The aim of this investigation was to describe for the first time the parasitic copepod attached to the skin of
the yellowfin tuna fish Thunnus albacares (Bonnaterre, 1788) in the state of Sinaloa along the Mexican
Pacific coast. Five copepods were identified as Pennella filosa L. (Copepoda:Pennellidae), members of
this genus are characterized by shape, size and the length of the parasite, type of host, arrangement of
cephalothoracic papillae, segmentation of the first and second antenna, and structure of the abdominal
plumes among the most important. This study is significant because it is the first time that this copepod of
the family Pennelidae is described parasitizing this tuna fish Thunnus albacares which is a high-valued
fish species that are caught year-round by both the coastal commercial and recreational fishing in Sinaloa,
Mexico. Although there are several reports worldwide, locally is a new geographical distribution area for
this copepod and thus contributes to our understanding of the biology, the biodiversity and host preference
of these parasites.
ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
FIRST RECORD OF PENNELLA FILOSA L. (COPEPODA, SIPHONOSTOMATOIDA,
PENNELLIDAE) PARASITISING THE YELLOWFIN TUNA THUNNUS ALBACARES
(BONNATERRE, 1788) FROM THE MEXICAN PACIFIC COAST
PRIMER REGISTRO DE PENNELLA FILOSA L. (COPEPODA, SIPHONOSTOMATOIDA,
PENNELLIDAE) PARASITANDO AL ATUN DE ALETA AMARILLA THUNNUS ALBACARES
(BONNATERRE, 1788) EN LA COSTA DEL PACÍFICO MEXICANO
1Facultad de Ciencias del Mar. Universidad Autónoma de Sinaloa. Apartado Postal 610.
Mazatlán, Sinaloa, México. C.P. 82000.
2Centro Interdisciplinario de Ciencias Marinas. IPN. Apartado Postal 592. La Paz, Baja California Sur, México. C.P. 23000.
Phone number (612-12) 25344. Fax: (612-12) 2 5322.
3Universidad Autónoma de Occidente, Av. del Mar 1200, Flamingos, 82149, Mazatlán, Sinaloa, México
*Corresponding author: E-mail: fgalvan@ipn.mx
ABSTRACT
Keywords: Copepoda – ectoparasites – Tuna – Pacific Ocean – México
Neotropical Helminthology
109
Volume13,Number1(jan-jun2019)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Auspiciado por:
Neotropical Helminthology, 2019, 13(1), ene-jun:109-114.
1 2 2*
Cristóbal Román-Reyes José ; Sofía Ortega-García ; Felipe Galván-Magaña
1,3
& Mayra I. Grano-Maldonado
110
RESUMEN
El objetivo de esta investigación fue describir por primera vez al copépodo ectoparásito en la piel del atún
aleta amarilla Thunnus albacares (Bonnaterre, 1788) en el estado de Sinaloa en las costas del Pacífico
mexicano. Se identificaron cinco copépodos Pennella filosa L. (Copepoda: Pennellidae), los miembros de
este género se caracterizan por la forma, el tamaño y la longitud del parásito, el tipo de hospedero, la
disposición de las papilas cefalotorácicas, la segmentación de la primera y la segunda antena, y la
estructura de las plumas abdominales. Este estudio es significativo porque es la primera vez que se
describe este copépodo de la familia Pennelidae que parasita al atún Thunnus albacares, que es
considerado una especie de pez de gran valor que se captura todo el año tanto por la pesca costera
comercial como por la pesca recreativa en Sinaloa. México. Aunque existen varios informes en todo el
mundo, localmente es una nueva área de distribución geográfica para este copépodo y, por lo tanto,
contribuye a nuestra comprensión de la Biología, la biodiversidad y la preferencia de hospedadores de
estos parásitos.
Palabras clave: Copepoda – ectoparásitos – Atún – Océano Pacíco – México
INTRODUCTION studies on this fish from the Eastern Pacific Ocean
have been published, some of them recorded only
trematodes endoparasites species (Nikolaeva,
1985; Kazachenko & Titar, 1985) also few
copepods (Rodríguez-Santiago et al., 2015). The
ectoparasite Pennella filosa Linnaeus, 1758 was
described by Pollock (1994) from the pectoral fin
of an albacore tuna Thunnus alalunga and from the
pelvic fin and dorsal surface of 2 out of 20
swordfish Xiphias gladius Linnaeus, 1758. Also,
Tanrikul & Akyol (2011) described specimens of
Pennella filosa on swordfish from the Turkish
Aegean sea. Other parasitic studies on tuna
Thunnus thynnus Linnaeus, 1758 and amberjack
Seriola dumerili (Risso, 1810) aquaculture in
Turkey (Tuncer et al., 2010; Toksen et al., 2012). In
the mediterranean some works have been focused
on ecological aspects of P. filosa from Coryphaena
hippurus Linnaeus, 1758 These authors revealed a
possible transmission factor during the migratory
period from the strait of Gibraltar to the Balearic
Islands (Alboran Sea) where squid and cuttlefishes
are abundant. According to Kabata (1979, 1981)
cephalopods may be intermediate hosts in Penella
sp. Oken, 1815 life cycle.
Other authors, like Bullard et al., (2015)
characterized lesion-associated capsaline
infections (Capsala biparasiticum) (Goto, 1894)
Price, 1938 on T. albacares in the Gulf of Mexico,
and other records in the Pacific showed that mako
shark Isurus oxyrinchus Rafinesque, 1810 is
parasitized by the copepod Dinemoura producta
(Müller, 1785) and striped marlin Kajikia audax
In the northwestern coasts of Mexico, the yellowfin
tuna (Thunnus albacares) (Bonnaterre, 1788)
(Family Scombridae) is high-valued fish species
that are caught year-round by both the coastal
commercial and recreational fishing in Mazatlán,
Sinaloa (northwest Pacific). T. albacares
contributes to many national food fisheries
(Shomura et al., 1994) and according with the
Inter-American Tropical Tuna Commission
(IATTC) are the largest and main catches of
yellowfin tuna in the Eastern Pacific Ocean which
is obtained by the Mexican tuna fleet. The analysis
of the parasites species composition in high-valued
fish species are of interest because studies have
shown that parasites can reduce host density
causing that some populations could be
endangered to extinction (Dobson & Hudson,
1986). Some parasites have been used as indicators
of specific features of host ecology (Konovalov &
Butorina, 1985). Parasitological studies in wild
animals are important because they lead to a better
understanding of the behavioral links between the
host and parasite (Lamothe-Argumedo et al.,
1997). This knowledge may help in understanding
copepod parasite life cycles in marine ecosystems.
In the case of T. albacares these ectoparasites may
have a negative effect on fisheries in economic
terms (Rodriguez-Santiago et al., 2015).
Yellowfin tuna is an important fishing species with
worldwide distribution and few parasitological
Román-Reyes et al.
Neotropical Helminthology, 2019, 13(1), ene-jun
111
MATERIAL AND METHODS
the northwest of the Pacific coast. These
ectoparasites were attached mainly to the
dorsolateral anterior and posterior muscular tissue
(Fig. 2). Parasitic copepods are the second and third
largest group on Neotropical marine and
freshwater fishes, respectively (Luque & Poulin
2008). In accordance with Boxshall (2013), most
of the copepods infecting teleost fish and
elasmobranchs are mainly members of the order
Siphonostomatoida, which consist of 39 families.
Copepods from the genus Pennella Oken, 1816
have been recorded as large parasites found in the
flesh of a wide range of marine hosts (Kabata,
1992), and P. filosa is one species found on large
fishes (Scombridae, Molidae) (Hogans, 1987);
however, reports of occurrence of this parasitic
specie on yellowfin tuna are not documented in
Mexico.
Pennellidae family shows a two-host cycle, and
some teleosteans and cephalopods have been
reported as intermediate host (Grabda, 1991).
Approximately 700 species of 173 genera of
parasitic copepods on marine fishes have been
recorded in the Pacific Ocean, and only 60 were
reported in the Eastern Pacific Ocean (Kazachenko
& Titar, 1985; Rodríguez-Santiago et al., 2015).
These records increased the existing information
concerning the parasitic fauna associated to
yellowfin tuna in the Eastern Pacific Ocean, and
according with Carbonell et al. (1999), P. filosa is
potentially useful as a biological tag for studying
their migratory movements and stock
differentiation. Also these large, and very easily
seen ectoparasite produce a prominent scar after
their death. This finding allowed the existing
information concerning the parasitic fauna of
yellowfin tuna in the Pacific Ocean to be extended.
Further studies on parasites are required for
characterization of ecto and endoparasites, in order
to understand the transmission, life cycle,
pathology and possible control treatments. Several
reports are available on parasites from fish species
in different parts of the world, however, this work
shows the presence of P. filosa in specific part of
the Mexican coast and that could be useful to
conduct the comparative studies with other
ectoparasites mainly copepods on fish and other
aquatic systems. This information could be of
particular interest by parasitologist groups working
on diseases, infections, tranmsisison, ecological
factors, and migration in marine fish.
(Philippi, 1887) by P. filosa (González-Armas et
al., 2013). Furthermore, other authors described
the acanthocephalan Echinorhynchus Müller, 1776
sp. infection of T. albacares from India (Sakthivel
et al., 2014). In this context, there are no records of
the occurrence of the specie P. filosa in yellowfin
tuna in Mexico. This fish is an important economic
resource for both consumption and fishing
activities. The knowledge of a parasite contributes
to understand essential links between them and its
host, and to the basic knowledge on the copepod
biology.
The fish host was a large yellowfin tuna (94.3 cm
fork length and 14.5 kg weight), that had been
caught during the summer by a sport fishing boats,
at least 300 miles west off Mazatlan, Sinaloa Port in
Mexico (106º 24.5' N y 23º 12.5' W) (Fig.1).
Ectoparasites were attached mainly to the
dorsolateral anterior and posterior muscular tissue
(Fig. 2). The fish was washed with freshwater in
situ and the washed material was transported in
individual plastic bags in a cool box to the
laboratory. The examination of copepods on the
body surface of the fish was performed under good
illumination in a Petri dish using a Leica MZ9.5
stereomicroscope. The plastic bag contents were
also examined for the presence of detached
copepods. Parasites found on the fish were
preserved in labeled vials with 70% etanol and then
glycerol. The identification of the parasitic
copepods was based on the morphometrical similar
features described by Kabata (1979), Hogans
(1987, 1987), Grabda (1991), Benz & Hogans
(1993) and Abaunza et al. (2001).
Ethic aspects: Animal care and handling were
carried out in accordance with Mexican laws
(NOM-033-ZOO-1995).
Five ectoparasites (12.3-15.8 cm; mean 14 cm)
were identified as the ectoparasitic P. filosa
(Copepoda: Pennellidae) collected from the skin of
the tuna fish T. albacares in Mazatlán, Sinaloa in
RESULTS AND DISCUSSION
Pennella losa parasitising Thunnus
Neotropical Helminthology, 2019, 13(1), ene-jun
112
Figure 1. Map location of the coastal waters of Mazatlán, Sin. Mexico.
Figure 2. Yellowfin tuna infected with Pennella filosa (Copepoda: Pennellidae) in coastal waters of Mazatlán, Sin. Mexico.
Román-Reyes et al.
Neotropical Helminthology, 2019, 13(1), ene-jun
113
species known to date. FAO Fish. Synopis.
vol. 2, pp. 125-137.
Cressey, R & Boyle Cressey, H, 1980. Parasitic
copepods of mackerel and tuna´like fishes
Scombridae of the world. Smithsonian
Contribution of Zoology, vol. 311, pp.1-
186.
Delmare-Deboutteville, C & Nunes-Ruivo, L.
1951. Etude de Pennella remorae Murray et
remarques sur la biologie et la systématique
des Pennella Oken. Revista da Faculdade de
Direito da Universidade de Lisboa, vol. 1,
pp. 341-352.
Dobson, A & Hudson, P J. 1986. Parasites disease
a n d t h e s t r u c t u re o f e c o l o g i ca l
communities. Trends in Ecology &
Evolution, vol. 1, pp. 11-15.
García, M, Sureda, M & González González, P.
2010. Pennella filosa (Linnaeus, 1758)
( C o p e p o d a , S i p h o n o s t o m a t o i d a ,
Pennellidae) from Coryphaena hippurus
Linnaeus, 1758 (Pisces, Coryphaenidae)
captured in western Mediterranean
(Balearic Islands). Morphological and
biological aspects. Nereis, Revista
Iberoamericana Interdisciplinar de
Métodos, Modelización y Simulación vol.
3, pp. 33-35.
González- Armas, R, Hernández-Trujillo, S, &
Funes-Rodríguez, R. 2013. Marlin rayado
(Kajikia audax) y tiburón mako (Isurus
oxyrinchus) capturados por la flota
deportiva en Cabo San Lucas, B.C.S.,
parasitados por copépodos. Conference:
XX Congreso Nacional de Ciencia y
Tecnología del Mar, Cabo San Lucas, Baja
California Sur, Mexico, pp.45.
Grabda, J. 1991. Marine fish parasitology. Polish
Scientific Publisher, Warszawa. 306 pp.
Hogans, W. E. 1987. Morphological variation in
Pennella balaenoptera and P. filosa
(Copepoda:Pennellidae) with a review of
the genus Pennella Oken, 1816 parasitic on
cetacea. Bulletin of Marine Science, vol.
40, pp. 442-453.
Inter-American Tropical Tuna Commission. 2018.
Informes mensuales de capturas y datos
2007–2017. Comisión Interamericana del
A t ú n T r o p i c a l .
http://www.iattc.org/MonthlyReports.htm
[accessed Jan 29 2019].
Kabata, Z. 1979. Parasitic Copepoda of British
Abaunza, P, Arroyo, N, L, & Preciado, I. 2001. A
contribution to the knowledge on the
morphometry and the anatomical
characters of Pennella balaenopterae
( C o p e p o d a , S i p h o n o s t o m a t o i d a ,
Pennellidae), with special reference to the
buccal complex. Crustaceana, vol. 74, pp.
193-210.
Benz, G & Hogans, W. 1993. Penella filosa (L.
1758) (Copepoda: Siphonostomatoida)
f ro m t h e e s c o l a r L epi docyb ium
flavobrunneum (Smith, 1849) in the north-
west Atlantic. Systematic Parasitology, vol.
26, pp.127-131.
Boxshall G. 2013. Siphonostomatoida. In: Walter,
TC & Boxshall, G (eds.). World of copepods
d a t a b a s e .
http://www.marinespecies.org/copepoda/a
phia. [accessed Feb 20 2019].
Bullard, SA, Womble, MR, Maynard, MK, Orélis-
Ribeiro, R & Arias, CR. 2015. Skin lesions
on yellowfin tuna Thunnus albacares from
Gulf of Mexico outer continental shelf:
Morphological, molecular, and histological
diagnosis of infection by a capsalid
monogenoid. Parasitology International,
vol. 64, pp. 609-21.
Carbonell, E, Massutí, E, Castro J & García, RM.
1999. Parasitism of dolphin fishes,
Coryphaena hippurus and Coryphaena
equiselis, in the western Mediterranean
(Balearic Islands) and central-eastern
Atlantic (Canary Islands). Scientia Marina,
vol. 63, pp. 343-354.
Caton, A, Colgan, K, Sahlqvist, P, Ward, P,
Ramirez, C & Scott, M.1998. Swordfish,
Xiphias gladius, and the fisheries for tunas
and billfishes in the Australian fishing zone.
In: Barrett, I, Sosa-Nishizaki, O & Bartoo,
N (eds.). Biology and Fisheries of
swordfish, Xiphias gladius. Papers from the
International Symposium on Pacific
swordfish, Ensenada, México, 11-14
December 1994. NOAA Technical Report
NMFS 142.
Collete, B & Nauen, C. 1983. FAO species
catalogue. Vol. 2. Scombrids of the world.
An annotated and illustrated catalogue of
tunas, mackerels, bonitos and related
BIBLIOGRAPHIC REFERENCES
Pennella losa parasitising Thunnus
Neotropical Helminthology, 2019, 13(1), ene-jun
114
NOAA Technical Report NMFS vol. 25.
Pollock, C.M. 1994. Pennella filosa (Copepoda)
parasitic on albacore tuna, sunfish and
swordfish. Irish Naturalists' Journal, vol. 24,
pp. 473-474.
Rodríguez-Santiago, M A, Gómez, S, Rosales-
Casián, J A & Grano-Maldonado, MI.2015.
Parasitic copepods of the Vermilion
Rockfish Sebastes miniatus (Pisces:
Scorpaenidae) from inshore waters of Baja
California (Eastern Pacific). Neotropical
Helminthology, vol. 9, pp. 1-12.
Sakthivel, P & Gopalakrishnan S. 2014.
Acanthocephalan (Echinorhynchus sp.)
infection of yellowfin tuna (Thunnus
albacares) from Nagapattinam, south east
coast of India Journal of Coastal Life
Medicine, vol. 2, pp. 596-600.
Shomura, RS, Majknowski, J & Langi, S. 1994.
Interaction of Pacific tuna fisheries: vol.2
papers on biology and fisheries. Rome,
FAO.
Tanrikul, T & Akyol, O. 2011. First record of the
parasitic Copepoda, Pennella filosa (L.,
1758), on swordfish from the Turkish
Ae gea n Se a. Journal of Applied
Ichthyology, vol. 27, pp. 1392-1393.
Tokşen, E, Nemli, E, Değirmenci, U & Karacalar,
U. 2012. Parasitic diseases and their
controls in sustainable development of
aquaculture of bluefin tuna (Thunnus
rd
thynnus). 3 Int. Symp. Sustainable Dev.
May 31 - June 01 2012, Sarajevo, pp. 41-50.
Tuncer, S, Çelik, EŞ & Öktener, A. 2010. Pennella
filosa (L., 1758) (Copepoda: Pennellidae)
on greater amberjack Seriola dumerili
(Risso, 1810) from Turkey. Electronic
Journal of Ichthyology, vol. 6, pp. 27–30.
Fishes. London: The Ray Society, The
British Museum, London, vol. 152, pp. 1–4.
Kabata, Z. 1981. Copepoda (Crustacea) parasitic
of fishes: problems and perspectives.
Advances in Parasitology, vol. 19, pp. 1-17.
Kabata, Z. 1992. Copepods parasitic on fishes.
Keys and notes for identification of species.
In: Kermack, DM, Barnes, RS & Crothers,
JH (eds.), Synopses of the British Fauna,
(new ser.), vol. 47, pp. 1-264.
Kazachenko, V N & Titar, VM. 1985. Special
features of the geographical distribution
and practical significance of the parasitic
copepods of fishes of the Pacific. In: Hargis,
Jr., WJ (ed.).Parasitology and pathology of
marine organisms of the world Ocean.
NOAA Technical Report NMFS vol. 25.
Konovalov, S M & Butorina, T E. 1985. Parasites
as indicators of specific features of fish
ecology. In:Hargis, Jr., WJ (ed.).
Parasitology and pathology of marine
organisms of the world Ocean. NOAA
Technical Report NMFS vol. 25.
Kurochkin, V. 1985. Applied and scientific aspects
of marine parasitology. In: Hargis, Jr., WJ.
(ed.). Parasitology and pathology of marine
organisms of the world Ocean. NOAA
Technical Report NMFS vol. 25.
Lamothe-Argumedo, R, Garcia-Prieto, L, Osorio
Sarabia, D, & Pérez Ponce De Leon, G.
1997. Catálogo de la Colección Nacional
de Helmintos. Instituto de Biología,
UNAM, CONABIO. México D.F. pp. 211.
Luque, JL & Poulin, R. 2008. Linking ecology with
parasite diversity in neotropical fishes.
Journal of Fish Biology, vol. 72, pp. 189-
204.
Nikolaeva, VM. 1985. Trematodes-Didymozoidae
fauna, distribution and biology. In: Hargis,
Jr., WJ. (ed.). Parasitology and pathology of
marine organisms of the world Ocean. Received February 25, 2019.
Accepted April 27, 2019.
Román-Reyes et al.
Neotropical Helminthology, 2019, 13(1), ene-jun