P.

maculatofasciatus (Steindachner, 1868), and 2) the

group of Central and South America, made up of P.

humeralis (Valenciennes, 1828), P. loro Walford,

1936, P. albomaculatus (Jenyns, 1840), P.

callaensis Starks, 1906 and P. dewegeri

(Metzelaar, 1919) (Pondella et al., 2003) (Fig. 1).

This genus is considered the basal taxon in the

subfamily Serraninae (Pondella et al., 2003;

Sadovy & Domeier, 2005; Martínez-Brown et al.,

2012).

The genus Paralabrax includes mesocarnivorous

fish, dominant components of the rocky

environment and marine reef of the Eastern Pacific

and Western Atlantic of the American Continents.

Their dominance has made them commercially and

ecologically important, and therefore they have

been subject to intensive fishing (Pondella et al.,

2003). The basal limbs of the Paralabrax genus, P.

clathratus and P. humeralis, are the most species

representatives of the group (Pondella et al., 2003).

P. clathratus is distributed from the Columbia

River, Washington, USA to Bahía Magdalena,

BCS, Mexico and P. humeralis from Colombia to

southern Chile (Fischer et al., 1995). P. clathratus

according to its conservation status is considered to

be of minor concern and P. humeralis as deficient

data (IUCN, 2015a, b).

In South America, several comparative studies of

eumetazoan parasite communities in congeneric

freshwater and marine fish have been carried out in

recent years. In the erythrinoids Hoplias

malabaricus Bloch, 1794 and H. lacerdae Miranda

Ribeiro, 1908 in Brazil (Rosim et al., 2010). In the

labrisomids Auchenionchus microcirrhis

(Valenciennes, 1836), A. variolosus (Valenciennes,

1836) and A. crinitus (Jenyns, 1842) in Chile

(Muñoz & Castro, 2012). In the blennids

Scartichthys variolatus (Valenciennes, 1836), S.

viridis (Valenciennes, 1836) and S. gigas

(Steindachner, 1876) in Chile (Díaz & Muñoz,

2010), among others. However to date there is no

information on the comparative biodiversity of the

parasitofauna of P. clathratus and P. humeralis

despite being species of high ecological and

economic relevance for each geographic region in

which they are distributed. Therefore, this paper

presents the comparative analysis of the parasitic

biodiversity of P. clathratus and P. humeralis from

the Eastern Pacific.

Neotropical Helminthology, 2017, 11(1), jan-jun

169

Biodiversity parasitic of two species of Paralabrax

The information presented is an exhaustive

compilation of the records generated by several

authors of the parasitic fauna eumetazoa in the two

species of fish studied (P. clathratus and P.

humeralis). Records in scientific articles,

unpublished thesis and cybernetic information

search portals such as "Google Scholar" were taken

into account. The taxonomic classification

followed the Cohen et al. (2013) nomenclature for

the monogeneans, Yamaguti (1971), Gibson et al.

(2002), Jones et al. (2005) and Bray et al. (2008)

for the digeneans. Heinz & Dailey (1974) and

Schmidt (1986) for tapeworms and Moravec

(2006) for nematodes was used. Petrochenko

(1971) and Amin (2013) were used for

acanthocephalans and Luque & Tavares (2007) for

crustaceans. At the level of order the classification

of parasites of Ruggiero et al. (2015) was used.

Comparison of beta parasite biodiversity at family

and species level (P. clathratus and P. humeralis)

was measured using the Sörensen (Is) qualitative

similarity index: Is = (2c*100 /a+b), where a =

number of parasite families / species present in P.

clathratus, b = number of parasite families / species

present in P. humeralis, and c = number of parasite

families / species present in both species of

Paralabrax. This index varies between 0 when

there are no families / species of parasites present in

both species of Paralabrax, up to 100% when for

all species of Paralabrax all the families / species

of parasites are the same (Iannacone et al., 2010,

Calderón- Patrón et al., 2012; Bernués-Bañeres &

Jiménez-Peydró, 2013). The Chi-square statistic

was used to determine whether the same proportion

of larvae and adults of metazoan parasites, direct

and indirect biological cycle of parasites, and

metazoan ectoparasites and endoparasites exist

between P. clathratus and P. humeralis at a level of

significance of 0.05 (Preacher, 2001).

Comparative parasite biodiversity of both species

of fish was found to be constituted of helminths and

crustaceans grouped into 22 families, two orders

MATERIAL AND METHODS

RESULTS

0.57). The same proportion of metazoan

ectoparasites in the fish host (44.44% in P.

clathratus and 32.5 % in P. humeralis) (Chi-square

= 0.79, p = 0.37) and metazoan endoparasites in the

fish host (55.56% in P. clathratus and 67.5% in P.

humeralis) (Chi-square = 0.58, p = 0.44).

Of the 22 parasite families, two orders and one

class present in P. clathratus and P. humeralis, 10

of them (40%) are probably shared as a result of

their phylogenetic kinship as clades of the North

American and Central-South American groups

respectively (Pondella et al., 2003; Sadovy &

Domeier, 2005; Martínez-Brown et al., 2012).

However, it turned out that the biodiversity of

metazoan parasites at the family level between

these two species is not shared in 60% of cases.

This maybe due to differences in the composition

of marine invertebrates that serve as intermediate

hosts and habitats that serve as food, recruitment,

larval settlement and reproduction of each species

of fish (Cisternas & Sielfeld, 2008). The

distribution of P. humeralis on the coasts of Peru

and Chile is frequently associated with two

subsystems of kelps, Lessonia trabeculata Villouta

& Santelices and Macrocystis integrifolia Bory de

Saint-Vincent (Cisternas & Sielfeld, 2008; Ortiz,

2010; Henríquez & González, 2012). While P.

clathratus, although it is a species considered to be

close to algae grasslands in southern California and

northern Baja California (Quast, 1968; Miller &

Lea, 1972; Erisman & Allen, 2005, 2006) has been

more frequently associated with rocky-type coral

habitats (Stephens et al., 1984; Gómez del Prado-

Rosas, 2012). Possibly due to this habitat

difference there is a greater parasitic biodiversity in

P. humeralis with respect to P. clathratus.

Monogeneans of the family Diclidophoridae,

Pseudotagia clathratus and Mamaevicotyle

villalobosi have not been registered in other

species of fish, but Hemitagia galapagensis was

found in Paranthias furcifer (Valenciennes, 1828)

and Tagia sp. which has been found in a greater

variety of fish species (Lamothe-Argumedo, 1984;

Gómez del Prado-Rosas, 2012; Cohen et al., 2013).

In all cases, both species of groupers act as final

hosts of monogeneans.

and one class. P. humeralis presented higher

parasite richness at the species level than P.

clathratus (n = 40 vs n = 27): monogeneans (n = 3

vs n = 3), digeneans (n = 10 vs n = 10), tapeworms

(n = 6 vs n = 1), acanthocephalans (n = 2 vs n = 1),

nematodes (n = 9 vs n = 4), copepods (n = 8 vs n =

8), isopods (n = 1 vs n = 0) and hirudinean (n = 1 vs

n = 0) (Table 1). The 27 species of metazoan

parasites of P. clathratus were found in the USA

(14.81%) and in Mexico (88.88%). In contrast, the

40 species of metazoan parasites of P. humeralis

were Galapagos-Ecuador (12.5%), Peru (40%) and

Chile (67.5%) (Table 1).

From this parasite richness, it was observed that

both hosts share ten families: Diclidophoridae and

Capsalidae (Monogenea), Opecoelidae and

Hemiuridae (Digenea), Polymorphidae

(Acanthocephala), Anisakidae and Cucullanidae

(Nematoda), Caligidae, Bomolochidae and

Hatschekiidae (Copepoda). It was also observed

that P. clathratus does not share families:

Monorchiidae and Zoogonidae (Digenea) and

Spiruridae (Nematoda). P. humeralis does not

share the families: Derogenidae (Digenea),

Bothriocephalidea (unidentified family),

Lacistorhynchidae, Tentacularidae and

Diphyllobothriidae (Cestoda), Philometridae and

Cystidicolidae (Nematoda), Lernaeopodidae and

Chondracanthidae (Copepoda), Cymothoidae

(Isopoda) and an unidentified family of Hirudinea

(Table 1). The qualitative Sörensen index was used

to compare parasite biodiversity at the family and

species levels of P. clathratus and P. humeralis, and

showed a value of 11.94% and 57.14%,

respectively. Only four parasitic species: H. nimia,

A n i s a k i s s p . , C o r y n o s o m a s p . a n d

Hysterothylacium sp. were present in both species

of grouper, P. clathratus and P. humeralis.

A similar proportion of larvae relative to total

parasite load was observed in both fish species

(14.81% in P. clathratus and 26.83% in P.

humeralis) (Chi-square = 1.75, p = 0.18) and adults

(85.19% in P. clathratus and 73.17% in P.

humeralis) (Chi-square = 0.46, p = 0.50) for

metazoan parasites. The same proportion of

metazoan parasites with direct biological cycle

(40.74% in P. clathratus and 32.5% in P.

humeralis) (Chi-square = 0.43, p = 0.51) and

indirect biological cycle (59.26% in P. clathratus

and 77.5% in P. humeralis) (Chi-square = 0.32, p =

Neotropical Helminthology, 2017, 11(1), jan-jun

170

Gómez del Prado-Rosas et al.

DISCUSSION

Neotropical Helminthology, 2017, 11(1), jan-jun

171

Biodiversity parasitic of two species of Paralabrax

Shared Locality Reference

Order Family families Genus/Species

Host (Country)

Monogenea

Mazocraeidea

Diclidophoridae

Yes

Pseudotagia clathratus Crane, 1972 A, D Pc USA Crane (1972)

Mamaevicotyle villalobosi Lamothe, 1984

A, D Pc Mexico

Gómez del Prado-Rosas

(2012)

Tagia sp.

A, D Ph Peru Armas (1977)

Chile

Henríquez

González

(2012)

Hemitagia galapagensis (Meserve, 1938)

Sproston, 1946

A, D

Galápagos

Kohn & Cohen (2003)

Peru

Iannacone & Alvariño

(2009)

Capsaloidea

Capsalidae

Yes

Bajacaliornia universitaria

Gómez del Prado & Lamothe, 2009

A, D

Mexico

Gómez del Prado-Rosas

(2012)

Neobenedenia

sp.

A, D

Chile

Henríquez

& González

(2012)

Digenea

Plagiorchiida

Opecoelidae

Yes

Helicometrina nimia

Linton, 1910

A, I

Mexico

Arai (1962)

Chile

Oliva & Muñoz (1985);

Muñoz & Olmos (2008);

Henríquez

& González

(2012);

González et al.

(2013);

Oliva et al. (2015)

Table 1. Biodiversity of shared and non-shared metazoan parasite families among Serranids Paralabrax clathratus (Pc) and P. humeralis (Ph). A = Adult stage. L

= larvae stage. D = Direct biological cycle. I = Indirect biological cycle. NI = Not indicated.

Neotropical Helminthology, 2017, 11(1), jan-jun

172

Gómez del Prado-Rosas et al.

Shared Locality

Order Family families Genus/Species Host (Country)

Odhner, 1902

A, I

Chile

Oliva & Muñoz (1985);

Kohn et al. (2007);

Muñoz & Olmos (2008);

Henríquez

& González

(2012); González et al.

(2013)

Peru

Iannacone & Alvariño

(2009)

Helicometra pulchella (Rudolphi, 1819)

Odhner, 1902

A, I

Peru

Tantaleán et al. (1975)

Plagioporus isaitschikowi

(Layman, 1930) Price, 1934

A, I

USA

Manter & Van Cleave

(1951)

Mexico

Druk-González (1983)

Opecoelus mexicanus Manter, 1940

A, I

Mexico

Gómez del Prado-Rosas

(2012)

Opecoelus lutiani (Bravo Hollis & Manter,

1957) Aken´Ova, 2007

A, I

Mexico

Gómez del Prado-Rosas

(2012)

Pseudopecoelus

sp.

A, I

Chile

Henríquez

& González

(2012)

Macvicaria

sp.

A, I

Chile

Henríquez

& González

(2012)

Macvicaria calotomi (Yamaguti, 1934)

Gibson & Bray, 1982 A, I Pc Mexico Gómez del Prado-Rosas

(2012)

Macvicaria issaitschikowi (Layman, 1930)

Bray, 1985 A, I Pc Mexico Gómez del Prado-Rosas

(2012)

Reference

Helicometra fasciata (Rudolphi, 1819)

Neotropical Helminthology, 2017, 11(1), jan-jun

173

Biodiversity parasitic of two species of Paralabrax

et al.

Opecoelidae gen. sp.1

A,I

Chile

Henríquez & González

(2012)

Opecoelidae gen. sp.2

A,I

Chile

Henríquez & González

(2012)

Plagiorchiida

Hemiuridae

Yes

Parahemiurus merus (Linton, 1910)

Vaz &

Pereira, 1930

A, I

Mexico

Gómez del Prado-Rosas

(2012)

Ellytrophallus mexicanus Manter, 1940

A, I

Mexico

Manter & Van Cleave

(1951)

Lecithochirium microstomum

Chandler, 1935

A, I

Galápagos

Manter (1940)

Lecithiochirium magnaporum Manter, 1940

A, I

Galápagos

Manter (1940); Kohn

(2007);

Iannacone & Alvariño

(2009)

Plagiorchiida

Derogenidae

Yes

Derogenes varicus (O.F. Müller, 1784)

Looss, 1901

A, I

Galápagos

Manter (1940); Kohn

(2007);

Iannacone & Alvariño

(2009)

Plagiorchiida

Monorchiidae

Monorcheides alexanderi Arai, 1962

A, I

Mexico

Arai (1962); Gómez del

Prado (2012)

Plagiorchiida Zoogonidae No

Deretrema (Deretrema) pacicum

Yamaguti, 1942 A, I Pc Mexico Gómez del Prado-Rosas

(2012)

Cestoda

Bothriocephalidea NI No Bothriocephalidea gen. sp. A, I Ph Chile Henríquez & González

(2012)

Trypanorhyncha NI No Trypanorhyncha sp. L, I Pc Mexico Gómez del Prado-Rosas

(2012)

Shared Locality

Order Family families Genus/Species Host (Country)

Reference

Neotropical Helminthology, 2017, 11(1), jan-jun Gómez del Prado-Rosas et al.

Trypanorhyncha

Lacistorhynchidae

Grillotia

sp.

L, I

Peru

Armas (1977); Tantaleán &

Huiza (1994);

Iannacone & Alvariño

(2009)

Callitetrarhynchus

sp.

L, I

Peru

Armas (1977)

Callitetrarhynchus

gracilis (Rudolphi, 1819)

L, I

Peru

Tantaleán & Huiza (1994);

Iannacone & Alvariño

(2009)

Tentaculariidae

Nybelinia sp.

L, I

Chile

Henríquez

González

(2012)

Diphyllobothriidea

Diphyllobothriidae

Adenocephalus pacicus Nybelin, 1931

L, I

Peru

Iannacone & Alvariño

(2009)

Acanthocephala

Polymorphida

Polymorphidae

Yes

Corynosoma

sp.

L, I

Mexico

Gómez del Prado-Rosas

(2012)

Chile

Muñoz & Olmos (2008);

Henríquez & González

(2012)

Peru Armas (1977); Tantaleán et

al. (2005)

Corynosoma obtuscens Lincicome, 1943 L, I Ph Chile Muñoz & Olmos (2008)

Peru Tantaleán et al. (2005)

Nematoda

Ascaridida Anisakidae Yes

Anisakis sp. L, I Pc Mexico Gómez del Prado-Rosas

(2012)

Ph Chile Henríquez & González

(2012)

Shared Locality

Order Family families Genus/Species Host (Country)

Reference

174

Neotropical Helminthology, 2017, 11(1), jan-jun

175

Biodiversity parasitic of two species of Paralabrax

Shared Locality

Order Family families Genus/Species Host (Country)

Reference

Anisakis simplex

(Rudolphi, 1809)

L, I

Chile

Jofré et al. (2008);

Iannacone & Alvariño

(2009)

Hysterothylacium

sp.

L, I

Mexico

Gómez del Prado-Rosas

(2012)

L, A, I

Chile

Henríquez

& González

(2012)

Ascaridida

Cucullanidae

Yes

Cucullanus

sp.

A, I

Mexico

Gómez del Prado-Rosas

(2012)

Cucullanellus

sp.

A, I

Peru

Armas (1977)

Dichelyne (Cucullanellus) sp.

A, I

Peru

Sarmiento et al. (1999);

Iannacone & Alvariño

(2009)

Camallanida

Philometridae

Philometra sp.

A, I

Chile

Oliva et al. (1992);

Henríquez

& González

(2012)

Peru Muñoz & Olmos (2008);

Sarmiento et al.

(1999); Iannacone &

Alvariño (2009)

Rhabditia Cystidicolidae No

Cystidicolidae gen. sp.1 A, I Ph Chile Henríquez & González

(2012)

Ascarophis sp. A, I Ph Chile Henríquez & González

(2012)

Pseudoascarophis sp. ? A, I Ph Chile Henríquez & González

(2012)

Spiruroidea Spiruridae No

Dollfusnema piscícola

Caballero-Rodríguez, 1974 A, I Pc Mexico Caballero-Rodríguez

(1974)

Neotropical Helminthology, 2017, 11(1), jan-jun

176

Gómez del Prado-Rosas et al.

Copepoda

Siphonostomatoida

Caligidae

Yes

Caligus mutabilis Wilson, 1905

A, D

Mexico

Causey (1960);

Gómez del Prado-Rosas

(2012)

Caligus productus

Dana, 1853

A, D

Mexico

Causey (1960)

Caligus elongatus

von Nordmann, 1832

A, D

Mexico

Gómez del Prado-Rosas

(2012)

Caligus quadratus

(Shiino, 1954)

A, D

Chile

Muñoz & Olmos (2007);

Henríquez

& González

(2012);

Peru Iannacone & Alvariño

(2009)

Lepeophtheirus dissimulatus Wilson, 1905 A, D Ph Galápagos Wilson (1937)

Lepeophtheirus longipes Wilson, 1905 A, D Pc USA Wilson (1921)

Lepeophtheirus frecuens

Castro-Romero & Baeza-Kuroki, 1984 A, D Ph Chile Henríquez & González

(2012)

Siphonostomatoida Lernaeopodidae No

Clavella sp. A, D Ph Chile Henríquez & González

(2012)

Cyclopoidea Bomolochidae Yes

Bomolochidae gen. sp. A, D Ph Chile Henríquez & González

(2012)

Acantholochus paralabracis

Luque & Bruno, 1990 A, D Ph Peru Luque & Bruno (1990);

Iannacone & Alvariño

(2009)

Shared Locality

Order Family families Genus/Species Host (Country)

Reference

Neotropical Helminthology, 2017, 11(1), jan-jun

177

Biodiversity parasitic of two species of Paralabrax

Shared Locality

Order Family families Genus/Species Host (Country)

Reference

Siphonostomatoida

Hatschekiidae

Poecilostomatoida Chondracanthidae

Isopoda

Cymothoida Cymothoidae

Hirudinea

Bomolochus longicaudus Cressey, 1969

Bomolochus soleae Claus, 1864

Yes

Hatschekia albirubra Wilson, 1913

Hatschekia amphiprocessa

Castro & Baeza, 1986

Hatschekia pacica Cressey, 1970

Juanettia cornifera Wilson, 1921

Meinertia sp.

No Hirudinea gen. sp.

A, D

USA

A, D

Mexico

A, D

Mexico

A, D Ph Chile

Peru

A, D Pc Mexico

A, D Ph Chile

L, D Ph Chile

A, D Ph Chile

Cressey (1969)

Causey (1960)

Castro & Baeza-Kuroki

(1986);

Muñoz & Olmos (2007);

Henríquez & González

(2012)

Luque et al. (1991);

Iannacone & Alvariño

(2009)

Gómez del Prado-Rosas

(2012)

Stuardo & Fagetti (1961);

Muñoz & Olmos (2007)

Henríquez & González

(2012)

Henríquez & González

(2012)

Opecoelidae is a family well represented in marine

fish, with species that can be used to assess the

health of the aquatic ecosystem.

Helicometrina nimia is a digenean trematode with

wide distribution in the world (Roumbedakis et al.,

2014) that is located in the intestine and stomach of

fish. It has been registered to date in more than 60

fish species, mainly of the families Serranidae,

Haemulidae Gill, 1885 (Syn = Pomadasyidae),

Scorpaenidae Risso, 1827 and Clinidae Swainson,

1839 in 13 countries: United States of America,

Regarding the digeneans, although they are

generalists, only the families Opecoelidae and

Hemiuridae were found in both fish species

probably reflecting the fact that groupers are their

definitive hosts when these helminths are found in

adult stage (Gibson & Bray, 1982; Bray, 1985;

Aken'Ova, 2007; Iannacone et al., 2011).

Opecoelidae was the family that presented the

greatest diversity of species (n = 12) in the genus

Paralabrax. Bray et al. (2016) notes that this is the

largest family of digenea with 90 genera and about

900 species. Derbel et al. (2012) notes that

Neotropical Helminthology, 2017, 11(1), jan-jun

178

Gómez del Prado-Rosas et al.

Figure 1. Geographical distribution of Paralabrax spp. of the phylogeographic group of North America (P. clathratus, P.

auroguttatus, P. nebulifer and P. maculatofasciatus) and of the phylogeographic group of Central and South America (P.

humeralis, P. loro, P. albomaculatus, P. callaensis and P. dewegeri).

parasites of the second family are generalist

(Cressey, 1969). The copepods Caligidae are

among the ectoparasites with the most species

richness in Paralabrax. Regarding to Juanettia

cornifera there are only one record of this species

in P. humeralis (Stuardo & Fagetti, 1961;

Yamaguti, 1963b). In all cases, the groupers are

their definitive hosts (Muñoz & Olmos, 2007).

The monogenean Bajacalifornia universitaria is a

capsalid that was found in adult stage in P.

clathratus and could be occurs in other two species

of Paralabrax (P. nebulifer and P. auroguttatus) in

the Pacific ocean of the Peninsula of Baja

California and Gulf of California, Mexico

respectively. For this monogenean the Paralabrax

groupers are the definitive hosts (Gómez del

Prado-Rosas, 2012)..

The digenean Monorcheides alexanderi of the

family Monorchiidae, seems so far, preference for

fish of the genus Paralabrax. Because it had

previously been recorded in P. clathratus from Isla

Guadalupe, Mexico (Arai, 1962), in P. nebulifer

from Ensenada, Baja California, Mexico (Druk-

González, 1983) and in P. maculatofasciatus from

El Pardito, Bahía de La Paz, Baja California Sur,

Mexico (Gómez del Prado-Rosas, 2012). While

Deretrema (Deretrema) pacificum of the family

Zoogonidae is considered as generalist (although

part of a genus with nine species) because it has

been found in fish of the families Labridae,

Monocentridae, Pempheridae, Triglidae and the

order Scorpaeniformes. However, D. (D.)

pacificum has been described in fish belonging to

the following orders: Scorpaeniformes,

Perciformes and Beryciformes (Linton, 1910;

Gómez del Prado-Rosas, 2012). Derogenes varicus

of the family Derogenidae is a parasite of little host

specificity because it has been found in a great

variety of fishes (Yamaguti, 1971), so due to its

attributed a wide geographical distribution.

The records of tapeworms belong to the orders

Trypanorhyncha and Diphyllobothriidea were in

larval stage (plerocercoid), while the order

Bothriocephalidea was in adult stage. Khalil et al.

(1994) mentioned that adult of these parasites are in

elasmobranch fish and marine mammals. The

presence in larval stage indicating that the

Paralabrax spp. are only an intermediate or

paratenic host in the cycle of these parasites

Bahamas, Jamaica, Puerto Rico, Mexico, Panama,

Colombia, Peru, Brazil, Chile, the Arabian Gulf,

Pakistan and India (Vélez, 1987; Pérez-Ponce de

León et al., 2007; Iannacone & Alvariño, 2011;

Roumbedakis et al., 2014; Oliva et al., 2015;

Ramos-Ascherl et al., 2015; Sowjanya et al., 2015;

Merlo-Serna & García-Prieto, 2016). H. nimia has

been recorded in both species of grouper studied

here, P. clathratus and P. humeralis (Table 1).

On the other hand, the acanthocephalans registered

in both species of groupers belong to the genus

Corynosoma in larval stage. Aznar et al. (2006)

point out that in the marine ecosystem the

cystacanths of Corynosoma species are most

frequently in fishes, which act as paratenic hosts

and serve as a link between intermediate hosts

(mainly crustacean-amphipods) and definitive

hosts (marine mammals) (Yamaguti, 1963a; Aznar

et al., 2006). Although recently Lozano-Cobo et al.

(2017) propose the chaetognaths as a new

intermediate host in the life cycle of the

Corynosoma species due to the presence of 12

cystacanths in three species of chaetognaths in a

monthly zooplankton time series of three years

(1996 to 1998). Tantaleán et al. (2005) and Chero et

al. (2014) mentioned that Paralabrax spp. are only

an intermediate or paratenic host in the life cycle of

these acanthocephalans and we consider the same.

Regarding nematodes, the species recorded in the

family Anisakidae (Anisakis sp., A. simplex and

Hysterothylacium sp.) are cosmopolitan (Gómez

del Prado-Rosas, 2012; Luque et al., 2016). All

correspond to larval forms and indicate the role of

Paralabrax spp. in the Anisakidae life cycle as

intermediate or paratenic hosts, because of

Anisakis spp. have marine mammal as definitive

hosts and Hysterothylacium spp. have fish as

definitive hosts (Anderson, 2000). Nematodes of

the family Cucullanidae [Cucullanus sp. and

Dichelyne (Cuculanellus) sp.] are generalists

(Yamaguti, 1961) and in the Paralabrax spp. were

found in the adult stage, so that the groupers are

definitive hosts for these nematodes (Luque et al.,

2016).

The coincidence of copepods corresponding to the

families Hatschekiidae, Caligidae and

Bomolochidae is an indicator of the preference

that shown the first family by serranid fish (Jones,

1985; Castro & Baeza-Kuroki, 1986). While the

Neotropical Helminthology, 2017, 11(1), jan-jun

179

Biodiversity parasitic of two species of Paralabrax

study. P. clathratus may have a maximum length of

72 cm while P. humeralis can measure a maximum

length of 55 cm. In this sense we would be expected

to have higher parasite richness in P. clathratus

than P. humeralis. Contrary to this, the diversity

was higher in P. humeralis (n = 40) than in P.

clathratus (n = 27), so that differences in size

between the two hosts were not a factor in

determining their parasitic biodiversity.

Although both species are carnivorous, P.

clathratus has a greater spectrum of prey (benthic

and planktonic invertebrates, cephalopods and

fish) (Roberts et al., 1984; Henríquez & González,

2012). In contrast, the diet of P. humeralis is

dominated mainly by decapod crustaceans and to a

lesser extent by invertebrates and fish (Love et al.,

1996; Pérez-Matus et al., 2012). Although, P.

clathratus has a greater spectrum of prey, this host

did not have a greater richness of parasites that

could be transmitted trophically (digeneans,

tapeworms and nematodes) in comparison to P.

humeralis. Lowe et al. (2003) and Pérez-Matus et

al. (2012) indicated that P. clathratus and P.

humeralis have greater residence to their

geographic distribution and have little variation in

diet. Lira-Guerrero et al. (2008) indicate that

differences in the diet of host carnivorous fish

species could cause differences in the interactions

with their prey that are their possible intermediate

hosts. It is likely that the differences in the parasitic

richness of endoparasites in P. clathratus and P.

humeralis can be attributed to the general behavior

of hosts that can modulate the loss and acquisition

of new parasites (Henríquez & González, 2012).

Luque & Oliva (1999) and Rosim et al. (2010)

indicate that the unstable environmental conditions

in the aquatic environment would cause a

disturbance in the population dynamics of the

endoparasites transmitted trophically in

Paralabrax. As can be seen with the outcrop

systems in the Peruvian cold current and in the

California current where both species of grouper in

this study (P. humeralis and P. clathratus) are

distributed respectively. Also being periodically

affected by the El Niño event which may represent

a direct influence on the distribution of parasites

(Marcogliese, 2008). Henríquez & González

(2012) point out that the differences in the

composition of ectoparasites (monogeneans,

copepods, isopods and hirudineans) in P. humeralis

(Iannacone & Alvariño, 2009; Gómez del Prado-

Rosas, 2012; Luque et al., 2016). Adenocephalus

pacificus in plerocercoid larvae was found only in

P. humeralis. Kutcha et al. (2015) mentioned that

marine fish such P. humeralis act as a second

intermediate host and these fish would be part of

the marine mammal diet (Iannacone & Alvariño,

2009; Chero et al., 2014).

The nematode Dollfusnema piscicola of the family

Spiruridae, apparently, has not been registered in

another host in Mexico. P. clathratus is the type

host (Gibbons, 2010). While the nematode

Philometra sp. of the family Philometridae,

generally parasitizes a great diversity of fishes

(Yamaguti, 1961).

Respect to copepods, the members of the family

Chondracanthidae are recorded parasitizing a wide

variety of marine fish, but in particular the copepod

Juanettia cornifera has been found only in P.

humeralis of Isla Juan Fernández, Chile (Stuardo &

Fagetti, 1961; Yamaguti, 1963b; Muñoz & Olmos,

2007).

As regards the presence of families of parasites

non-shared between the two species of groupers (P.

clathratus and P. humeralis) could be indicate: 1)

particular conditions of the environment in the

geographical distribution; 2) presence of different

intermediary hosts; 3) more specific food behavior

and 4) a certain degree of host specificity of each

parasite (Manter, 1967; Díaz & Muñoz, 2010). It is

also considered that the absence of overlap in the

distribution of host fish could reduce the similarity

of species and families of parasites among

congeneric hosts (Díaz & Muñoz, 2010). P.

clathratus is a subtropical species that is

distributed from Columbia River, Washington,

USA to Bahía Magdalena, BCS, Mexico and P.

humeralis is a tropical species from Colombia to

southern Chile (Fischer et al., 1995). There are

families of parasites that do not coincide between

both species of Paralabrax despite being

congeneric species.

Henríquez & González (2012) and Muñoz &

Castro (2012) indicated that the variation in the

community of parasites among species of fish of

the same family would be to the sizes of the hosts,

observing a greater diversity in the larger fish.

However, this condition was not observed in this

Neotropical Helminthology, 2017, 11(1), jan-jun

180

Gómez del Prado-Rosas et al.

of four localities from Chile could be attributed to

different circulation models of water bodies. that

would affect the dispersal ability of the infective

larval stages of these ectoparasites. The richness of

ectoparasites in P. humeralis and P. clathratus can

be explained by this factor.

The results of this comparative study of helminth

and crustacean parasites between P. clathratus and

P. humeralis reflect possible differences in the

parasite richness of two congeneric hosts. Even

though they are species that come from the same

monophyletic group, the evidence of the

phylogeographic importance of these two hosts is

clear and reflected in the families of parasites that

were not shared. Probably the parasitic fauna in the

species of the genus Paralabrax has greater

similarity between those species of the same

phylogeographic group than between species of

different distribution. This would mean that the

parasitic biodiversity of P. clathratus would be

similar to that of P. maculatofasciatus, P. nebulifer

and P. auroguttatus because they belong to the

North American group (Fig. 1). While P. humeralis

would be more similar to the parasites of P. loro, P.

albomaculatus, P. callaensis and P. dewegeri

belonging to the Central and South American

group (Pondella et al., 2003) (Fig. 1). However it

would be necessary to analyze if there are

differences in the parasitic biodiversity among the

species of each phylogeographic group. This

review represents one of the first comparative

studies of parasitic richness among congenital

basal species of a monophyletic group of marine

environment in any Teleosteos fish family.

Therefore it is advisable to continue efforts to

better understand the factors that determine the

differences in parasitic biodiversity of host species

of monophyletic origin.

Neotropical Helminthology, 2017, 11(1), jan-jun

181

Biodiversity parasitic of two species of Paralabrax

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C & Danemann, G. 2008. Serránidos de

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California: Ecología, Pesquerías y

Conservación. Ciencia y Conservación,

vol.1, pp.1-23.

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