CONFIRMATION OF CENTROCESTUS FORMOSANUS

Research and Reviews in Parasitology, 54 (2): 99·103 (1994)
© 1994 Asociacion de Parasitologos Espanoles
CONFIRMATION
Editorial
Fontalba,
Printed
OF CENTROCESTUS FORMOSANUS (NISHIGORI,
(TREMAlODA: HETEROPHYIDAE) IN MEXICO
S.A.
in Spain
1924) PRICE, 1932
D. AMAYA-HUERTA1& R.J. ALMEYDA-ARTIGAS2
1 Laboratorio
de Helmintologia,
Instituto de Biologia, Universidad Naciona/ Aut onomo de Mexico,
Apdo. Postal 70·/53, Delegacion Coyoacdn, 045/0, Mexico D.F., Mexico
2Laboratorio de Sanidad Acuicola, Universidad Aut onoma Metropolitona-Xochimilco,
Calzada del Hueso No. 1100, Col. ViI/a Quietud, Detegacion Coyoacdn, 04960, Mexico D.F., Mexico
Received 22 September
1993; accepted
20 April
1994
REFERECE:AMAYA-HUERTA
(D.) & ALMEYDA-ARTIGAS
(R.J.), 1994.- Confirmation of Centrocestus formosanus (Nishigori, 1924) Price,
19J2 (Trematoda: Heterophyidae) in Mexico. Research and Reviews in Parasitology, 54 (2): 99-103.
ABSTRACT:
A distome leptocercous cercaria shed by Melanoides tuberculata (Muller, 1774) (Prosobranchia: Thiaridae) collected from a
stream near «Las Estacas» Spa, Morelos State that fitted completely the morphometric descriptions known for Centrocestus formosanus
(Nishigori, 1924) Price, 1932, an heterophyid trematode native of Southeast Asia, is described chaetotaxilly for the first time in Mexico.
Thus, the taxonomic importance of this powerful tool and inexpensive method is heightened. The way C formosanus was introduced accidentally to Tezontepec de Aldama's cyprinid-breeding Station in 1979 (through imported Chinese snails) and the role of fish-eating birds
(Ardeidae) as its natural definitive potential hosts in both localities are briefly discussed. Finally, the fluke's colonizing ability and the
factors that may speed up its dispersion within the Mexican territory are fully discussed.
KEYWORDS:Trematoda, Centrocestusformosanus,
Taxonomy.
cercarial chaetotaxy,
INTRODUCTION
Centrocestusformosanus
(Nishigori, 1924) Price, 1932
is an heterophyid
trematode
of Southeast
Asian origin.
It uses 2 thiarid prosobranch
gastropods,
Me/anoides
tubercu/ata (Muller, 1774) and Stenomelania newcombi
Lea, as first intermediate
hosts in Asia and Hawaii,
respectively. Several species of fresh-water fishes and tadpoles are second intermediate
hosts, and adults are found
in piscivorous
birds and carnivorous
mammals
(CHEN,
1942; CHEN, 1948; MARTIN, 1958; MADHAVI & RUKMINI,
1991). In the past decade BAYSSADE-DuFOUR, ALBARET
& Ow-Y ANG (1982) practiced
a chaetotaxic
study on
Malaysian
cercariae shed by M tuberculata.
This snail is native from Africa eastward to the East
Indies. Actually, populations
live in various isolated freshand brackish-water
bodies in tropical, subtropical,
and
temperate regions (SMITH, 1989). Accidentally
introduced to the Caribbean area around 1960, possibly through
the aquatic plant trade (POINTlER, 1989), it was subsequently used as a biological control against local Biomvector
phalaria spp. populations (human schistosomiasis
snails) by competitive exclusion (SMITH, 1989; POINTlER
& MCCULLOUGH, 1989).
M tubercu/ata was first observed in Mexico from
Veracruz State about 21 years ago, according to ABBOTT
(1973); however, POINTlER & MCCULLOUGH (1989) mentioned Coahuila State as its first record in 1980. Its present distribution
includes more than 60 localities of 13
states (Fig. 1) (CONTRERAS-ARQUIETA, pers. comm.) and,
recently, «Presidente
Miguel Alernan» dam, Oaxaca (second author's field observation)
(Fig. 1). It was reported
as a C. formosanus intermediate
host in 1985 from one
of the most important
cyprinid-breeding
fish farms,
Prosobranchia, Melanoides tuberculata. Morelos State, Mexico.
Tezontepec de Aldama Station, Hidalgo State (LOPEZJIMENEZ, 1987) (Fig. 1). Gill arch filaments
of 8
cultivated carp species were found to carry heavy burdens
of encysted metacercariae,
causing severe respiratory
damages and death of the host fishes (LOPEZ-JIMENEZ,
1987; ARIZMENDI, 1992), which fully illustrates
the
sanitary significance
of this fluke. From Morelos and
Veracruz
states,
SALGADO-MALDONADO,
V ARGASRODRiGUEZ & CAMPOS-PEREZ (1994) recorded M. tuberculata and Xiphophorus
helleri (Poeciliidae),
and
Gobiomorus dormitor (Gobiidae), respectively, as intermediate
hosts of this heterophyid
(Fig. I). In all 3
Fig. L- Present distribution of Melanoides tuberculata and Centrocestusformosanus in Mexico (o=«Las Estacas» Spa, Morelos
State; :::: = states in which the snail host has been recorded;
• = «Prcsidente Miguel Alernan» dam, Oaxaca State; ~ = states in
which both the thiarid snail and natural cercariae and metacercariae
have been recorded).
D. AMAYA-HUERTA& R.J. ALMEYDA-ARTIGAS
lOO
instances, specific identification
was based either upon
natural cercarial and metacercarial
morphometric
comparative studies or experimentally-recovered
adults.
Hence, the present study deals with the comparative
chaetotaxic
study of a cercaria shed by M. tubercula ta,
identified as C. formosanus on morphometric
grounds,
and its confirmation
within Mexican territory.
MATERIAL A D METHODS
Molluscs were collected manually from a stream near «Las
Estacas» Spa from February to August 1992. The stream is located
about 300 km southwest of Mexico City, in Morelos State (Fig. I).
In the laboratory, the snails were placed in 50 x 25 x 25 cm aquaria
with aerated water at 25° C, and fed ad libitum with Tetralvlin'"
flake food. Snails carrying mature infection were isolated as in
MALEK& CHENG(1974). Newly shed cercariae were studied live,
unstained and stained with vital stains, and as fixed permanent whole
mounts. Cercariae were killed in hot water, fixed in 5070formalin,
preserved in 70070ethanol, and mounted in a 1:1 mixture of Amman's lactophenol and Faore's liquid. Body proportions were
measured by ocular micrometer. COMBES,BAYSSADE-DuFOUR
&
CASSOE's (1976) method was employed for silver nitrate papillae
impregnation, choosing newly emerged cercariae; for its designation,
RICHARD's(1971) nomenclature was followed.
Cephalic region: It bears 33 to 36 papillae,
five cycles (Fig. 2, 3 and 4):
Cl =1 CII, 11-12 CI2
CII = 1 Clll, 3 C1I2, 2 C1I3, 2 or I CII4
CIII =2 Cllll, 2 C1I12, 3 CII13
Cly=2 Clvl, 1 CIy2
Cy=2 c.i, 0 or I Cy2, 2 Cy3
Corporal region: It bears 16 to 21 papillae
AI =2 AIV, 3-4 AIL, 1 AID
All = I AIIIV, 1-2 AIIL, 2 or 3 AIID
AIII=1 AIIIV, I or 2 AIIP
M=O MV, I ML, 3 MD
PII=1 PilL
distributed
in
(Fig. 4):
Tail:
U=2
UD
Remarks
Cercariae
used for chaetotaxic
study were morphometrically
identical to C. formosanus described by
CHEN (1948). Specimen measurements
were greater than
those mentioned
by ARIZMENDI (1992), probably due to
RESULlS
Centrocestus formosanus (Nishigori, 1924) Price, 1932
Host: Melanoides tuberculata (Muller,
1774) (Prosobranchia: Thiaridae).
Locality: Stream near «Las Estacas» Spa, Morelos State,
Mexico.
Material deposited: Laboratorio
de Sanidad Acuicola,
Universidad
Aut6noma
Metropolitana-Xochimi1co,
Mexico
City, Mexico
(LSAUAMX
015-01: 700/0
ethanol;
LSAUAMX
015-02:
permanent
whole
mounts).
Morphometry
of the cercaria
Cercariae, shed diurnally before noon, fully agree morphologically with the descriptions and drawings of C. formosanus from M. tuberculata of China, Hong Kong,
Taiwan, and Mexico (CHEN, 1948; ARIZMENDI, 1992),
and
S. newcombi
of Hawaii
(MARTIN,
1958).
Measurements
(given in JAm, with average in parentheses)
of 30 fixed and stained specimens,
without cover glass
pressure, are: body length 113-154 (140); body width 76-103
(83); oral sucker length 28-36 (33); oral sucker width 27-35
(30); pharynx diameter 13-16 (14); ventral sucker diameter
21-26 (24); tail length 114-155 (131); tail width 18-24 (20).
Fig. 2.- Ventral cephalic region of the cercaria of Centrocestus formosanus (Nishigori, 1924) Price, 1932 shed by M. tuberculata
(Miiller) from Mexico: A) I CIII; B) 3 C1I2; C) 2 C1I3; D) 2 CIIII;
E) 2 C1I12;F) 2 Clvl; G) I Cvl (in part). Scale bar=6,5 I'm.
Cercarial chaetotaxy in sagital plane
The
in Fig.
ings of
Fig. 1
cercarial chaetotaxy
in sagital plane is illustrated
2, 3 and 4. For more details, see the original drawBAYSSADE-DuFOUR, ALBARET & Ow-Y ANG (1982:
and 3).
Fig. 3.- CentrocestusJormosanus cercarial dorsal anterior end: A)
I Cly2; B) 2 Cv3. Scale bar=6,5 I'm.
Centrocestus formosanus confirmation
in Mexico
101
it would be convenient
to address
systematic
and
phylogenetic
principles to cercariae rather than to adult
forms, mainly on chaetotaxic grounds. The taxonomic importance of this efficient, simple, powerful, and practical
tool and inexpensive method is known for a great number
of invertebrates;
in cercariae, specially, this aspect of the
distribution
of cilia has been comparatively
poorly
studied.
However, these sensory receptors,
which are
directly connected with the nervous system, are as stable
as the excretory apparatus and less subject to convergences
and adaptative
phenomena
than general morphology
(RICHARD, 1971). Clearly, the present study strongly supports Richard's
standpoint.
Centrocestiasis
was discovered,
in Mexico,
from
Tezontepec's
Station around 1985 in the first fingerling
generation
of China's
black carp Mylopharyngodon
piceus (L6PEZ-JIMENEZ, 1987). According to him, the
fluke was introduced
in 1979 together with 5 black carp
mating couples from Shangai. If this is true, the existence
of natural pre-existing definitive and first intermediate
potential hosts, needed to complete its life cycle successfully and to establish itself permanently
in the area, are tacitIyassumed.
Field observations
of Tezontepec's
contiguous
zones
yielded the presence of several bird (Ardeidae) and mammal (Rodentia and Carnivora) species that act as natural
definitive hosts in China (CH EN, 1942), Hawaii (MARTIN,
1958), India (PREMVATI & PANDE, 1974), and Japan
(Y AHONARA, 1985). In spite of this, it seems quite im-
o
A
E
®
Fig. 4.- Ventral right sagital plane of the cercaria of Centrocestus
formosanus: A) 2 C,vl; B) 2 Cvl; C) 2 A,Y; D) I AIIY; E) I AII,Y.
Scale bar= 15 Ilm.
the type of killer medium employed (hot 10070 formalin),
lesser number (12), and nature (immature,
isolated from
dissected snails) of the examined larvae.
The resultant cilia distribution
is drastically
distinct
from that described for Centrocestus sp. (due to the 20
differences encountered)
and essentially indistinguishable
from that reported
for Malaysian
C. formosanus
(BAYSSADE-DuFOUR, ALBARET & Ow-Y A G, 1982), the
Mexican form differing
exclusively in the number of
AII,Y observed papillae (Fig. 4 and Table I).
DISCUSSION
At present, Trematoda systematics lies basically, on the
species level, in generally
questionable
adult
morphological
characters;
on the generic and supra generic
levels, it lies in commonly
arbitrarious
appreciations.
Thus, the phylogeny of the group appears quite obscure.
Since trematodes
were originally parasites of molluscs
(and not of vertebrates),
RICHARD (1968) proposed that
Centrocestus
Species
sp.
Malaysia'
Country
Host
15
2
3
3
Cv3
I
11-12
3
2
2
3
2
2
2
2
o
I
I
o
A,Y
AIIY
AII,Y
A,vY
A,L
AIIL
A,vL
ML
P,L
AIID
AII,D
MD
1.-
formosanus
Malaysia' & Mexico
Melanoides tuberculata
C,2
CII2
CIIII
C",2
CII,3
C,vl
Cvl
Table
Centrocestus
I or 2
I or 2
I
I
4
I
I
0-1"
o
3-4
1-2
o
o
I
o
I
I
I
2
Chaetotaxic
differences
2 or 3
I or 2
3
between
the cercariae
of Cen-
trocestus sp. from Malaysia and of Centrocestus formosanus from
Malaysia and
YANG, 1982;
Mexico (' = BAYSSADE-DuFOUR,
ALBARET & O\\,rarely I for Malaysia, I for Mexico).
'* = 0
102
probable that any of them could have preyed on these 1,5
m mating carps (live or dead). Besides, this species has
never been autochthonously recorded as a C. formosanus
second intermediate host.
Although the prosobranch was wanting, thousands of
Chinese M. tuberculata were introduced simultaneously
as a food source for this malacophagous
cyprinid
(LOPEz-JIMENEz, pers. comm.). Thus, the authors dissent with the hypothesis referred to and consider that the
parasite arrived in sporocyst or redial stage. The rapid colonization of other culture pools where 5 carp species introduced since 1965 were being cultivated, could have
allowed emerged cercariae to invade gill arch filaments
and, in consequence, facilitated their further development.
As already stated, M tuberculata has demonstrated its
capacity to colonize rapidly and densely many types of
habitats. In Mexico, it was first collected around 1973
from Veracruz City proximities (ABBOTT, 1973); this
author related its presence to the rapid southward dispersion pattern, from southern U.S.A. towards Central and
South America. In spite of its present distribution, it has
never been recorded as a C. formosanus first intermediate
host from any neotropical country. Seemingly, it is quite
improbable that the presence of this heterophyid in Mexico (Hidalgo, Morelos, and Veracruz, hitherto known
states) is directly and causally associated with the
mollusc's previous accidental introductions, migrations
and dispersion pattern.
It may be true that M. tuberculata came to Morelos
State due to a rapid southward dissemination; nevertheless, the authors believe instead that C. formosanus
occurence in «Las Estacas» Spa is intimately related with
fish-eating birds' egg dispersal (possibly of Ardeidae
naturally infected in Tezontepec's Station), both states being surely included in their migratory routes. The role of
herons, egrets, and bitterns (Nycticorax nycticorax, Ardea
spp., Egretta spp., Bubulcus ibis, Butorides striatus
virescens and Ixobrychus exilis, among others) as natural
definitive hosts in the 2 localities remains to be investigated.
The thiarid snail's distribution combined with the extensive carp transplantation
to different aquatic environments (fish farms, rustic culture-pools, dams, and
river basins) and the low host specificity exhibited by C.
formosanus within second intermediate and definitive
hosts may speed up its dispersion, and therefore it may
colonize the Mexican territory almost entirely in the next
few years. As stated above, egg dissemination by migratory
birds could play an essential role in the development
phenomenon. The high density of the snail in a given area
would permit a massive invasion of hatched miracidia,
an increase in the density of infective stages, and hence
the recruitment of cercariae into almost any fish host
population. Correspondingly, an increase in the density
of infection in fish hosts would also occur (MADHAVI&
RUKMINI, 1991). Finally, metacercarial establishment
within intestines of piscivorous birds and carnivorous
mammals occuring in the newly-colonized area could easily take place.
D. AMAYA-HUERTA
& R.J. ALMEYDA-ARTlGAS
CONCLUSIO S
The nervous papillae distribution observed in the leptocercous cercaria shed by Melanoides tuberculata of «Las
Estacas» Spa (indistinguishable from that recorded for
Malaysian larvae) confirms the presence of Centrocestus
formosanus in Mexican territory. Thus, the taxonomic
value of this powerful and inexpensive method is
strengthened. It is believed that this Asian heterophyid
arrived accidentally in Hidalgo State in partenite-bearing
Chinese M. tuberculata introduced simultaneously as a
food source of the China's black carp Mylopharyngodon
piceus in 1979. Fish-eating migratory birds may play an
essential role in the fluke's dispersion to Morelos State.
Finally, this parasitosis may have dangerous repercussions
in fish-farm fingerling production and hence in regional
economical
activities, due to the biological and
behavioural features of C. formosanus, its intermediate
and definite hosts, and common transplantation
of
cyprinid species to different aquatic environments.
ACK OWLEDGME
TS
The authors wish to express their thanks to Biol. lsabel JirnenezGarcia, Laboratorio de Helrnintologia, Instituto de Biologia, UNAM,
and Mr. Manuel Arnaya-Huerta,
for helping in field collections, and
Pas. Biol. Victor R. Zarate-Rarnirez,
Laboratorio
de Sanidad
Acuicola, UAM-Xochimilco,
for assisting with maps.
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