DOI: 10.1515/ap-2016-0100© W. Stefański Institute of Parasitology, PASActa Parasitologica, 2016, 61(4), 713–719; ISSN 1230-2821

Monocotyle luquei n. sp. (Monogenea: Monocotylidae),from the gills of diamond stingray Dasyatis dipterura

(Jordan and Gilbert, 1880) (Myliobatiformes: Dasyatidae), in the South Pacific

Jhon D. Chero1, Celso L. Cruces1, José Iannacone2,3*, Lidia Sanchez4, David Minaya1, Gloria Sáez1 and Lorena Alvariño2

1Laboratorio de Parasitología, Facultad de Ciencias Naturales y Matemática (FCNNM), Universidad Nacional Federico Villarreal (UNFV),El Agustino, Lima, Perú; 2Laboratorio de Ecología y Biodiversidad Animal (LEBA), Facultad de Ciencias Naturales y Matemática

(FCNNM), Universidad Nacional Federico Villarreal (UNFV), El Agustino, Lima, Perú; 3Facultad de Ciencias Biológicas, Universidad Ricardo Palma (URP), Santiago de Surco, Lima, Peru; 4Departamento de Protozoología, Helmintología e Invertebrados afines,

Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Perú

AbstractMonocotyle luquei n. sp. (Monogenea: Monocotylidae) was described from gills of diamond stingray Dasyatis dipterura (Jordan and Gilbert, 1880) (Dasyatidae) off Peru. The new species can be differentiated from the other species of the genus by

the combination of the following characteristics: (1) accessory sclerites on the dorsal posterior surface of the body absent, (2)

only one testis is present, (3) 1–2 loops in the copulatory organ, (4) the male copulatory organ with a sclerotized accessory piece,

(5) shape of five sclerites in marginal papillae, (6) size of anchor and (7) posterolateral septa bifurcated. This is the first record

of species of Monocotyle Taschenberg, 1878 from the southern Pacific.

KeywordsDasyatidae, Diamond stingray, Monocotyle luquei new species, Monocotylidae, Monogenea, Pacific Ocean

Introduction

Monocotyle Taschenberg, 1878 (Monogenea: Monocotylidae),

as amended by Chisholm (1998) and Tazeuroti et al. (2011),

accommodates species possessing a haptor with 1 central and

8 peripheral loculi, which are surrounded by small sclerites

on the inner and outer rings, on the radial septa between the lo-

culi and on digitiform marginal papillae that are covered by a

marginal membrane, and additional vaginal sclerite sometimes

present in the proximal portion of the vagina. Currently, 18

valid species of Monocotyle are recognized, all of them hav-

ing been described in marine fishes of two different orders

(Myliobatiformes and Rajiformes) (Table I). In South Amer-

ica, only Monocotyle guttatae has been described from Dasy-atis guttata (Bloch and Schneider, 1881) off the coast of Brazil

(Portes Santos et al. 2006; Cohen et al. 2013).

During a parasitological survey of marine fish from Peru,

specimens representing a new species of the genus Mono-

cotyle were found on the gills of the stingray Dasyatisdipterura (Jordan and Gilbert, 1880) (Dasyatidae). In this

paper, this new species is described.

Materials and Methods

Five individuals of D. dipterura were collected in April 2015

off the coast of Chorrillos, Lima, Peru, using gillnet and were

dissected shortly after capture. Gills excised from fish were

placed in Petri dishes with tap water and examined for mono-

geneans using dissecting microscope. Monogeneans found

were fixed in 4% hot formalin, slightly flattened between slide

and coverslip, stained with Gomori’s trichrome and mounted

in Canada balsam to study internal organs.

Drawings were made with a Leitz microscope drawing

tube. All measurements are given in micrometres by the range

followed with mean in parentheses, and the number measure-

*Corresponding author: joseiannacone@gmail.com

Author's copy

Jhon D. Chero et al.714

Tab

le I

. L

ist

of

val

id s

pec

ies

of

Mon

ocot

yle

Tas

chen

ber

g, 1878

Sp

ecie

sH

ost

Host

fam

ily

Cou

ntr

yR

efer

ence

s

M. a

ncyl

osto

mae

Tim

ofe

eva,

1984

Rhin

a an

cylo

stom

a B

loch

and S

chnei

der

, 1801*

Rhin

idae

Chin

aT

imofe

eva

(1984)

M. c

asey

aeC

his

holm

and W

hit

tingto

n, 2005

Him

antu

ra sp

.*

Him

antu

ra u

arna

k(G

mel

in, 1789)

Him

antu

ridae

Aust

rali

aC

his

holm

and W

hit

tingto

n (

2005)

M. c

oral

iChis

holm

, 1998

Past

inac

hus s

ephe

n (F

ors

skål

, 1775)*

Pas

tinac

hid

aeA

ust

rali

aC

his

holm

(1998)

M. d

iade

mal

isH

argis

, 1955

Das

yatis

sabi

na (L

esueu

r, 1

824)*

Das

yatis

sp.

Das

yat

idae

US

AC

his

holm

(1998)

M. g

ranu

lata

eYoung, 1967

Him

antu

ra g

ranu

lata

(Mac

Lea

y, 1

883)*

Him

antu

ridae

Aust

rali

aC

his

holm

(1998)

M. g

utta

tae

Port

es S

anto

s, S

anto

s an

d G

ibso

n, 2006

Das

yatis

gut

tata

(Blo

ch a

nd S

chnei

der

, 1801)*

Das

yat

idae

Bra

zil

Port

es S

anto

s et

al.

(2006)

M. h

elic

opha

llusM

easu

res,

Bev

erle

y-B

urt

on a

nd W

illi

ams,

1990

Him

antu

ra fa

i Jord

an a

nd S

eale

, 1906*

Him

antu

ridae

Aust

rali

aM

easu

res

et a

l. (1

990)

M. i

jimae

Goto

, 1894

Das

yatis

pas

tinac

a (L

innae

us,

1758)*

Das

yat

idae

Japan

Chis

holm

(1998)

M. j

orda

niC

his

holm

, 1998

Myl

ioba

tis te

nuic

auda

tus H

ecto

r, 1

877*

Myli

obat

idae

Aust

rali

aC

his

holm

(1998)

M. k

uhlii

Young, 1967

Neo

tryg

on k

uhlii

(Müll

er a

nd H

enle

, 1841)*

Neo

trygonid

aeA

ust

rali

aC

his

holm

(1998)

M. l

uque

in. sp

.D

asya

tis d

ipte

rura

(Jord

an a

nd G

ilber

t, 1

880)*

Das

yat

idae

Per

uP

rese

nt

study

M. m

ultip

arou

sMea

sure

s, B

ever

ley-B

urt

on a

nd W

illi

ams,

1990

Him

antu

ra fa

i Jord

an a

nd S

eale

, 1906*

Him

antu

ridae

Aust

rali

aM

easu

res

et a

l. (1

990)

M. m

ylio

batis

Tas

chen

ber

g, 1878**

Myl

ioba

tis a

quila

(Lin

nae

us,

1758)*

Myli

obat

idae

Ital

yC

his

holm

(1998)

M. p

rice

iPea

rse,

1949

Das

yatis

am

eric

ana

Hil

deb

rand a

nd S

chro

eder

,

1928*

Das

yatis

say

(Les

ueu

r, 1

817)

Das

yat

idae

US

AC

his

holm

(1998)

M. s

pire

mae

Mea

sure

s, B

ever

ley-B

urt

on a

nd W

illi

ams,

1990

Him

antu

ra fa

i Jord

an a

nd S

eale

, 1906*

Him

antu

ridae

Aust

rali

aM

easu

res

et a

l.(1

990)

M. s

piro

phal

lus(

Tri

pat

hi,

1959)

Tim

ofe

eva,

1985

Past

inac

hus s

ephe

n (F

ors

skål

, 1775)*

Pas

tinac

hid

aeIn

dia

Chis

holm

(1998)

M. t

rite

stis

Young, 1967

Neo

tryg

on k

uhlii

(Müll

er a

nd H

enle

, 1841)

*N

eotr

ygonid

aeA

ust

rali

aC

his

holm

(1998)

M. u

ndos

ocir

rusT

imofe

eva,

1984

Gym

nura

japo

nica

(Norm

an, 1925)

*G

ym

nuri

dae

Chin

aT

imofe

eva

(1984)

M. y

oung

iChis

holm

, 1998

Him

antu

ra fa

i Jord

an a

nd S

eale

, 1906*

Him

antu

ridae

Aust

rali

aC

his

holm

(1998)

*T

ype

host

. H

ost

fam

ilie

s fo

llow

Lim

et a

l.(2

015).

** T

ype

spec

ies

Author's copy

Monocotyle luquei n. sp. from stingray in the South Pacific 715

ments (n). Haptoral terminology follows that Neifar et al.(1998). Worm length is given as the body length excluding the

haptor, and length of the male copulatory organ is the total

length including the loops. Terminology and measurements of

anchors (blade, guard, handle and point) followed Tazerouti

et al. (2011) and Pulido-Flores et al. (2015). Sclerites of the

haptor are classified as unicuspid, bicuspid, tricuspid, quadri-

cuspid and pentacuspid according to Neifar et al. (1998).

Dasyatis dipterura was identified employing the keys of

Peruvian marine fishes of Chirichigno and Vélez (1998), and

nomenclature of host families follow keys of Lim et al.(2015). The current name of the host, D. dipterura, follows

Smith et al. (2006).

Type material is deposited in the Helminthological and Re-

lated Invertebrates Collection of the Museum of Natural His-

tory at the San Marcos University (MUSM-UNMSM), Peru,

Nacional Collection of Helminths, Institute of Biology, Na-

tional Autonomous University of Mexico, UNAM, (CNHE),

Mexico and in the Scientific Collection of Protozoa and Meta-

zoan Parasites of the Federico Villarreal University (CPMP-

UNFV), Peru.

Results

Class Monogenea Van Beneden, 1858

Subclass Polyonchoinea Bychowsky, 1937

Order Monocotylidea Lebedev, 1988

Family Monocotylidae Taschenberg, 1878

Subfamily Monocotylinae Taschenberg, 1878

Monocotyle luquei sp. n. (Figs. 1–9)

Description (based on 10 specimens): Body 2.25–2.55 mm

(2.39 mm) (n = 10) long and 499–581 (549) (n = 10) wide at

level of ovary (Fig. 1). Haptor subcircular, 777–992 (899) (n

= 10) long and 615–800 (726) (n = 10) wide, with posterior

half little more wide than anterior. Haptor with one central and

8 peripheral loculi (Fig. 1). Sclerotized anchor well- devel-

oped, 251–305 (279) (n = 20) long, nearly similar in size

as medial posterolateral radial septa, posterolateral septa

bifurcated; anchor with long handle (236–298) (266) (n = 20),

reduced guard 24–31 (29) (n = 20), short blade 70–73 (72)

(n = 20), and acute point 30–36 (32) (n = 20) (Fig. 2). Four-

teen uncinuli (7 pairs), 11–14 (13) (n = 21) long, distributed

symmetrically around marginal membrane (Fig. 4). Haptoral

sclerites of 4 types: bicuspid, tricuspid, quadricuspid and pen-

tacuspid (Figs 3, 5). Sclerites of inner ring (surrounding cen-

tral loculus) quadricuspid, intercalating with single

pentacuspid sclerite at level of each radial septum (Fig. 5).

Sclerites of radial septa from inner to outer extremities start

with single pentacuspid on inner ring, followed by 15–23

quadricuspid sclerites. Single row of marginal haptoral papil-

lae around ventral margin of haptor, 92–96 in number; papil-

lae digitiform, 10–15 papillae on each loculi, each armed with

5 sclerites arranged, from inner to outer end, as 1 tricuspid,

3 bicuspid, and 1 terminal quadricuspid; single tricuspid scle-

rite between each marginal papillae (Fig. 5).

Cephalic complex consists of 22 cephalic organ adhesives,

11 on each side of side on margins of anterior part of body,

communicate through fine ducts, with glands on either side of

pharynx (Fig. 6). Mouth ventral, subterminal, surrounded by

muscular pseudosucker. Pharynx pyriform, with thick muscu-

lar walls, 174–220 (188) (n = 9) long and 132–163 (140)

(n = 9) wide. Unbranched intestinal blind not converged pos-

teriorly. Oesophagus short. Eye-spots as highly dispersed

pigment granules anterodorsal pharyngeal area. Posterodorsal

body surface lacks accessory sclerites, contains weakly

developed, muscular structure.

Testis single, 329–689 (473) (n = 10) long, 221–349 (290)

(n = 10) wide, elongated, subquadrangular, posterior to ovary,

vas deferens arises from left anterior margin of testis, passes

ventrally toward viteline duct and vagina, but dorsally toward

male copulatory organ. Vas deferens clockwise right, expand-

ing to form seminal vesicle, which enters posterior end of ejac-

ulatory bulb. Ejaculatory bulb bipartite, 112–129 (119)

(n = 10) long, 74–114 (93) (n = 10) wide, posterior portion

containing sperm, anterior region with thick muscular walls.

Male copulatory organ 449–491 (473) (n = 8) long, with 1–2

proximal loops and a slight straight in distal end near begin-

ning of accessory piece. Accessory piece sclerotized, 76–89

(83) (n = 8) long, near genital pore (Fig. 7).

Ovary V-shaped, in all specimens with right arm larger than

left, left arm straight and more anterior, right arm slightly sin-

uous. Right arm passes over right intestinal caecum, forming

short oviduct. Vitelline follicles extending from anterior mar-

gin of pharynx to anterior haptoral margin. Yolk transverse

ducts join oviduct at level of ovary. Oval seminal receptacle

63–112 (82) (n = 10) long, 54–83 (64) (n = 10) wide, con-

nected to oviduct by narrow duct. Vagina sclerotized, long,

with a basal quadrangular sclerotized; Spermatophore acorn-

shaped; vaginal pore sinistral, unarmed. Mehlis gland and ducts

present at base of oötype. Oötype with thick glandular walls in

diameter 68–124 (102) (n = 10) long; uterus pyriform, opens

into common genital pore. Eggs tetragonal, 85–113 (95) (n = 3)

long, 73–120 (94) (n = 3) wide, with posterior polar filament,

137–178 (158) (n = 3) long, with terminal knob (Figs 8–9).

Type host: Dasyatis dipterura (Jordan and Gilbert, 1880)

(Dasyatidae).

Site of infection: Gills.

Type-locality: Chorrillos, Lima, Peru (12°30`S, 76°50`W).

Prevalence: Two of five hosts infected with a total of 14

worms.

Intensity: 6–8.

Type material: Holotype MUSM 3245; paratypes MUSM

3246; paratypes CNHE 9877; voucher CPMP-UNFV 160-161.

Etymology: The species epithet is in honor of Jose Luis

Fernando Luque Alejos (Federal Rural University of Rio de

Janeiro, Brazil) for his contribution to the Neotropical ichthy-

oparasitology.

Author's copy

Jhon D. Chero et al.716

Figs 1–7. Monocotyle luquei n. sp. from Dasyatis dipterura. Holotype MUSM-UNMSM Coll. N° 3245. 1. Whole-mounted specimens (ventral view). 2. Hamuli. 3. Configuration of sclerites of the inner ring of the central loculus. 4. Uncinuli. 5. Sclerites on marginal haptoralpapillae. 6. Adhesives cephalic organs. 7. Male copulatory organ. 8. Egg

Author's copy

Monocotyle luquei n. sp. from stingray in the South Pacific 717

Fig. 9. Monocotyle luquei n. sp. from Dasyatis dipterura. Holotype MUSM-UNMSM Coll. N° 3245. Reproductive system in ventral view.Abbreviations: ap, accessory piece; eb, ejaculatory bulb; mco, male copulatory organ; ov, ovary; spm, spermatophore; sr, seminal recepta-cle; sv, seminal vesicle; t, testis; tvd, transverse vitelline ducts; vd, vas deferens; vp, vaginal pore

Author's copy

Jhon D. Chero et al.718

Differential diagnosis

Monocotyle luquei n. sp. could be easily distinguished from

all congeners by presenting the posterolateral septa bifur-

cated. The new species also differs from M. pricei Pearse,

1949, M. diademalis Hargis, 1955, M. kuhlii Young, 1967,

M. youngi Chisholm, 1998 and M. caseyae Chisholm and Whit-

tington, 2005, because these species present accessory scle-

rites on the dorsal posterior surface of the body but they are

absent in M. luquei n. sp. Monocotyle ijimae Goto, 1894 and

M. tritestis Young, 1967 have three testes, whereas M. luquein. sp. has only one testis. Considering the number of loops of

the copulatory organ, M. luquei n. sp. can be distinguished

from M. myliobatis Taschenberg, 1878, M. spirophallus(Tripathi, 1959), M. granulatae Young, 1967, M. ancy-lostomae Timofeeva, 1984, M. undosocirrus Timofeeva,

1984, M. corali Chisholm, 1998 and M. jordani Chisholm,

1998 by the possession 1–2 loops, whereas the eight other

species have from 4 to 20 loops. Monocotyle helicophallusMeasures, Beverley-Burton and Williams, 1990 and M. mul-tiparous Measures, Beverley-Burton and Williams, 1990 do

not have a sclerotized accessory piece of the male copulatory

organ, whereas the sclerotized accessory piece is present in

the new species. Monocotyle luquei n. sp. differs from

M. spiremae Measures, Beverley-Burton and Williams, 1990

by the number of sclerites in marginal papillae (three scle-

rites in M. spiremae and five in M. luquei n. sp.) and the shape

of the copulatory organ. The new species is most similar to

M. guttatae Portes Santos, Santos and Gibson, 2006, but it

can be easily distinguished by the following features: (1)

number of sclerites in marginal papillae (papillae with 5–7

sclerites in M. guttatae versus papillae only with 5 sclerites in

M. luquei n. sp.); (2) size of anchor (132–189 in M. guttataeand 251–305 in M. luquei n. sp.).

Discussion

In South America, Cohen et al. (2013) registered 23 species

of monocotylid monogeneans. Of these species 11 parasitize

marine and 12 freshwater fishes. Only one species, M. gut-tatae was described from a marine chondrichthyan fish from

Brazil. Most records were from the North Atlantic (off Florida

and Chesapeake Bay), Indian and Pacific Ocean (Table I)

(Portes Santos et al. 2006). Ten species of Monocotyle are

parasites of chondrichthyan fishes in Australian waters

(Chisholm and Whittington 2005; Tazerouti et al. 2011; Lim

et al. 2015).

Most of the hosts of Monocotyle belong to Himanturidae

and Dasyatidae (Chisholm, and Whittington 2005; Tazerouti

et al. 2011). Six species are parasites of the genus Dasyatis, six

of Himantura J. P. Müller and Henle, 1837, two of Pasti-nachus Rüppell, 1829 and two of Neotrygon Castelnau, 1873.

The remaining species occurs on species of MyliobatisCuvier, 1816 (2), Gymnura van Hasselt, 1823 (1) and Rhina

Bloch and Schneider, 1801 (1) (Table I). Himantura fai Jordan

and Seale, 1906, Pastinachus sephen (Forsskål, 1775) and

Neotrygon kuhlii (Müller and Henle, 1841) are hosts harbor-

ing four, two and two species of Monocotyle, respectively

(Table I).

Dasyatis dipterura, host of M. luquei n. sp., is typically

a subtropical to tropical species. The confirmed range of its

distribution is from southern California, USA to Chile (where

it occurs only occasionally); including the Galápagos and

Hawaiian Islands. This host does not overlap in its geographic

distribution with other hosts of Monocotyle registered all over

the word (Smith et al. 2006).

Acknowledgments. We are grateful to Tomas Scholz for

useful comments on an early draft of the manuscript.

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Monocotyle luquei n. sp. from stingray in the South Pacific 719

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