Ciencia Pesquera (2016) número especial 24: 15-21
New records of parasitic copepods (Copepoda:
Pandaridae, Eudactylinidae, Caligidae) on
elasmobranchs (Chondrichthyes) in the Gulf of Mexico
María Amparo Rodríguez-Santiago, Francisco Neptalí Morales-Serna,
Samuel Gómez y Mayra I. Grano-Maldonado
The aim of this study was to identify the parasitic copepod species in some elasmobranchs (two rays and four
shark species) that are commercially important in the Southern Gulf of Mexico (Mexico). In the spotted
eagle ray, Aetobatus narinari six species of parasitic copepods (Alebion sp., Caligus dasyaticus, C. haemulonis,
Euryphorus suarezi, Lepeophtheirus acutus and L. marginatus) were found and in the Southern stingray
Hypanusamericanus two species (C. dasyaticus and Euryphorus sp.). The four shark species (Carcharhinus
leucas, C. limbatus, C. plumbeus and Sphyrna tiburo) that were examined had at least one copepod species.
The copepod species found on C. leucas were: Nesippus orientalis, Nemesis sp. and Paralebion elongatus; in C.
limbatus: Tuxophorus caligodes, L. longispinosus and Pandarus sinuatus; in C. plumbeus: Pandarus sp. and in S.
tiburo: Eudactylina longispina. The copepod species recorded in this study belong to families Caligidae, Pandaridae and Eudactylinidae, which had not been documented in the Mexican coast off the Gulf of Mexico,
contributes to the knowledge of the biodiversity of parasitic copepods in Mexico.
Key words: Copepods, crustaceans, ectoparasites, elasmobranchs, fish parasites, Gulf of Mexico.
Nuevos registros de copépodos parásitos
(Copepoda: Pandaridae, Eudactylinidae, Caligidae) en elasmobranquios
(Chondrichthyes) en el Golfo de México
El objetivo de este estudio fue identificar las especies de copépodos parásitos en algunos elasmobranquios
(rayas y tiburones) de importancia comercial en el sudeste del Golfo de México (México). En la raya pinta,
Aetobatus narinari se encontraron seis especies de copépodos parásitos (Alebion sp., Caligus dasyaticus,
C. haemulonis, Euryphorus suarezi, Lepeophtheirus acutus y L. marginatus) y en la raya látigo americana
Hypanus americanus, dos especies (C. dasyaticus y Euryphorus sp.). Las cuatro especies de tiburones examinadas (Carcharhinus leucas, C. limbatus, C. plumbeus y Sphyrna tiburo) tuvieron al menos una especie
de copépodo. Las especies de copépodos encontradas en C. leucas fueron: Nesippus orientalis, Nemesis sp.
y Paralebion elongatus; en C. limbatus: Tuxophorus caligodes, L. longispinosus y Pandarus sinuatus; en C.
plumbeus: Pandarus sp. y en S. tiburo: Eudactylina longispina. Las especies de copépodos registradas en
el presente estudio pertenecen a las familias Caligidae, Pandaridae y Eudactylinidae, que no habían sido
documentadas para las costas mexicanas del Golfo de México, con lo cual se contribuye al conocimiento
de la biodiversidad de los copépodos parásitos en México.
Palabras clave: Copépodos, crustáceos, ectoparásitos, elasmobranquios, parásitos de peces, Golfo de México.
*
**
***
****
conacyt, Universidad Autónoma del Carmen (unacar).
Facultad de Ciencias Naturales, Centro de Investigación de
Ciencias Ambientales (cica). Av. Laguna de Términos s/n
Col. Renovación 2da Sección, cp 24155 Ciudad del Carmen,
Campeche, México. *autor de correspondencia: marodriguezsa@conacyt.mx, amparoshalom@hotmail.com
conacyt, Centro de Investigación en Alimentación y
Desarrollo, ac, Unidad Mazatlán en Acuicultura y Manejo
Ambiental. Av. Sábalo Cerritos s/n, 82100 Mazatlán, Sinaloa,
México. francisco.morales@ciad.mx
Instituto de Ciencias del Mar y Limnología, Unidad
Académica Mazatlán. Universidad Nacional Autónoma
de México. Joel Montes Camarena s/n, Mazatlán, 82040,
Sinaloa, México. samuelgomez@ola.icmyl.unam.mx
Facultad de Ciencias Marinas, Universidad Autónoma de
Sinaloa. Paseo Claussen s/n. ap 610. Mazatlán, Sinaloa,
México. grano_mayra@hotmail.com
Introduction
Elasmobranchs share part of their geographical distribution in all tropical and subtropical
oceans. Both rays and sharks species are located on the top of the food chain and also show
a broad food pattern that includes both planktonic and benthic organisms from coastal areas,
estuaries, shallow freshwater creeks and coastal
lagoon systems (Compagno 1999, Randhawa &
Poulin 2010). These food habits provide and exceptional habitat for a variety of parasitic fauna
Ciencia Pesquera
15
M.A. Rodríguez-Santiago, F.N. Morales-Serna, S. Gómez y M.I. Grano-Maldonado
(Caira 1990, Caira et al. 2005, Randhawa and
Poulin 2010, Palm 2011) and give them a great
potential as definitive hosts in the parasitic system based on trophic transmission and biological
indicators (Vankara et al. 2007, Haseli et al. 2010,
Palm 2011).
The spotted eagle ray Aetobatus narinari
(Euphrasen 1790), for example, is currently
considered as a threatened species by the Red
List of the International Union for Conservation of Nature red list (iucn), because of their
low reproductive potential and intense and unregulated fishing, which probably have caused
the decline of their populations (Compagno
1999, Kyne & White 2006). Particularly, in the
Southern Gulf of Mexico, the spotted eagle ray
remains as a target species for fisheries. In fact,
it is the second most captured batoid in the region (about 40 tons/year) (conapesca 20131). A
similar situation occurs with small shark species
in this region, which are usually sold fresh and
whole, and in local markets can be also found as
dried and salted fillets (Bonfil 1997).
However, despite the economic and ecologic
importance of these organisms, parasitological
studies on elasmobranchs are in general scarce
for this region, particularly those related with parasitic copepods that may affect them. The impact of “sea lice” a common name used for ectoparasitic copepods is well known to cause serious
cutaneous lesions and mortality in farmed teleosts (Costello 2009), as they graze the epidermis,
often inducing secondary infections (Benz 1981),
and causing destruction of gill tissue, emaciation
and sometimes death (Dezfuli et al. 2011).
The life cycle of these small aquatic crustacean parasites is described in De Meeûs et al.
(1990). Generally, they have a direct cycle with
a fairly long free-swimming phase (at least three
days). Once attached to the host, the parasite becomes mucophagous. Mating occurs on the body
surface of the host and, once fertilized, females
colonise the gill cavity where they lay eggs that
1.
16
conapesca 2013. Base de datos de producción. Anuario
2013. Secretaría de Agricultura, Ganadería, Desarrollo Rural,
Pesca y Alimentación [in Spanish]. http://www.conapesca.gob.
mx/work/sites/cona/dgppe/anuarios/BASE_DE_DATOS_
DE_PRODUCCION_ANUARIO_2013.zip
Ciencia Pesquera
develop and give birth to free swimming larvae.
Most parasitic copepods parasitize more than
one host (Álvarez & Winfield 2001), showing
in general very little specificity. Regarding their
distribution, it seems to be worldwide as they,
like their hosts, occur in all warm and temperate
seas.
The aim of the present study was to identify
the parasitic copepods in six elasmobranch species (two ray species and four sharks) of commercial importance in the coastal zone of Tabasco and Campeche, Mexico. The present study
contributes to the knowledge of biodiversity of
parasitic copepods from marine fish in Mexico.
Materials and methods
During the years 2013-2014, two species of rays
Hypanus americanus (Hildebrand & Schroeder 1928), n = 27, and A. narinari, n = 5, and
four of sharks C. leucas (Valenciennes 1839),
n = 6; C. limbatus (Valenciennes 1839), n = 9;
C. plumbeus (Nardo 1827), n = 4, and S. tiburo
(Linnaeus 1758), n = 24, were measured (total
length and width in rays and length in sharks)
and inspected for parasitic copepods. These
elasmobranch species were obtained from commercial catches in four localities from Tabasco
and Campeche (Mexico): San Pedro (18°64’09”
n, 92°46’88” w), Champoton (19°21’ n, 90°43’
w), Ciudad del Carmen (18°39’38” n, 91°48’51”
w), and Seybaplaya (17°51’ n, 89°06’ w) (Fig. 1).
All elasmobranchs were washed with freshwater
and visually examined for the presence of parasitic copepods on skin, fins and gills. The washing
material and gills were transported in individual
plastic bags in a cool box to the Parasitology Laboratory at the Universidad Autónoma del Carmen (unacar) for parasitological examination.
The examination of copepods on the body surface of the hosts was performed under good illumination, and gill arches were removed from each
fish and carefully inspected in a Petri dish using a
leica mz 9.5 stereomicroscope. The plastic bag
contents were also examined for the presence
of detached copepods. Parasites found on each
fish were preserved in labeled vials with 70%
ethanol. The identification of the parasitic copepodswas performed following Yamaguti (1963),
24: 15-21, núm. especial, diciembre de 2016
Parasitic copepods of elasmobranchs in Mexico
Kabata (1979, 1988, 1992a, b), Cressey & Cressey (1980, 1985), Boxshall & Halsey (2004) and
Hayes et al. (2012). Prevalence (percent of infected hosts among all hosts examined) was determined according to Margolis et al. (1982).
Results
Seventy percent of the examined elasmobranch
specimens harbored at least one parasitic copepod species. A total of six caligid species (family
Caligidae) were found on the skin of five specimens of A. narinari: Alebion sp. Krøyer 1863,
Caligus dasyaticus Rangnekar 1957, Caligus
haemulonis Krøyer 1863, Euryphorus suarezi
Morales-Serna, Rodríguez-Santiago & Gómez
2016, Lepeophtheirus acutus Heegaard 1943
and Lepeophtheirus marginatus Bere 1936 (Fig.
2). The most abundant copepod species were
Alebion sp. (up to 79 individuals per host) and E.
suarezi (37 individuals per host). In the Southern
stingray H. americanus two species were found
C. dasyaticus and Euryphorus sp. The prevalence
of the seven-copepod species was 100%, as they
were present in all the examined hosts.
In the case of sharks, eight copepod species
were found on its skin. Nessipus orientalis Heller
1865 (Pandaridae), Nemesis sp. (Eudactylinidae)
and Paralebion elongatus Wilson 1911 (Caligidae)
were found on C. leucas (prevalence = 100% for
the three copepod species). Tuxophorus caligodes
Wilson 1908 (Caligidae), Lepeophtheirus
longispinosus Wilson 1908 (Caligidae) and
Pandarus sinuatus Say 1818 (Pandaridae) were
found on C. limbatus (prevalence = 22.2%,
44.4% and 77.7%, respectively). Pandarus sp.
(Pandaridae) was found on C. plumbeus (prevalence = 50%), and Eudactylina longispina (Eudactylinidae) on S. tiburo (prevalence = 29.1%).
Discussion
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
Fig. 1. Location of the study area where specimens of rays and sharks were obtained
(Tabasco and Campeche, Mexico).
24: 15-21, núm. especial, diciembre de 2016
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17
M.A. Rodríguez-Santiago, F.N. Morales-Serna, S. Gómez y M.I. Grano-Maldonado
Fig. 2. Images of some of the parasitic copepod species reported in this study. a) Paralebion elongatus b) Pandarus
sp. c) Caligus bifurcatus d) Side view of Nemesis sp. e) Nessipus orientalis, f) Alebion sp., g) Caligus dasyaticus,
h) Caligus haemulonis, i) Lepeophtheirus acutus, and j) Lepeophtheirus marginatus.
copepods infecting teleost fish and elasmobranchs are mainly members of the order Siphonostomatoida, which consist of 39 families. In fact,
it has been suggested that about 210 chondrichthyan species may be infected by this order of
copepods (Compagno 1999). In this study, the 15
parasitic copepod species found on the six elasmobranch species are also of the order Siphonostomatoida (67% belonging to family Caligidae,
20% to Pandaridae and 13% to Eudactylinidae).
This overall species diversity of parasitic copepods was within the range of that reported in
elasmobranchs from other regions worldwide.
For example, Luque & Tavares (2007) documented 14 parasitic copepod species on 10 species
of chondrichthians collected from Brazilian waters. Their study is the highest number of parasitic copepods recorded in the Neotropics for the
elasmobranch group of the family Carcharhinidae. Among the copepod species that they mentioned, P. sinuatus was present on C. limbatus,
18
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which coincided with our findings for this same
shark species.
Other studies that have also recorded a great
diversity of parasitic copepod species in elasmobranchs are that conducted by Henderson et al.
(2013) and Rokicki & Bychawska (1991) in the
northern Indian Ocean and the central Atlantic Ocean, respectively. In the first, the authors
reported 12 parasitic copepod species (families
Pandaridae and Caligidae) on 13 elasmobranch
host species (Henderson et al. 2013). Meanwhile
in the second, 14 copepod species were reported
on seven elasmobranch species from the families Carcharhinidae and Sphyrnidae (Rokicki &
Bychawska 1991).
Among the copepod species that were found
parasitizing the elasmobranchs in this study,
some have also been reported for other elasmobranch species in other regions of the world. Such
is the case of C. dasyaticus, a common parasite
species, that has been reported on stingrays of
24: 15-21, núm. especial, diciembre de 2016
Parasitic copepods of elasmobranchs in Mexico
India (Pillai 1968), Japan (Tang et al. 2013) and
Taiwan (Ho et al. 2007), and C. bifurcatus. Also,
L. acutus has been reported on elasmobranchs
in Germany, Japan and the Netherlands, on the
tiger shark Galeocerdo cuvier (Péron & Lesueur
1822), zebra shark, Stegostoma fasciatum (Hermann 1873), the Alfred manta Mobula alfredi
(Krefft 1868), and the whale shark Rhincodon
typus Smith 1828, held in sea pens off Okinawajima Island, Japan (Kik et al. 2011, Tang et al.
2013). In eastern India (Benz et al. 2007) and
South Africa (Lebepe & Dippenaar 2013), L.
acutus has even been considered a dangerous
pathogen of captive elasmobranchs. This species
has a broad adaptive spectrum (Kik et al. 2011)
as they can be found in a wide regime of salinity
and temperature, as well as in a vertical range
from highland lakes to the ocean trenches (Huys
& Boxshall 1991). In addition, it can be found
in both, the water column (planktonic) and the
sediment (benthic) in association with other organisms (symbionts). In this sense, Álvarez &
Winfield (2001) observed that the site of attachment is variable among hosts, being the most
usual sites the gills, nasal cavity, mouth, tail, fin
and body surface in general. These authors also
documented that most species of sharks appear
to have one to a few species of copepods, and
harbor one to several hundred individuals of
each of those species.
Moreover, the only published reports of parasitic copepods on fish species (including both,
teleosts and elasmobranchs) in the Mexican
coasts of the Gulf of Mexico are those of Causey (1960), who reported 25 genera and 46 species of parasitic copepods. Álvarez & Winfield
(2001) reported Dinemoura latifolia (Steenstrup
& Lütken 1861) and Pandarus smithii Rathbun
1886 from sharks in Veracruz State. In our research group, Morales-Serna et al. (2016) described for the first time to Euryphorus suarezi on the
spotted eagle ray A. narinari from Tabasco and
Campeche. In fact, in the recent review by Morales-Serna et al. (2012) there had been only five
species of parasitic copepods recorded in elasmobranchs for the Mexican coasts, all of them
from sharks and rays collected from the northwestern coasts of Mexico. However, of these
species of copepods that they found in elasmo-
branches none coincides with those reported in
our study. The bull shark (C. leucas) is the only
shark species in which parasitic copepods have
been reported in both coasts of Mexico: Pacific
(Cressey 1972) and Gulf of Mexico (this study).
In the Mexican Pacific, only one species of parasitic copepod was reported in this shark, while
in the Gulf of Mexico this study reports three.
Another interesting finding was that both ray
species shared two species of parasitic copepods despite having different habits (one benthonic and the other pelagic). Although the exact
geographic coordinates and depths of catch locations were not available, it is known that these
two ray species share its distribution range in the
Gulf of Mexico, so it is possible that this kind of
ectoparasites are acquired in places where they
coexist.
In summary, this study provides a baseline
of new information on the distribution of species of parasitic copepods from six commercially
important elasmobranch species in the Southern
Gulf of Mexico. A total of 15 parasitic copepod
species were reported here, which are representatives of three families (Caligidae, Pandaridae
and Eudactylinidae) that had not been documented for elasmobranchs in Mexican coasts
of the Gulf of Mexico. Moreover, despite these
species of rays and sharks are common target for
local commercial fisheries, the limitation of the
study is that these fish are not so abundant in the
region. Consequently, their capture to perform
parasitological studies is limited. The present
study is part of an ongoing survey of the parasitic copepods on fishes from coastal waters in the
Southern Gulf of Mexico.
Acknowledgements
mars thanks the support of the program Cátedras conacyt. The authors also thank to the two
anonymous reviewers for their valuable comments on a previous version of the manuscript.
To Juan Carlos Pérez Jiménez (ecosur-Campeche) for his help during field samplings and for
his assistance with the identification of elasmobranchs.
24: 15-21, núm. especial, diciembre de 2016
Ciencia Pesquera
19
M.A. Rodríguez-Santiago, F.N. Morales-Serna, S. Gómez y M.I. Grano-Maldonado
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Recibido:13 de junio de 2016.
Aceptado: 15 de octubre de 2016.
24: 15-21, núm. especial, diciembre de 2016
Ciencia Pesquera
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