acta parasitologica, 2016, 61(4), 713–719; issn 1230-2821 .... monocotyle n.sp… · were fixed...
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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: [email protected]
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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