ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

Neotropical Helminthology, 2018, 12(2), jul-dic:213-222.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

INTESTINAL HELMINTH PARASITES OF BLACKTIP SHARK CARCHARHINUS LIMBATUS

(MÜLLER & HENLE, 1839) (CARCHARHINIFORMES: CARCHARHINIDAE), IN CHACHALACAS

BEACH, VERACRUZ, MÉXICO

HELMINTOS PARÁSITOS INTESTINALES DEL TIBURÓN PUNTAS NEGRAS CARCHARHINUS

LIMBATUS (MÜLLER & HENLE, 1839) (CARCHARHINIFORMES: CARCHARHINIDAE), EN PLAYA

CHACHALACAS, VERACRUZ, MÉXICO

1Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional. Av. IPN S/N Col. Playa Palo de Santa Rita CP

23096, La Paz, Baja California Sur, México

2Laboratorio de Hidrobiología, Facultad de Biología, Campus Xalapa, Universidad Veracruzana. Circuito Gonzalo Aguirre

Beltran S/N Zona Universitaria CP 91090 Xalapa, Veracruz, México

*Corresponding author: spiroxys@hotmail.com

1 2

Miguel Angel Dorantes-González & Oscar Méndez *

ABSTRACT

Keywords: cestodes - Gulf of Mexico - nematodes - parasites – sharks - spiral valves

Thirty-nine spiral valves of blacktip shark Carcharhinus limbatus (Müller & Henle, 1839) caught by

artisanal fisheries in Chachalacas Beach, Veracruz were examined for helminth parasites. A total of 7029

helminth was found, of which 99% were cestodes and 1% was a nematode. We recorded 20 species of

cestodes and one nematode. The cestodes Paraorygmatobothrium cf sinuspersicense (Malek, Caira &

Haseli, 2010) and Nybelinia sp. 1 (Poche, 1926), registered the mayor values of prevalence and mean

intensity of infection. C. limbatus is recorded as new host for P. cf sinuspersicense; Anthobothrium

laciniatum (Linton, 1890); Rhinebothrium sp. (Linton, 1889); Thysanocephalum thysanocephalum

(Linton, 1899); Cathetocephalus thatcheri (Daily & Overstreet, 1973); Oncomegas cf wageneri (Palm,

1995); Disculiceps pileatus (Linton, 1891); Poecilancistrum caryophyllum (Diesing, 1850) and

Hysterotylacium sp. Ward & Magath, 1917. All helminths found in blacktip shark C. limbatus represent

new records for the coastal zone of the state of Veracruz, Mexico.

Neotropical Helminthology

213

Volume12,Number2(jul-dec2018)

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

Lima-Perú

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

The Blacktip shark Carcharhinus limbatus (Müller

& Henle, 1839) is one of the most valuable species

for the artisanal fishery of the Gulf of Mexico

(Tovar-Ávila, 1995; Castillo-Géniz et al., 1998;

Tovar-Ávila et al., 2009). The sharks act as final

host of a wide range of intestinal parasitic

helminths (Vankara et al., 2007; Haseli et al., 2010;

Palm, 2011), mainly cestodes (Caira & Healy,

2004; Vankara et al., 2007; Randhawa & Poulin,

2010; Palm, 2011). Multiple taxonomic studies

about helminths of sharks have been made of all

around the world (Caira et al., 1999) covering large

regions, however, the pattern of distribution of the

parasites may vary within the host with a wide

distribution. Thus, the presence of certain parasites

in cosmopolitan sharks may be common in

multiple areas or be restricted locally. In Mexico,

the knowledge about the helminths infecting this

fishing resource is scarce (Méndez & Galván-

Magaña, 2016; Merlo-Serna & García-Prieto,

2016), therefore, the objective of this research is to

describe the helminth fauna of the spiral valve of

blacktip shark C. limbatus in the locality of

Chachalacas, Veracruz, México, contributing to the

knowledge of the diversity of parasitic helminths

of sharks in our country.

214

Neotropical Helminthology, 2018, 12(2), jul-dic

INTRODUCTION MATERIAL AND METHODS

RESUMEN

Se examinaron 39 válvulas espirales de tiburón puntas negras Carcharhinus limbatus (Müller & Henle,

1839) capturados por la pesca artesanal en la localidad de Playa Chachalacas, Veracruz. Se encontró un

total de 7029 helmintos, de los cuales el 99% pertenecieron a los cestodos y 1% a los nematodos. Cada

helminto colectado fue procesado mediante las técnicas específicas para cada grupo. Registramos 21

especies de helmintos, de las cuales 20 fueron céstodos y una de nemátodo. Los céstodos

Paraorygmatobothrium cf sinuspersicense (Malek, Caira & Haseli, 2010) y Nybelinia sp. 1 (Poche,

1926), presentaron los mayores valores de prevalencia e intensidad promedio de infección. Se registra a C.

limbatus como nuevo hospedero para P. cf sinuspersicense; Anthobothrium laciniatum (Linton, 1890);

Rhinebothrium sp. (Linton, 1889); Thysanocephalum thysanocephalum (Linton, 1899); Cathetocephalus

thatcheri (Daily & Overstreet, 1973); Oncomegas cf wageneri (Palm, 1995); Disculiceps pileatus

(Linton, 1891); Poecilancistrum caryophyllum (Diesing, 1850) y Hysterotylacium sp. Ward & Magath,

1917. Todos los helmintos encontrados en el tiburón puntas negras C. limbatus representan nuevos

registros para la zona costera del estado de Veracruz, México.

Palabras clave: cestodos - Golfo de México - nematodos - parásitos – tiburones - válvulas espirales

Thirty-nine spiral valves of blacktip shark C.

limbatus was collected by the artisanal fisheries in

Chachalacas Beach (19°25'03'' N y 96°19'29''O),

Veracruz, México, at a distance of 20 km from the

coast, between January 2012 and November 2014.

Data of total length, sex, date and place of capture

were taken from each host. The spiral valves were

obtained by the fishermen according to their

routine. Each intestine was sealed with rubber

bands at each end, placed in plastic bags with

formaldehyde 10% and tagged with the data of

each shark (number of host, scientific name, date

and locality). In the laboratory, each spiral valve

was washed with normal water to remove the

excess of formaldehyde. These was cut

longitudinally and extended in a dissection tray.

Spiral valve cuts of approximately 10 cm were

made to facilitate the search for helminths. The

collect of helminths was made under a stereoscopic

microscope. Each helminth was counted and

transferred to vial jar with 70% ethanol. The

nematodes were placed in glycerin vials at

concentrations of 50%, 75% and 100% for their

transparency. For the taxonomic determination, 10

specimens of each species were dehydrated in

ethanol 70%, 96% and 100%, stained with Mayer

carmine, clarified with methyl salicylate and

permanent preparations were made with Canada

Miguel Angel Dorantes-González & Oscar Méndez

215

balsam. The nematodes once cleared and identified

were returned to the vials glycerin vials. The

identification of the helminths was done to the

largest possible taxon using specialized literature

for cestodes (Khalil et al., 1994; Palm, 2004;

Ruhnke et al., 2006; Ruhnke & Caira, 2009) and

nematodes (Anderson, 2000). Some samples were

prepared for examination with scanning electron

microscopy (SEM). For scanning electron

microscopy (SEM) studies, the specimens were

washed for 30 min with sodium cacodylate buffer

0.1 M, and are post - fixed with osmium tetroxide

1% for 30 min; Subsequently the samples were

washed again for 30 min in sodium cacodylate and

then were dehydrated in ethanol gradients from

30% to 100% for 10 min in every step, at the end

were dried in a critical point dryer. The sample was

subsequently recovered with a film of typically one

evaporator in high vacuum (sputter/coater Polaron

SC7640). Some micrographs were obtained using a

Philips XL-30 environmental SEM. The

specimens were deposited in the Colección

Nacional de Helmintos (CNHE) from Instituto de

Biología, Universidad Nacional Autónoma de

México (UNAM), CNHE: 9353– 9356. Prevalence

and mean intensity (± standard deviation)

following Bush et al. (1997) were used to describe

the infection of each cestode species.

A total of 7029 individuals from 21 species (Table

1) of helminths were collected. The Cestoda class

was the most representative with 20 species and the

Phylum Nematoda with one species. The intestinal

cestodes of C. limbatus are mainly of species

belonging to the orders Trypanorhyncha,

Tetraphyllidea and Onchoproteocephalidea.

All the host were parasitized by at least two species

of helminths. Only three sharks (10%) recorded the

highest number of species (12 species) and four

sharks (13%) the lowest number of species (two

species). The mean number of helminths by shark,

regardless of species, for the 39 hosts was 180 ±

225 individuals, with a range of 3 - 1177 helminths.

Of the 7029 helminths found, 64% correspond to

Paraorygmatobothrium cf sinuspersicense

(Malek, Caira & Haseli, 2010), followed by

Nybelinia sp.1 (Poche, 1926) (12%) and

Paraorygmatobothrium sp.1 (Ruhnke, 1994) (6%)

(Table 1).

The values of prevalence and mean intensity are

shown in Table 1; where the species of cestodes

with higher prevalence and mean intensity were

Paraorygmatobothrium cf sinuspersicense and

Nybelinia sp.1. (Fig. 1A). The remaining species

showed low prevalence values, parasitizing less

than 50% of the hosts, similarly their abundances

and mean infection intensity were low (Table 1).

All the helminths collected are new records for the

locality and the cestodes Oncomegas cf wageneri

(Palm, 1995); Paraorygmatobothrium cf

sinuspersicense (Fig. 1D); Anthobothrium

laciniatum (Linton, 1890); Rhinebothrium sp.

( L i n t o n , 1 8 8 9 ) ; T h y s a n o c e p h a l u m

t h y s a n o c e p h a l u m ( L i n t o n , 1 8 9 9 ) ;

Cathetocephalus thatcheri (Daily & Overstreet,

1973) (Fig. 1G); Poecilancistrum caryophyllum

(Diesing, 1850) (Fig. 1C) Disculiceps pileatus

(Linton, 1891) (Fig. 1F), as well as the nematode

Hysterothylacium sp. Ward & Magath, 1917, are

new records for C. limbatus.

This is the first study on intestinal helminths of the

blacktip sharks C. limbatus in Mexican waters of

the Gulf of Mexico, which consists of 21 species:

20 cestodes and 1 nematode. This high

composition of cestode species shows that C.

limbatus acts as the final host of a wide variety of

cestodes, indicating the presence of multiple prey

that act as intermediary hosts and that are part of the

diet of C. limbatus. Owens (2008) recorded 15

species of cestodes in 20 black tip sharks, C.

limbatus on the shores of Mississippi and Florida in

the Gulf of Mexico, while Méndez & Dorantes-

González (2013) recorded eight species of

tapeworms in bull shark Carcharhinus leucas

(Müller & Henle, 1839) in the Gulf of Mexico,

confirming the richness of helminths as predators.

The blacktip shark C. limbatus feeds on 99%

teleost fishes (de Silva et al. 2001; Barry, 2002),

that act as intermediate host of the four orders of

r e g i s t e r e d c e s t o d e s . T h e g e n e r a

Paraorygmatobothrium and Anthobothrium

Neotropical Helminthology, 2018, 12(2), jul-dic

RESULTS

DISCUSSION

Intestinal helminth parasites of blacktip shark

Helminths N Prevalence

(%)

Mean Intensity

± SD

Range

Order Tetraphyllidea Carus, 1863

Paraorygmatobothrium cf

sinuspersicense

(Malek, Caira & Haseli, 2010) 4516 89.74

129.03 ± 187.71

1─883

Paraorygmatobothrium sp. (Ruhnke, 1994) 405 43.59 23.82 ± 44.09

1─187

Anthobothrium laciniatum (Linton, 1890) 45 28.21 4.09 ± 7.33

1─26

Anthobothrium sp. 1 (Van Beneden, 1850) 96 38.46 6.4 ± 7.52

1─25

Anthobothrium sp. 2 (Van Beneden, 1850) 17 2.56 17 17

Rhinebothrium sp. (Linton, 1889) 2 5.13 1 1─1

Thysanocephalum thysanocephalum (Linton, 1899) 2 2.56 2 2

Order Cathetocephalidea Schmidt & Beveridge, 1990

Cathetocephalus thatcheri (Daily & Overstreet, 1973)

7.69

12 ± 12.17

4─26

Disculiceps pileatus

(Linton, 1891)

7.69

1.33

1─2

Order Onchoproteocephalidea Caira, Jensen,

Waeschenbach, Olson & Littlewood, 2014

Phoreiobothrium

sp. 1 (Ruhnke, 1994)

255

38.46

17 ± 37.33

1─137

Phoreiobothrium sp. 2 (Ruhnke, 1994)

211

48.72

11.11 ± 19.75

1─89

Phoreiobothrium

sp. 3 (Ruhnke, 1994)

10.26

7.5 ± 6.35

2─13

Order Trypanorhyncha

Diesing, 1863

Nybelinia

sp. 1 (Poche, 1926)

868

66.67

33.38 ± 33.63

1─136

Nybelinia

sp. 2 (Poche, 1926)

204

48.72

10.74 ± 14.47

1─49

Nybelinia

sp. 3 (Poche, 1926)

28.21

7.09 ± 7.06

2─25

Table 1. Helminth parasites collected in 39 spiral valves of Carcharhinus limbatus in Playa Chachalacas, Veracruz, México. The acronyms were the

following: N = number of individuals; SD = standard deviation.

216

Neotropical Helminthology, 2018, 12(2), jul-dic Miguel Angel Dorantes-González & Oscar Méndez

Eutetrarhynchidae

sp. 1 (Guiart, 1927)

136

48.72

7.16 ± 9.9 1─34

Eutetrarhynchidae

sp. 2 (Guiart, 1927)

12.82

5.2 ± 1.3 1─4

Oncomegas cf wageneri (Palm, 1995)

2.56

1 1

Poecilancistrum caryophyllum (Diesing, 1850)

5.13

2.5 2─3

Otobothrium australe (Palm, 2004)

10.26

1.5 ± 1 1─3

Order Ascaridida

Hysterothylacium sp. Ward & Magath, 1917 86 48.72 4.53 ± 5.99 1─26

Continued Table 1

Neotropical Helminthology, 2018, 12(2), jul-dic Intestinal helminth parasites of blacktip shark

217

Figure 1. Some cestodes presented in the blacktip shark Carcharhinus limbatus: Nybelinia sp.1. (A); Nybelinia sp. 2 (B);

Poecilancistrum caryophyllum (C); Paraorygmatobothrium cf sinuspersicense (D); Phoreiobothrium sp. 1 (E); Disculiceps

pileatus (F); Cathetocephalus thatcheri (G); genus Anthobothrium (H).

Neotropical Helminthology, 2018, 12(2), jul-dic Miguel Angel Dorantes-González & Oscar Méndez

218

219

(Tetraphyllidea) (Fig. 1H), as well as

Phoreiobothrium (Onchoproteocephalidea)

mature in large sharks (Carcharhiniforms) and their

larval stages only infect teleost fishes (Chambers et

al., 2000; Jensen & Bullard, 2010), suggesting that

teleosts occupy a place emphasized in the life

cycles of the species of these genera. However, a

diversity of other carcharhinid and sphyrnid sharks

have been reported as hosts for species of these

genera in the Gulf of Mexico (Jensen, 2009),

indicating that the web of trophic connections

among intermediate teleost hosts and

elasmobranch definitive hosts involved in the life-

cycles of species in these genera is likely much

more complex.

The cestodes Paraorygmatobothrium cf

sinuspersicense and Nybelinia sp. 1 were

numerically dominant species in our study,

followed by Paraorygmatobothrium sp.;

Phoreiobothrium sp. 1 (Ruhnke, 1994) (Fig. 1E);

Phoreiobothrium sp. 2(Ruhnke, 1994) and

Nybelinia sp. 2 (Poche, 1926) (Fig. 1B) (Table 1). A

similar pattern was found previously by Méndez &

Dorantes-González (2013) for the cestodes of bull

shark from the Chachalacas region, who reported

the trypanorhynchid cestodes Callitetrarhynchus

gracilis (Rudolphi, 1819) Pintner, 1931,

Otobothrium sp. 1 Linton, 1891 and Otobothrium

sp. 2 Linton, 1891 as numerically dominant

species. In contrast, Owens (2008) record the order

Tetraphyllidea with the highest composition of

species, according to Caira & Jensen (2014) these

species of cestodes belong to the orders

Tetraphyllidea (four species), to the order

Onchoproteocephalidea (six species), to the order

Cathetocephalidea (one species), and to the order

Trypanorhyncha (four species). In our study, three

s p e c i e s b e l o n g i n g t o t h e o r d e r

Onchoproteocephalidae are recorded, however, the

number of species may increase with a more

exhaustive review of the genus Phoreiobothrium.

The record of Oncomegas cf wageneri and

Rhinebothrium sp., extend its geographic

distribution range and register new hosts. Several

authors have reported the larva of O. wageneri

from host teleos intermediaries. Thatcher (1961)

records a plerocercoid of O. wageneri in Lutjanus

aya (Bloch, 1790) (Lutjanidae) collected in the

Gulf of Mexico, near Isla Grande, Louisiana, USA.

Vidal-Martínez et al. (2004) record O. wageneri in

the sole Syacium gunteri Ginsburg, 1933 in

Campeche, south of the Gulf of Mexico. O.

wageneri adults are recorded in the Dasyatis

centroura (Mitchill, 1815) (Rajiformes:

Dasyatidae) as a definite host for the Gulf of

Mexico (Toth et al., 1992). The presence of O.

wageneri in the blacktip shark C. limbatus

indicates that this shark is possibly feeding on

benthic fish such as S. gunteri and Paralichthys sp.

Girard, 1858. The rhinebothrideans parasitize

elasmobranchs (sharks and rays) as adults and their

larvae infect both teleosts and molluscs. In the Gulf

of México, the larval stages have been recorded in

the southern flounder, Paralichthys lethostigma

Jordan & Gilbert, 1884 (Paralichthyidae) (Jensen

& Bullard, 2010), although the consumption of

squid from the Loliginidae family is not ruled out

as part of the diet of C. limbatus (Barry, 2002).

The presence of Hysterothylacium sp., in C.

limbatus represent the first record of nematodes as

parasites of this shark. Méndez (2005) report

nematodes of the family Anisakidae in the blue

shark Prionace glauca (Linnaeus, 1758) for the

coast of Baja California Sur (Mexico). Moravec &

Justine (2006) report to Terranova scoliodontis

(Baylis, 1931) Johnston & Mawson (1945) in the

tiger shark Galeocerdo cuvier (Péron & Lesueur,

1822) in New Caledonia. The adult worms of

Hysterothylacium mostly parasitize the digestive

tract of fishes (Deardorff & Overstreet, 1980)

whereas the larval stages live in different tissues of

numerous fish species, which act as intermediate

and/or paratenic hosts (Køie, 1993). The present

finding of this species represent new host.

Paraorygmatobothrium sp. 1 together with

Nybelinia sp. 1 showed the highest values of

prevalence and intensity of infection. Malek et al.

( 2 0 1 0 ) m e n t i o n t h a t g e n d e r

Paraorygmatobothrium is the most common

parasite in carcharhinid sharks, mainly the genus

Carcharhinus (C. limbatus; Carcharhinus

acro notus (Poey, 1861); Ca rcha rhinus

amblyrhynchoide (Whitley, 1934); Carcharhinus

am boinensis (Müller & Henle, 1839);

Carcharhinus falciformis (Müller & Henle, 1839);

Carcharhinus melanopterus (Quoy & Gaimard,

1824); Carcharhinus obscurus (Lesueur, 1818);

Carcharhinus plumbeus (Nardo, 1827);

Carcharhinus sorrah (Müller & Henle, 1839) and

Carcharhinus leucas) (Ruhnke & Thompson,

Neotropical Helminthology, 2018, 12(2), jul-dic Intestinal helminth parasites of blacktip shark

2006; Méndez & Dorantes-González, 2013).

This study reports C. limbatus as a new host for

eight species of cestodes (P. cf sinuspersicense; A.

l a c i n i a t u m ; R h i n e b o t h r i u m s p . ; T.

thysanocephalum; C. thatcheri; O. cf wageneri; D.

pileatus; P. caryophyllum) and one species of

nematode (Hysterotylacium sp.). All the helminths

found in the blacktip shark C. limbatus represent

new records for the coastal zone of the state of

Veracruz, expanding their ranges of distribution

and contributing to the registration of helminth

fauna of elasmobranchs for the Gulf of Mexico.

To the laboratory of Hydrobiology, Facultad de

Biología, Universidad Veracruzana Campus

Xalapa (UV). To José Luís Recio Silva, Israel

Lozano, Jonathan Gómez and Yitzendi López

Serrano for their help in the field work. To the

fishermen of the locality of Playa Chachalacas and

to the staff of the fish shop "Carillo". To Ana Ruth

Cristobal by SEM (CINVESTAV─Mérida). Part of

this project was funded by the postdoctoral

CONACyT scholarship # 205133.

ACKNOWLEDGMENTS

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hosts of metazoan parasites. In: Carrier, JC,

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Received November 27, 2018.

Accepted December 25, 2018.

Neotropical Helminthology, 2018, 12(2), jul-dic Miguel Angel Dorantes-González & Oscar Méndez

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