RESEARCH NOTE/ NOTA CIENTÍFICA
NEW RECORDS OF PARASITIC COPEPODS (COPEPODA: PANDARIDAE,
EUDACTYLINIDAE, CALIGIDAE) ON FIVE SHARK SPECIES (PISCES:
ELASMOBRANCHIA) IN THE GULF OF MEXICO
NUEVOS REGISTROS DE COPÉPODOS PARÁSITOS (COPEPODA: PANDARIDAE,
EUDACTYLINIDAE, CALIGIDAE) EN CINCO ESPECIES DE TIBURONES (PISCES:
ELASMOBRANCHIA) EN EL GOLFO DE MÉXICO
1 2 3,4
M. Amparo Rodríguez-Santiago , Samuel Gómez & Mayra I. Grano-Maldonado
1Catedras 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, C.P. 24155
Ciudad del Carmen, Campeche, México. Tel. 938 11018 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
3Departamento 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: 177-182.
177
ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ABSTRACT
Keywords: Atlantic Ocean - Elasmobranchs - fish parasites - Mexico - Parasitic copepods - sharks - Siphonostomatoida.
The present study is part of an ongoing survey of the parasitic copepods on fishes from coastal
waters in Campeche State (Southern Gulf of Mexico). The aim of this work is to describe the
parasitic copepod species found on five shark species: Carcharhinus leucas (Müller & Henle,
1839), Carcharhinus limbatus (Müller & Henle, 1839), Carcharhinus plumbeus (Nardo, 1827),
Rhizoprionodon terraenovae (Richardson, 1836), and Sphyrna tiburo (Linnaeus, 1758). Except
for R. terraenovae, all shark species were at least infected with one copepod species. A total of
eight copepod species were found: Nesippus orientalis Heller, 1865, Nemesis sp. and Paralebion
elongatus Wilson C.B., 1911 on C. leucas (n = 6); Tuxophorus caligodes Wilson C.B., 1908,
Lepeophtheirus longispinosus Wilson C.B., 1908 and Pandarus sinuatus Say, 1818 on C.
limbatus (n = 9); Pandarus sp. on C. plumbeus (n = 4); and Eudactylina longispina Bere, 1936 on
S. tiburo (n = 24). The occurrence of these copepod species on these sharks from the Gulf of
Mexico constitutes new host records and extends their known geographical distribution, and
contributes to the knowledge of the biodiversity of parasitic copepods in Mexico.
INTRODUCTION
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Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Rodríguez-Santiago et al.
Elasmobranchs have a widespread distribution
in all tropical and subtropical seas. They can be
found in coastal areas, estuaries, shallow
freshwater creeks and coastal lagoon systems,
usually near the bottom (Compagno, 1984).
Since sharks are located on the top of the food
chain (Randhawa & Poulin, 2010), they
provide and exceptional habitat for a variety of
parasitic fauna (Caria, 1990; Caira & Healy,
2004; Caira et al., 2005; Randhawa & Poulin,
2010; Palm, 2011), and have been used as
biological indicators (Vankara et al., 2007;
Haseli et al., 2010; Palm, 2011). In Mexico,
consumption of shark meat is widespread and
has traditionally been used as food particularly
appreciated because of its quality. There are at
least 34 species of sharks in the Gulf of
Mexico. These species belong to the genera
Carcharhinus de Blainville, 1816 and Sphyrna
Rafinesque, 1810 (Bonfil, 1997). Species like
the bullshark Carcharhinus leucas (Müller and
Henle, 1839), the blacktip shark C. limbatus
(Müller and Henle, 1839), the sandbar shark C.
plumbeus (Nardo, 1827), the atlantic
sharpnose shark Rhizoprionodon terraenovae
(Richardson, 1836), and the bonnethead
Sphyrna tiburo (Linnaeus, 1758) are also some
of the most economically important species
(Bonfil, 1997). Small shark species are usually
sold fresh and whole are generally sold in local
markets as dried and salted fillets (Bonfil,
1997). The general pattern these parasitic
copepods exhibit with regard to their host
includes the following aspects according with
(Alvarez & Winfield, 2001): the site of
attachment is variable among hosts, the usual
sites are the gills, nasal cavity, mouth, tail, fin
and body surface in general; and most species
of sharks appear to have from one to a few
species of copepods, and to harbour from one
to several hundred individuals of each those
species. The life cycle of these small aquatic
crustacean parasites is described in De Mees et
al. (1990). 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 develop and give birth to free
swimming larvae. Most parasitic copepods
RESUMEN
Palabras clave: copépodos - Elasmobranquios - parásitos - Siphonostomatoida - Mexico - Océano Atlántico - tiburones.
El presente estudio es parte de una investigación en curso de los copépodos parásitos de peces de
las aguas costeras en el Estado de Campeche (sur del Golfo de México). El objetivo de este
trabajo fue describir las especies de copépodos parásitos que se encontraron en cinco especies de
tiburones: Carcharhinus leucas (Müller & Henle, 1839), Carcharhinus limbatus (Müller &
Henle, 1839), Carcharhinus plumbeus (Nardo, 1827), Rhizoprionodon terraenovae
(Richardson, 1836), y Sphyrna tiburo (Linnaeus, 1758). A excepción de R. terraenovae, todas las
especies de tiburones estuvieron infectados al menos con una especie de copépodo. Un total de
ocho especies de copépodos fueron encontrados: Nesippus orientalis Heller, 1865, Nemesis sp. y
Paralebion elongatus Wilson C.B., 1911 en C. leucas (n = 6); Tuxophorus caligodes Wilson C.B.,
1908, Lepeophtheirus longispinosus Wilson C.B., 1908 y Pandarus sinuatus Say, 1818 en C.
limbatus (n = 9); Pandarus sp. en C. plumbeus (n = 4); y Eudactylina longispina Bere, 1936 en S.
tiburo (n = 24). La ocurrencia de estas especies de copépodos en estos tiburones del Golfo de
México constituye nuevos registros de hospedero y extienden su distribución geográfica
conocida, y contribuye al conocimiento de la biodiversidad de los copépodos parásitos en
México.
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Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015
Parasitic copepods (Pandaridae, Eudactylinidae, Caligidae) on sharks
parasitize more than one host (Alvarez &
Winfield, 2001), showing in general very little
specificity. Regarding their distribution, it
seems to be world-wide as they, like their
hosts, occur in all warm and temperate seas.
However, knowledge of parasitic copepods on
elasmobranches in the Gulf of Mexico is
limited. Therefore, the aim of this study was to
describe and report the parasitic copepod fauna
that infect five shark species in the southern
Gulf of Mexico, these records represent the
first from Campeche State. This study
contributes to the knowledge of ectoparasites
of sharks in this region, where there is a clear
need for studies to provide information
concerning both, parasitic copepods and their
hosts.
During year 2013, samples of five different
species of shark C. leucas (n = 6 specimens), C.
limbatus (n = 9), C. plumbeus (n = 4), R.
terraenovae (n = 2) and S. tiburo (n = 24) were
obtained from commercial catches of the local
fisherman in three regions in Campeche State;
San Pedro (18°.64'09?N, 92°46'88?S),
Champotón (19°21'N 90°43'W) and Ciudad
del Carmen (18° 39' 38? N, 91° 48' 51? W)
southeast Gulf of Mexico. Fish specimens
were sacrificed by decapitation to ensure a fast
dead, which is according to Mexican laws
(NOM-033-ZOO-1995) and were transported
in individual plastic bags in a cool box to the
Institute of Marine Sciences and Limnology,
National Autonomous University of Mexico El
Carmen Research Unit (ICMYL-UNAM). All
fishes 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 was performed under
good illumination, and 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. Copepods
identification was performed following
Cressey & Boyle (1980, 1985), Kabata (1979,
1988, 1992a, 1992b), Boxshall (2004) and
Hayes et al. (2012).
Except for R. terraenovae, all shark species
were at least infected with one copepod
species. A total of eight copepod species were
identified on the skin: Nesippus orientalis
Heller, 1865 (Siphonostomatoida:
Pandaridae), Nemesis sp. (Siphonostomatoida:
Eudactylinidae) and Paralebion elongatus
Wilson C.B., 1911 (Siphonostomatoida:
Caligidae) were identified from C. leucas
(prevalence = 100% in the three copepod
species). Tuxophorus caligodes Wilson C. B.,
1908 (Siphonostomatoida: Caligidae),
Lepeophtheirus longispinosus Wilson C.B.,
1908 (Siphonostomatoida: Caligidae) and
P a n d a r u s s i n u a t u s S a y, 1 8 1 8
(Siphonostomatoida: Pandaridae) on C.
limbatus (prevalence = 22.2%, 44.4% and
77.7%, respectively). Pandarus sp.
(Siphonostomatoida: Pandaridae) on C.
plumbeus (prevalence = 50%) and Eudactylina
l o n g i sp i n a ( S ip h o n o s to m a to i d a :
Eudactylinidae) on S. tiburo (prevalence =
29.1%).
Worldwide, there are several reports from
copepods parasites in sharks; Carcharodon
carcharias (Linnaeus, 1758) collected in
Canada and California (Hogans & Dadswell,
1985; Benz et al., 2003); in the tiger shark
Galeocerdo cuvier (Perón & Lesueur, 1822)
from off the northwestern coast of Australia
(Tang & Newbound, 2007). Despite the
economic importance sharks in the coasts of
MATERIAL AND METHODS
RESULTS
DISCUSION
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Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Rodríguez-Santiago et al.
Gulf of Mexico (Bonfil, 1994) little is known
about the ecology of its parasitic fauna,
particularly of the parasitic copepods found in
this study. Except for R. terraenovae, all shark
species were infected by at least one copepod
species. 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 from five species of sharks
from the Gulf of Mexico, 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) where the
presence of the following species were
reported: Kroyeria sphyrnae Rangnekar, 1957
in Sphyrna lewini (Griffith & Smith, 1834) and
Sphyrna zygaena (Linnaeus, 1758) (Deets,
1994); Kroyerina benzorum Deets, 1987 in
Alopias vulpinus (Bonnaterre, 1788) and
Isurus oxyrinchus Rafinesque, 1810 (Deets,
1987); Kroyerina cortezensis Deets, 1987 in
Carcharhinus falciformis (Müller and Henle,
1839) (Deets, 1987), Kroyerina elongata
Wilson C. B., 1932 in Prionace glauca
(Linnaeus, 1758) (Deets, 1987); Kroyerina
mobulae Deets, 1987 in Mobula japonica
(Müller & Henle, 1841) and Mobula thurstoni
(Lloyd, 1908) (Deets, 1987), and Kroyerina
scottorum Cressey, 1972 in Sphyrna zygaena
(Deets, 1987). In the Neotropical zone, the
importance of copepods, according to Luque &
Poulin (2007), is that these organisms
constitute the second and third largest parasitic
group on marine and freshwater fishes,
respectively. In this study, the five shark
species 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. For this reason, parasitic copepods
are without a doubt an important component of
global biodiversity and may reflect the
ecological status of fish species locally and in
the Gulf of Mexico. There is no doubt that
further surveys in the region will increase the
number of records of species of this group of
parasites providing ecological information.
Alvarez, F & Winfield, I. 2001.
Benz, G, Mollet, H, Ebert, D & Davis. C. 2003.
Bonfil, R. 1997.
Boxshall, G. 2004.
Caira, JN. 1990.
Caira, JN, Mega, J & Ruhnke. TR. 2005.
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.
Five species of parasitic copepods
(Siphonostomatoida: Pandaridae) from
the body surface of a white shark
captured in Morro Bay, California.
Pacific Science, vol.57, pp. 39-43.
Status of shark resources in
the southern Gulf of México and
Car i b bean: imp l ication s for
management. Fisheries Research, vol.
29, pp. 101–117.
An introduction to copepod
diversity. The Ray Society, London.
Metazoan parasites as
indicators of elasmobranch biology.
NOAA Tech Rep, National Marine
Fisheries Service, vol. 90, pp. 71–96. An
unusual blood sequestering tapeworm
(Sanguilevator yearsleyi n. gen., n. sp.)
from Borneo with description of
Cathetocephalus resendezi n. sp. from
Mexico and molecular support for the
r e c o g n i t i o n o f t h e o r d e r
Cathetocephalidea (Platyhelminthes:
Eucestoda). International Journal for
Parasitology, vol. 35, pp. 1135–1152.
Caira, JN & Healy, CJ. 2004. Elasmobranchs
as hosts of metazoan parasites. pp.
BIBLIOGRAPHIC REFERENCES
181
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015
Parasitic copepods (Pandaridae, Eudactylinidae, Caligidae) on sharks
523–551. In. The biology of sharks and
their relatives. Carrier, J, Musack, J &
Heithaus, E. (eds). CRC Press. Boca
Raton. An overview of
chondrichtyan systematic and
biodiversity in southern Africa.
Transactions of the royal society South
Africa, vol. 54, pp. 75-120.
Compagno, LJV. 1999.
Cressey R & Boyle, H. 1980.
C re s s e y, R & B o y l e . H . 1 9 85 .
De Mees, T, Renaud, F & Gabrion. C. 1990.
Haseli, M, Malek, M & Palm. HW. 2010.
Hayes, P, Justine JL & Boxshall. GA. 2012.
Hogans, WE & Dadswell. MJ. 1985.
Kabata, Z. 1979.
Kabata, Z. 1988.
Parasitic
copepods of Mackerel and tuna-like
fishes (Scombridae) of the world.
Smithsonian Contributions to Zoology,
vol. 311, pp. 54-61.
Hol obom o loch u s ( Cope p oda:
Bomolochidae) redefined, with
descriptions of three new species from
the eastern pacific. Journal of
Crustacean Biology, vol. 5, pp. 717–727.
A
model for studying isolation
mechanisms in parasitepopulations: the
genus Lepeophtheirus (Copepoda,
Caligidae). Journal of Experimental
Zoology, vol. 254, pp. 207–214.
Trypanorhynch cestodes from the
Persian Gulf. Zootaxa, vol. 2492, pp.
28–48.
The genus Caligus Müller, 1785
(Copepoda: Siphonostomatoida): two
new species from reef associated fishes
in New Caledonia, and some
nomenclatural problems resolved.
Zootaxa, vol. 3534, pp. 21–39. Parasitic
copepods of the white shark
(Carcharodon carcharius L.) from the
Bay of Fundy. Canadian Journal of
Zoology, vol. 63, pp. 740–741.
Parasitic copepoda of British
Fishes. The Ray Society, The British
Museum, London, vol. 152 (1-12): pp.
1–4. Some evolutionary trends in
caligid copepods. Hidrobiologia, vol.
167/168, pp. 617–622.
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. Metazoan
parasite species richness in Neotropical
fishes: hotspots and the geography of
biodiversity. Parasitology, vol. 134, pp.
865–878.
Parasitic copepods
reported from Mexico. Zootaxa, vol.
3234, pp. 43–68.
Fish parasites as biological
indicators in a changing world: Can we
monitor environmental impact and
climate change? pp. 223 –250. In:
Mehlhorn, H. (Eds.), Progress in
Parasitology, Research Monographs 2,
Springer-Verlag Berlin Heidelberg. DOI
10.1007/978-3-642-21396-0_12
Determinants of tapeworm species
richness in elasmobranch fishes:
untangling and phylogenetic influences.
Ecography, vol. 33, pp. 866–877.A new
species of copepod (Siphonostomatoida:
Caligidae) parasitic on the tiger shark
Galeocerdo cuvier (Péron and Lesueur)
from Western Australian waters.
Systematic Parasitology, vol. 58, pp.
69–80.
On a new
species, Cathetocephalus leucas
(Tetraphyllidea: Cathetocephalidae)
from the bull shark, Carcharhinus leucas
Kabata, Z. 1992 a.
Kabata, Z. 1992b.
Luque, JL & Poulin. R. 2007.
Morales-Serna, FN, Gómez, S & Pérez-Ponce
de León. G. 2012.
Palm, H.W. 2011.
Randhawa, HS & Poulin, R. 2010.
Tang, D. & Newbound, DR. 2004.
Vankara, AP, Vijayalkshmi, C &
Gangadharam. T. 2007.
182
Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Rodríguez-Santiago et al.
(Valenciennes, 1839) from Bay of
Bengal, Visakhaptnam coast, Pradesh,
India. Journal of Parasitic Diseases, vol.
31, pp. 114-119.
Received November 4, 2014.
Accepted February 2, 2015.
