RESEARCH NOTE/ NOTA CIENTÍFICA
NEW RECORDS OF PARASITIC COPEPODS (CALIGIDAE: SIPHONOSTOMATOIDA)
ON SPOTTED EAGLE RAY, AETOBATUS NARINARI (ELASMOBRANCHII:
MYLIOBATIDAE) FROM THE GULF OF MEXICO
NUEVOS REGISTROS DE COPÉPODOS PARÁSITOS (CALIGIDAE:
SIPHONOSTOMATOIDA) EN LA RAYA MANCHADA, AETOBATUS NARINARI
(ELASMOBRANCHII: MYLIOBATIDAE) DEL GOLFO DE MEXICO
1 2 3,4
M. Amparo Rodríguez-Santiago , Samuel Gómez & Mayra I. Grano-Maldonado
1Universidad 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, C.P. 24155 Ciudad del Carmen, Campeche,
México. Tel. 529383811018 EXT. 1806. marodriguezsa@conacyt.mx, amparoshalom@hotmail.com
2Instituto 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
Departamento de Ecofisiología, Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa. Paseo Claussen s / n. A. P.
4
610. Mazatlan, Sinaloa, Mexico Tel/Fax: + 52 669 982 86 56 grano_mayra@hotmail.com; CCMAR-CIMAR L.A., Centro
de Ciencias do Mar, Universidade do Algarve, Faro, Portugal. mgmaldonado@ualg.pt
Neotropical Helminthology, 2015, 9(1), jan-jun: 163-169.
ABSTRACT
Keywords: Caligidae - copepods - crustaceans- Gulf of México- rays - Siphonostomathoida.
The aim of this study was to investigate the occurrence of parasitic copepods (Caligidae:
Siphonostomatoida) in the spotted eagle ray Aetobatus narinari, which is considered a
threatened species worldwide. In southern Mexico, the spotted eagle ray represents a traditional
source of food, reaching the highest economic value with respect to other elasmobranchs. During
a recent survey of fish parasites from three localities of Campeche state (Southern Gulf of
Mexico), eight individuals of A. narinari caught by local fishermen were examined for
ectoparasites and five different species of copepods were recorder on the skin of this fish host:
Alebion sp. Krøyer, 1863; Caligus dasyaticus Rangnekar, 1957; Caligus haemulonis Krøyer,
1863 ; Euryphorus sp., Milne Edwards H., 1840; Lepeophtheirus acutus Heegaard, 1943 and
Lepeophtheirus marginatus Bere, 1936. This is the first document which describes; 1) a parasitic
copepod (sea lice) recorded for the spotted eagle ray A. narinari as commercially important
species, 2) a new host fish for the genus Euryphorus which has not been previously reported for
Mexico, and 3) C. dasyaticus represents a new geographical record in the Southern Gulf of
Mexico. The present study provides a new host and geographical record for six parasitic copepod
species in Campeche State, Mexico and contributes to the knowledge of biodiversity of parasitic
copepods in Mexico. There is no doubt that records of the number of species of this group of
parasites will increase with further surveys.
163
ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
INTRODUCTION
164
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Rodríguez-Santiago et al.
The spotted eagle ray Aetobatus narinari
(Euphrasen, 1790) is currently considered as a
threatened species by the Red List of the
International Union for Conservation of
Nature IUCN red list, because of their low
reproductive potential and intense and
unregulated fishing, which probably have
caused the decline of their populations (Kyne
& White, 2006; Compagno, 1999). In the
Southern Gulf of Mexico, the spotted eagle ray
still remains as a target species for fisheries. In
fact, it is the second most captured batoid in the
region (about 40 tons/year) (Conapesca,
2013). Only after the southern stingray
Dasyatis americana (Hildebrand & Schroeder,
1928). Despite its importance, studies about its
parasitofauna are in general scarce,
particularly those related with parasitic
copepods that may affect them. The impact of
sea lice (a common name used for copepodos
parasites) is well known to cause serious
cutaneous lesions and mortality in farmed
teleosts (Costello, 2009) where they graze the
epidermis, often inducing secondary
infections (Benz, 1981). So far, species of
parasitic copepods found world-wide in
aquatic environments, males are free-living in
the zooplankton and only females are parasitic
and found on fish hosts (Kabata, 1988a,b),
causing destruction of gill tissue, emaciation,
and sometimes death (Dezfuli et al., 2011).
Most species are found on freshwater fishes,
but a few infect marine fishes of coastal waters
(Boxshall & Halsey, 2004a,b). Luque &
Tavares (2007) reported 26 valid species plus
10 unidentified species of copepods, of which
23 are from freshwater hosts and 13 are from
RESUMEN
Palabras claves: Caligidae- copépodos - crustáceos- Golfo de México - rayas - Siphonostomathoida.
El objetivo de este estudio, fue investigar la ocurrencia de copépodos parásitos (Caligidae:
Siphonostomatoida) en la raya pinta Aetobatus narinari considerada una especie amenazada
mundialmente. En el sur de México, la raya manchada representa una fuente tradicional de
alimento, alcanzando el valor económico más alto con respecto a otros elasmobranquios. Durante
un reciente estudio de parásitos de peces de tres localidades del estado de Campeche (sur del
Golfo de México), ocho individuos de A. narinari capturados por pescadores locales fueron
examinados por ectoparásitos y cinco especies diferentes de copépodos fueron registrados en la
piel de este pez: Alebion sp. Krøyer, 1863; Caligus dasyaticus Rangnekar, 1957; Caligus
haemulonis Krøyer, 1863; Euryphorus sp., Milne Edwards H., 1840; Lepeophtheirus acutus
Heegaard, 1943 and Lepeophtheirus marginatus Bere, 1936. Este trabajo es el primero en
documentar; i) un copépodo parásito (piojo de mar) registrado para la raya pinta A. narinari como
especie de importancia comercial, ii) un nuevo hospedero para el género Euryphorus que no
había sido reportado previamente para México y iii) C. dasyaticus representa una nueva registro
geográfico en el Sur del Golfo de México. El presente estudio registra un nuevo hospedero y
registro geográfico para seis especies de copépodos parásitos en el Estado de Campeche, México
y contribuye al conocimiento de la biodiversidad de los copépodos parásitos en México. No hay
duda de que el número de registros de especies de este grupo de parásitos se incrementará con
nuevos estudios.
165
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015
gill arches were removed from each fish and
carefully inspected in a Petri dish using a
stereomicroscope (LEICA MZ9.5). 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 until its taxonomic
identification to the lowest level possible
(Vidal-Martínez et al., 2002). Copepods
identification was performed following
Cressey & Boyle (1980, 1985), Kabata
(1979a,b, 1992a,b), and Boxshall & Halsey
(2004a,b).
Eight individuals of spotted eagle ray were
examined, which measured between 160 cm
length and 190 cm width. A 70% of examined
fish specimens harbored at least one parasite
taxon. A total of six parasitic copepod species
(Caligidae, Siphonostomatoida) were found in
eight specimens of A. narinari: Alebion sp.
Krøyer, 1863 (see Boxshall, 2014); Caligus
dasyaticus Rangnekar, 1957 (see Boxshall,
2013); Caligus haemulonis Krøyer, 1863 (see
Boxhall & Walter, 2014a,b); Euryphorus sp.,
Milne Edwards H., 1840; Lepeophtheirus
acutus Heegaard, 1943 (see Walter &
Boxshall, 2009) and Lepeophtheirus
marginatus Bere, 1936 on the skin of this fish
host. The most abundant copepod parasite was
Euryphrus sp. and the less abundant and was
Alebion sp.
In the Neotropical zone, the importance of
copepods, according to Luque & Poulin
(2008), is that these organisms constitute the
second and third largest parasitic group on
marine and freshwater fishes, respectively. In
this study, the spotted eagle ray A. narinari as
brackish or marine hosts in Brazil. Brooks
(1992) reported helminths from stingrays in
the neotropics and later, Domingues &
Marques (2010) reported copepods of
freshwater stingrays (Potamotrygonidae) in
Brazil. In the case of Lepeophtheirus species
primarily infect teleosts; nevertheless, a few
have been reported from chondrichthyans
infecting skin, gills and nasal cavities
(Yamaguti, 1963; Cressey, 1967; Kabata,
1979a,b). Little is known about the
host–parasite interactions of most copepods
species in rays. Along with these new records
reported in the present study, copepods have
been currently reported on some
elasmobranches mainly sharks from Mexico
(Alvarez & Winfield, 2001). Therefore, the
aim of this study is to identify (by traditional
morphological methods) and quantify the
parasitic copepods of A. narinari, a
commercially important species in the
southern Gulf of Mexico.
Eight spotted eagle ray were obtained from
landings of small fishing boats at three
locations of Campeche, Mexico, at the
southern Gulf of Mexico; San Pedro
(18°.64'09?N, 92°46'88?S), Champotón
(19°21'N 90°43'W) and and Seybaplaya
(17°51'N 89°06'W) in 2013. Fish specimens
were sacrificed by decapitation to ensure a fast
dead, which is according to Mexican laws
(NOM-033-ZOO-1995). Fish samples were
transported in individual plastic bags in a cool
box to Institute of Marine Sciences and
Limnology, National Autonomous University
of Mexico del Carmen Research Unit
(ICMYL-UNAM) for parasitological
examination. The total length (cm) and weight
(g) were measured. All fish were examined for
the presence of parasitic copepods on skin,
fins, gills and gill rakers, the examination of
copepods on the body surface of the hosts and
Parasitic copepods on spotted eagle ray
MATERIAL AND METHODS
RESULTS
DISCUSSION
166
including new host records and new locality
records. The only published reports of parasitic
copepods Dinemoura latifolia (Steenstrup &
Lütken, 1861) and Pandarus smithii Rathbun,
1886 found in sharks in the Gulf of Mexico
were reported from Veracruz State by Alvarez
& Winfield (2001) and secondly, a recent
review by Morales-Serna et al. (2012),
however, this does not show previous records
on rays. Although some work has been
perfomed, still a lack of knowledge which
impede our understanding of the ecological
and biogeographical history of the host-
parasite associations. The ecological studies of
parasitic copepods in commercially important
fish species like sharks and rays which are
important due to a high market value. Also, this
fish species is highly appreciated by its meat,
texture and flavor. The limitation of the study is
that these fish species are not abundant in the
commercial fishing or sport-fishing from this
zone in México, despite being a common target
for local commercial fisheries. Consequently,
their capture just to perform parasitological
studies is limited. This study identified the
copepod parasitic fauna of commercially
important ray species, which has been
highlighted and shed some light on the
knowledge of biodiversity and biology of
parasitic copepods. New geographical host
records are important, for the reason that you
can detect distribution patterns. Studies on
copepod parasitizing other commercial fish
hosts, particularly in Mexico and Gulf of
Mexico, and the completion of their life cycle
warrant further investigation.
In conclusion, this is the first to document
which describes; i) a parasitic copepod (sea
lice) record for the spotted eagle ray A.
narinari as commercially important species in
the Southern Gulf of Mexico, ii) a new host fish
for the genus Euryphorus which has not been
previously reported for Mexico. The present
study provides new host and geographical
record for six parasitic copepod species in
Campeche State, Gulf of Mexico and
commercially important studied are
economically important in the region, and
further work will continue based on parasite
biodiversity in order to understand their
ecological importance, their biogeography and
evolution, and to support and improve
management and conservation strategies.
Most of the copepods infecting fish and also
elasmobranchs are mainly member of the
family Siphonostomatoida, which consist of
39 families (Boxshall, 2013) and around of 210
chondrichthyan species may be infected by
this family (Campagno, 1999). The species C.
dasyaticus are a common parasite on the
stingrays in India (Pillai, 1968); Japan (Tang et
al., 2013) and Taiwan (Ho et al., 2007). Also,
L. acutus has been reported from
elasmobranches in Germany, Japan and the
Netherlands (Tang et al., 2013; Kik et al.,
2011). In eastern India (George et al., 2007)
and South Africa (Lebepe & Dippenaar, 2013),
given its ability to infect a wide variety of
elasmobranchs and promote life-threatening
lesions on some hosts, L. acutus should be
considered a dangerous pathogen of captive
elasmobranchs (Kik et al., 2011), in Thailand
(Purivirojkul et al., 2009). This supports the
hypothesis that intensity of infection is a
species characteristic and that the biological
features of parasitic species can potentially
override local environmental conditions in
driving parasite population dynamics.
According to Poulin (2006), this is possible
because prevalence is determined by
encounter rates between parasites and hosts,
which are influenced by processes external to
the fish (e.g., survival of free-living parasite
stages), probably determined by local factors,
whereas intensity of infection is determined to
a large extent by processes acting within the
fish.
This study increases our knowledge of the
biodiversity of parasitic copepods in Mexico
and provides a baseline of new information on
the distribution of species of parasitic
copepods in rays from the Gulf of Mexico,
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Rodríguez-Santiago et al.
167
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Parasitic copepods on spotted eagle ray
and historical structure of the helminth
fauna inhabiting neotropical freshwater
stingrays (Potamotrygonidae). Journal
of Parasitology, vol.78, pp. 588–595.
An overview of
chondrichtyan systematic and
biodiversity in southern Africa.
Transactions of the royal society South
Africa, vol. 54, pp. 75-120.
Base anuario estadístico de
pesca de la comisión nacional de
acuacultura y pesca. (Eds.) La
Secretaria de agricultura ganadería
desarrollo rural, pesca y alimentación.
The global economic cost
of sea lice to the salmonid farming
industry. Journal of Fish Diseases,
vol.32, pp.115–118.
Revision of the family
Pandaridae (Copepoda: Caligoida).
Proc. U.S. Natural. Museum, vol.121,
pp. 1-33. Parasitic
copepods of Mackerel and tuna-like
fishes (Scombridae) of the world.
Smithsonian Contributions to Zoology,
vol. 311, pp. 54–61.
Holobomolochus (C opepoda:
Bomolochidae) redefined, with
descriptions of three new species from
the eastern pacific. Journal of
Crustacean Biology, vol. 5, pp. 717–727.
Mast cell responses to
Ergasilus (Copepoda), a gill
ectoparasite of Sea Bream. Fish and
Shellfish Immunology, vol.30, pp.1087-
1091.
Ergasilus trygonophilus sp. nov.
(Copepoda: Ergasilidae) a branchial
parasite of freshwater stingrays
(Potamotrygonidae) from state of Pará,
Brazil. Zoologia, vol. 27, pp.829-833.
Janinecaira
Compagno, LJV. 1999.
Conapesca, 2013.
Costello, M.J. 2009.
Cressey, R. 1967.
Cressey R & Boyle, H. 1980.
C r e s s e y, R & B o y l e , H . 1 9 8 5 .
Dezfuli, BS, Giari, L, Lui, A, Lorenzoni, M &
Noga, EJ. 2011.
Domingues, MV & Marques, TM. 2010.
George, W, Benz, B, Smith, E, Bullard SA &
Braswell, J. 2007.
Alvarez, F & Winfield, I. 2001.
Benz, G W. 1981.
Boxshall, GA & Halsey, SA. 2004a.
Boxshall, G & Walter, TC. 2014a.
Boxshall, G & Walter, TC. 2014b.
Brooks, DR. 1992.
New records of
Dinemoura latifolia and Pandarus
smithii (Copepoda, Siphonostomatoida,
Pandaridae) parasitizing the shark
Isurus oxyrinchus in the Gulf of Mexico.
Crustaceana, vol. 74, pp. 501–503.
Observations on the
attachment scheme of the parasitic
copepod Pandarus satyrus (Copepoda:
Pandaridae). Journal of Parasitology,
vol.67, pp. 966-967.
Copepod
Diversity. Volume 166: Copepod
Diversity. (Two volume set). The Ray
Society, The Natural History Museum.
Cromwell Road. London.
Caligus
haemulonis Krøyer, 1863. In: Walter, TC
& Boxshall, G. 2014. World of Copepods
database. Consultado 3 octubre 2014,
<http://www.marinespecies.org/copepo
da/aphia.php?p=taxdetails&id=356756
on 2014-10-03> Euryphorus
Milne Edwards H., 1840. In: Walter, TC
& Boxshall, G. 2014. World of Copepods
database. Consultado 3 octubre 2014,
<http://www.marinespecies.org/copepo
da/aphia.php?p=taxdetails&id=135589
on 2014-10-03>
Origins, diversification,
Boxshall, G. 2013.
Boxshall, G. 2014.
Boxshall, GA & Halsey, SH. 2004b.
Shiponostomatoida. In:
Water, TC, Boxhall, G. World of
Copepods database. Consultado el 4 de
O c t u b r e 2 0 1 4 ,
<http://www.mrinespecies.org/copepod
a/aphia.php?p=taxdetails&id=104>
Alebion Krøyer, 1863. In:
Walter, TC & Boxshall, G. 2014. World
of<http://www.marinespecies.org/cope
poda/aphia.php?p=taxdetails&id=1355
88 on 2014-10-03 >
An
introduction to copepod diversity. The
Ray Society. London, UK.
BIBLIOGRAPHIC REFERENCES
168
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Rodríguez-Santiago et al.
d a r k t h r e a d n . g e n . , n . s p .
(Eudactylinidae, Siphonostomatoida,
Copepoda) infects gills of the ornate
eagle ray Aetomylaeus vespertilio
(Bleeker, 1852) (Myliobatidae,
Myliobatiformes) in the Beagle Gulf
(Timor Sea, eastern Indian Ocean) off
northern Australia. Journal of
Parasitology, vol. 93, pp 32-38.
Four species of Caligus Müller, 1785
(Copepoda, Siphonostomatoida,
Caligidae) parasitic on marine fishes of
Taiwan. Journal of Natural History,
Volume 41, pp. 401-417.
Parasitic copepoda of
British Fishes. The Ray Society, The
British Museum, London, n° 152, I-xII:
1-4.
Copepoda and Brachiura.
Canadian Special Publication in
Fisheries and Aquatic Sciences.
Some evolutionary trends in
caligid copepods. Hidrobiologia, vol.
167/168, pp. 617–622.
The sea
louse Lepeophtheirus acutus (Caligidae,
Siphonostomatoida, Copepoda) as a
p a t h o g e n o f a q u a r i u m - h e l d
elasmobranchs. Journal of Fish
Diseases, vol.34, pp. 793–799. doi:
10.1111/j.1365-2761.2011.01295.x
Ho, JS, Ching-Long, L, & Wen-Been, C. 2007.
Kabata, Z. 1979a.
Kabata, Z. 1988a.
Kabata, Z. 1988b.
Kik, MJ, Janse, M & Benz, GW. 2011.
Kabata, Z. 1979b.
Kabata, Z. 1992 a.
Kabata, Z. 1992b.
Parasitic copepoda of
British Fishes. The Ray Society, The
British Museum, London, vol. 152, pp.
1–4.
Copepods Parasitic on
Fishes: keys and notes for identification
of the species. Synopses of the British
Fauna (New Series) No. 47. Universal
Book Services/W. Backhuys:
Oegstgeest. VII.
Copepoda parasitic on
Australian fishes, XV. Family
Ergasilidae (Poecilostomatoida).
Journal of Natural History, vol. 26, pp.
47–66.
Kyne, PM & White, WT. 2006.
Lebepe, MC & Dippenaar, SM. 2013.
Luque, JL & Tavares, LER. 2007.
Luque, JL. & Poulin, R. 2008.
Pillai, NK. 1968.
Poulin, R. 2006.
Purivirojkul, W, Chaidee, P & Thapanand-
Chaidee, T. 2009.
Tang, D, Venmathi Maran, BA, Matsumoto, Y,
& Nagasawa, K. 2013.
Taeniurops
meyeni. The IUCN Red List of
Threatened Species. Version 2014.2.
Consultado el 2 Noviembre 2014.
<htpp:www.iucnredlist.org>. A report
of symbiotic Siphonostomatoida
(Copepoda) infecting mobulids
(Rajiformes:Mobulidae) off the
KwaZulu-Natal coast, South Africa.
African Zoology, vol.48, pp. 326-332.
Checklist of
Copepoda associated with fishes from
Brazil. Zootaxa, vol. 1579, pp. 1-39.
Linking ecology
with parasite diversity in neotropical
fishes. Journal of Fish Biology, vol. 72,
pp. 189-204.
Additions to the copepod
parasites of South Indian fishes.
Parasitology, vol, 58, pp. 9–36.
Variation in infection
parameters among populations within
parasite species: Intrinsic properties
versus local factors. International
Journal for Parasitology, Vol. 8, pp. 877-
885.
Parasites of Deep-Sea
Sharks from the Andaman Sea with Six
New Records of Parasites in Thailand.
Journal of Natural Sciences, vol. 43, pp.
93-99.
Redescription of
Lepeophtheirus acutus Heegaard, 1943
(Copepoda: Caligidae) parasitic on two
elasmobranch hosts off Okinawa-jima
Island, Japan. Journal of Natural
History, vol. 47, pp 581-596.
Morales-Serna, NF, Gómez, S & Pérez-Ponce
de León, G. 2012.
Vidal-Martínez, V, Aguirre-Macedo, L, Sholz,
T, González-Solis, D & Mendoza-
Parasitic copepods
reported from Mexico. Zootaxa, vol.
3234, pp. 43-68.
169
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Parasitic copepods on spotted eagle ray
Franco, F. 2002. Atlas de los helmintos
parásitos de cíclidos de México.
Instituto Politécnico Nacional. México
D.F.
Walter, TC & Boxshall, G. 2009.
Walter, TC. 2014.
Lepeophtheirus von Nordmann, 1832.
In: World Copepoda Database. (ed. by
T.C. Walter & G. Boxshall), Consultado
3 o c t u b r e 2 0 1 4 , <
http://www.marinespecies.org/copepod
a/aphia.php?=taxdetails&id=135568.>
Caligus dasyaticus
Rangnekar, 1957. In: Walter, T.C. &
Boxshall, G. 2014. World of Copepods
database. Accessed through: Walter, T.C.
& Boxshall, G. (2014). World of
Copepods database Consultado 3
o c t u b r e 2 0 1 4 ,
<http://www.marinespecies.org/copepo
da/aphia.php?p=taxdetails&id=349606
on 2014-10-03>
Parasitic Copepoda and
Branchiura of fishes. Interscience Publs.
New york, London & Sydney. 1-1104.
Yamaguti, S. 1963.
Received January 2, 2015.
Accepted February 4, 2015.
