© W. Stefan ´ski Institute of Parasitology, PAS
Acta Parasitologica, 2012, 57(2), 149–153; ISSN 1230-2821
Description of Maritrema formicae sp. nov.
(Digenea, Microphallidae) parasitic in the kelp gull,
Larus dominicanus, from the Patagonian coast, Argentina
Julia I. Diaz1*, Carmen Gilardoni2and Florencia Cremonte2
1Centro de Estudios Parasitológicos y de Vectores (CCT La Plata, CONICET-UNLP), Calle 2 # 584, 1900 La Plata, Argentina;
2Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, U9120ACD Puerto Madryn, Chubut, Argentina
Maritrema formicae sp. nov. is described from the Patagonian coast, Argentina, based on adults obtained from the kelp gull,
Larus dominicanus. The new species fits with the “eroliae complex” and can be distinguished from other related species mainly
in shape and size of body, shape, size, and pattern of distribution of cirrus spines, uterus extension, number and size of eggs,
vitellarium in a complete ring in all specimens, and its Neotropical distribution. The new species is sympatric with another
species of the genus, Maritrema madrynense, which was recorded in the same host and locality.
Trematode digeneans, Maritrema, Microphallidae, Larus, Patagonia, Argentina
Species of Maritrema Nicoll, 1907 (Microphallidae) are par-
asites mainly of marine birds; gastropods act as first interme-
diate hosts, and crustaceans primarily as second intermediate
hosts (Deblock 1971; Yamaguti 1971, 1975). Three species of
the genus have been previously reported from Argentinean
waters, i.e., Maritrema bonaerensis Etchegoin et Martorelli,
1997 from Larus atlanticus Olrog, Larus maculipennis Licht-
enstein, and Larus dominicanus Lichtenstein; Maritrema
orensensis Cremonte et Martorelli, 1998 from L. dominicanus
and L. atlanticus; and Maritrema madrynensis Diaz et Cre-
monte, 2010 from L. dominicanus (Etchegoin and Martorelli
1997, Cremonte and Martorelli 1998, La Sala et al. 2009, Diaz
and Cremonte 2010).
As Maritrema is a neuter name (article 30.1.2 of the Inter-
national Code of Zoological Nomenclature; from Greek τρήμα,
neuter: a hole; type species: Maritrema gratiosum Nikoll, 1907),
the original spelling bonaerensis, orensensis, madrynensis, mi-
senensis, interrupta, patulus, minuta, jilenensis and kitanensis
must be corrected to bonaerense, orensense, madrynense,mise-
nense, interruptum, patulum, minutum, jilenense and kitanense
for gender agreement (article 34.2).
During surveys of helminth communities in birds from the
Argentinean Patagonian coast (Diaz and Cremonte 2010, Diaz
et al. 2011), two Maritrema species were found parasitizing
the intestine of the kelp gull, Larus dominicanus, M. madry-
nense and a new species which is described herein.
Materials and methods
Twenty nine kelp gulls, Larus dominicanus (Aves, Laridae),
were collected from March 2000 to April 2004, in Peninsula
Valdés and adjacent areas (24 adults from Fracasso Beach,
42°25´S, 64°07´W, San José Gulf, and 5 adults from Puerto
Madryn Beach, 42°47´S, 65°02´W, Nuevo Gulf) of Chubut
Province, Argentina. The birds were captured using a net,
killed with ether, and transferred as soon as possible to the lab-
oratory for dissection. The viscera were examined under a
stereomicroscope. Adult digeneans belonging to the genus
Maritrema were recovered from the intestine. The specimens
were fixed in 5% hot formalin, stored in 70% ethanol, stained
with Semichon’s acetocarmine, cleared in methyl salicylate,
mounted in Canada balsam, and studied using a light micro-
Illustrations were made with the aid of a drawing tube. Di-
mensions of mounted specimens are given in micrometers
with the mean value followed by the range in parentheses. The
forebody was measured from the anterior extremity to the an-
terior margin of ventral sucker. Some fixed adult specimens
were dehydrated, critical point dried, gold coated, and ob-
*Corresponding author: email@example.com
Julia I. Diaz et al.
served and photographed using a JEOL JSM 6360 LV (Jeol,
Tokyo, Japan) scanning electron microscope (SEM).
Maritrema formicae sp. nov. (Figs 1–6)
Diagnosis (measurements based on 14 stained specimens)
(Figs 1–6): Body “pyriform” (i.e. pointed at anterior extremity
and rounded posteriorly), 269 (230–350) long by 130 (102–
195) wide at ventral sucker level (Fig. 1). Spines transversally
arranged covering entire body surface (Figs 3–5). Body spines
multidentated, wider than longer (mean size 1.35 by 1.25), an-
terior spines compactly distributed (Figs 3–4). Oral sucker sub-
terminal, 32 (26–43) long by 32 (26–40) wide. Ventral sucker
28 (23–40) long by 29 (24–40) wide, located in the second third
of body. Forebody 135 (115–187) long. Sucker ratio (ventral
sucker/oral sucker width) 0.91 (0.82–1). Prepharynx 13 (6–20)
long. Pharynx 20 (17–28) long by 15 (13–18) wide. Oesopha-
gus 27 (20–35) long. Intestinal caeca reaching the middle of
ventral sucker. Testes postovarian, lateral, symmetrical, oval,
smooth or slightly lobed edges (Fig. 1). Right testis 36 (30–45)
long axis by 29 (23–40) short axis, left testis 36 (25–40) long
axis by 29 (25–35) short axis. Vasa differentia joining anterior
region of seminal vesicle. Cirrus sac shaped as inverted “J”,
102 (85–130) long by 23 (18–30) maximum width (Fig. 2); lo-
cated between intestinal caeca and ventral sucker; with a very
thin muscular wall. Cirrus sac enclosing oval seminal vesicle,
27 (20–45) long by 20 (17–25) wide; numerous prostatic cells
surrounding a curled ejaculatory duct, and a spinous cirrus(Fig.
2). Invaginated cirrus 41 (33–55) long. Cirrus spines irregu-
larly distributed, not covering entire cirrus, densely distributed
at base. Proximal cirrus-spines are rose-thorn shapedand larger
than distal ones (5.5–6.5 vs 3.0–4.0, respectively) (Figs 2, 6).
Ovary submedian, postacetabular, oval,slightly lobed, partially
displaced dextrally, covered by posterior border of ventral
sucker obliquely disposed, 42 (30–52) long axis by 28 (23–35)
wide (Fig. 2). Oviduct short. Seminal receptacle present.
Ootype and Mehlis’ gland situated immediately posterior to
ventral sucker. Laurer’s canal not observed. Metraterm with
thinmuscular diverticulated wall. Genital pore simple, slightly
differentiated, unarmed, located at left side of ventral sucker.
Uterus in hindbody, surrounding testes, from posterior border
of cirrus sac to end of body. Operculated eggs from 31 to ap-
proximately 100 in number, 16 (14–18) long by 8.5 (8–9)wide
(Fig. 1). Vitellarium with numerous small follicles forming 2
symmetrical ribbons, confluent posteriorly, enclosing uterus
and testes (Fig. 1). Excretory vesicle “Y” shaped.
Figs 1 and 2. Maritrema formicae sp. nov. 1. Naturally obtained adult, ventral view. 2. Genital system, ventral view. Abbreviations:
c, cirrus; cs, cirrus sac; cv, common vitelline duct; ed, ejaculatory duct; m, metraterm; o, ovary; pc, prostatic cells; sr, seminal receptacle;
sv, seminal vesicle; u, uterus; vs, ventral sucker. Scale bars = 100 µm (1), 50 µm (2)
Maritrema formicae sp. nov. from Patagonian coast
Type host: Larus dominicanus Lichtenstein (Aves, Laridae).
Type locality: Fracasso Beach (42°25´S, 64°07´W), Penín-
sula Valdés, Chubut Province, Argentina.
Site of infection: Small intestine.
Specimens deposited: Holotype N° 6501 and paratypes
N° 6502, voucher specimens N° 6503 at the Helminthological
Collection of Museo de La Plata (CHMLP), Museo de La
Plata, La Plata, and at the Parasitological Collection of the
Centro Nacional Patagónico (CNP-Par N°13), Puerto Madryn,
Etymology: The name of the new species is derived from
the Latin for ant, “formica,” as a tribute to “Hormiga”, the
nickname of our partner Miguel Angel Díaz (CENPAT-CON-
ICET), indefatigable worker and lover of the sea. The species
name is dedicated in his memory.
The new species can be included in the genus Maritrema
Nicoll, 1907 and in the subgenus M. (Maritrema) by the pres-
ence of postcaecal uterine coils, vitellarium in symmetrical
ribbons surrounding uterine coils and testes, a cirrus pouch
enclosing an invaginable cirrus like a finger of a glove turned
inside out, a simple, superficial, and unarmed genital pore, and
the absence of a spined acetabulo-atrial plate (Deblock 1971,
2008). The presence of a spinous cirrus enclosed in a cirrus
sac places the new species closest to the “eroliae complex”
proposed by Deblock and Canaris (1992), parasitizing mainly
Charadriiformes. Within this complex are grouped several
species, difficult to distinguish from each other, and very sim-
ilar to M. eroliae Yamaguti, 1939. At present, twelve Mari-
trema species are included in the “eroliae complex”. Deblock
and Canaris (1992) grouped the species related to this com-
plex into 3 subgroups according to body size, morphology of
the vitellarium, and geographical distribution, i.e., group A =
species smaller than 400 µm and with horseshoe-shaped vitel-
larium; group B = species larger than 600 µm and the vitel-
larium in a complete or subcomplete ring; and group C = some
species with intermediate features between A and B.
Following this grouping, and taking account that Mari-
trema formicae sp. nov. has a vitellarium in a complete ring
but they are smaller than 600 µm, it should be located near
to group C, which is comprised of Maritrema misenense
(Palombi, 1940), M. eroliae (sensu Deblock et Pearson, 1968),
Maritrema interruptum Oshmarin, 1970, Maritrema papil-
lorobusta Ke, 1976, and M. madrynense Diaz et Cremonte,
2010. In this group, only the smaller specimens of M. eroliae
Figs 3–6. Maritrema formicae sp. nov. 3–5. Body spines (SEM). 3. Preacetabular dorsal spines. 4. Postacetabular dorsal spines. 5. Posterior
spines, ventral view. 6. Details of cirrus spines (arrow) at LM. Scale bars = 10 µm (3), 5 µm (4), 30 µm (5), 20 µm (6)
Julia I. Diaz et al.
(sensu Deblock et Pearson, 1968) from Charadrius mongolus
from Australia measure less than 400 µm like the new species.
However, the Australian specimens were restudied and iden-
tified later as to Maritrema spinosulum Deblock et Canaris,
1996, a species that was described as having a horseshoe-
shaped vitellarium, and the cirrus covered by a continuous lin-
ing of uniform small spines (Deblock and Canaris 1992,
1996). In contrast, M. misenense from Southern Europe, M. in-
terruptum from Vietnam, M. papillorobusta from China, and
M. madrynense from Argentina, measured more than 400 µm
in length. In addition, M. interruptum has a horseshoe-shaped
vitellarium and M. papillorobusta has the cirrus totally cov-
ered by heterogeneous spines, and a horseshoe-shaped vitel-
larium. Also, the eggs of the new species are smaller than
those from M. papillorobusta (14–18 vs 25–28) (Prévot et al.
1976; Deblock and Canaris 1992, 1996; Diaz and Cremonte
2010). Maritrema misenense possesses the cirrus partially cov-
ered by spines like M. formicae sp. nov. (Prévot et al. 1976).
However, M. misenense, which was described based only on
experimental adults, has a horseshoe-shaped vitellarium and
the tip of cirrus is unarmed. Also, the new species has shorter
spines (5–6 vs 11) and smaller eggs (14–18 vs 19–22 long; 8–
9 vs 11–12.5 wide) than M. misenense.
On the other hand, taking into account the taxonomic dif-
ficulties arising from incomplete descriptions, poorly illus-
trated, and the lack of biological knowledge of species similar
to M. eroliae, Deblock and Canaris (1992) also considered
those species similar to M. eroliae in 5 groups of species
which are likely to be similar each other, in order to simplify
their study. Maritrema formicae sp. nov. is similar to some
species into “Group I or patulus” and “Group II or eroliae”.
However, all species in Group I have a horseshoe-shaped vitel-
larium and, with the exception of Maritrema patulum Coil,
1955, were found only in the Palearctic or Indomalaya Re-
gions. The new species has smaller eggs than Maritrema bor-
neonse Fischthal et Kuns, 1973 (14–18 vs 25–28). Moreover,
in some of the species included in these two groups, the pre-
cise morphology, size or distribution of the cirrus spines were
not described (i.e., Maritrema minutum Ke, 1976; Maritrema
jilenense Zhong, Ke-Feng et Min-Zen, 1988; Maritrema ero-
liae sensu Ogata, 1951) (Deblock and Canaris 1992, 1996).
Maritrema kitanense Shibue, 1953 and Maritrema magnicir-
rus Belopolskaia, 1952 were proposed as synonymies and/or
declared invalid (Deblock 1975), and other species where
restudied and found to have a smooth cirrus (i.e., M. patulum)
(Deblock and Canaris 1996). Other species including in these
groups I and II were considered and compared above (i.e.,
M. misenense, M. interruptum and M. papillorobusta).
Considering the valid species with a spinous cirrus and
vitellarium in a complete ring, only M. madrynense has a
Neotropical distribution (Diaz and Cremonte 2010). Mari-
trema formicae sp. nov. differs from M. madrynense in body
shape (pyriform vs linguiform), size (230–350 long by 102–
195 wide vs 400–690 long by 235–390 wide), cirrus size (33–
55 vs 100–150), patterns of distribution of cirrus spines
(partially vs totally covered), number of eggs (less to ~100 vs
more than four hundred), and egg size (14–18 long by 8–9 in
wide vs 18–23 long by 10–12). Size and shape of body spines
in the new species differ from those of M. madrynense; in
M. formicae sp. nov. they are smaller than in M. madrynense
(average of dorsal body spines: 1.35 by 1.25 vs 2.74 by 4.52).
Maritrema formicae sp. nov. and M. madrynense occur sym-
patrically in the same host species; however, differences be-
tween them are clear.
Many species of Maritrema have been reported parasitizing
avian hosts around the world (see Diaz and Cremonte 2010 and
references therein). In contrast, only a few species have been
reported in South American birds: Maritrema nicolli Travassos,
1920; Maritrema bravoae Caballero et Ibáñez, 1970;Maritrema
magdalenae Werding, 1973; M. bonaerense Etchegoin et Mar-
torelli, 1997; M. orensense and M. madrynense (see Deblock
1971; Caballero and Ibáñez 1970; Etchegoin and Martorelli
1997; Cremonte and Martorelli 1998; Diaz and Cremonte
2010). Maritrema spp. reported parasitizing birds of the genus
Larus in Argentina are M. bonaerense, M. orensense and
M.madrynense(Lunaschi et al. 2007, Diaz and Cremonte 2010,
Diaz et al. 2011). Only M. madrynense fits with the “eroliae
complex”. Adults of this last species parasitizedL.dominicanus
and the metacercaria was found in the crab Cyrtograpsus alti-
manus Rathburn (Grapsidae) at the same locality as the new
species (Diaz and Cremonte 2010, Diaz et al. 2011). Recently,
Gilardoni et al. (2011) described larval stages of two different
Maritrema species (i.e., Maritrema sp. 1 and Maritrema sp. 2)
in a survey of larval digeneans in the intertidal snails from the
northern Patagonian coast. Gilardoni et al. (2011) suggest that
sporocysts and cercariae of Maritremasp. 2 from the gastropod
Siphonaria lessoni (Blainville) probably correspond to M. ma-
drynense. Taking into account that only 2 adult Maritrema
species (i.e., M. madrynense and M. formicae sp. nov.) were
found in the study area, and also two different species were
identified as larval stages in the same area, it is probable that
Maritrema sp. 1 registered by Gilardoni et al. (2011) from
Crepipatella dilatata Lamarck, corresponds to M. formicae sp.
nov. Experimental and/or molecular analyses are needed to test
As was mentioned by Deblock and Canaris (1992, 1996)
and Diaz and Cremonte (2010) there are doubts regarding the
correct identification of specimens reported as M. eroliae by
Yamaguti (1939) and subsequent authors, as well as other re-
lated species, as a result of incomplete descriptions, non or
poorly illustrated specimens, and lack of knowledge about
the biology of the species. Additionally, there are many de-
scriptions and/or reports of metacercariae or immature spec-
imens. Maritrema formicae sp. nov. can be distinguished
from other species using a combination of features including
size, shape of vitellarium, size and pattern of distribution of
Maritrema formicae sp. nov. from Patagonian coast Download full-text
cirrus spines, number and size of eggs, and geographical
Acknowledgements. The authors gratefully thank Miguel Angel
Díaz and Ulyses Pardiñas for helping us in collecting the hosts, Maria
Cristina Estivariz for the drawings, and the staff of the Servicio de
Microscopía Electrónica de Barrido of the Museo de La Plata. We
specially thank Dr. Nestor Cazzaniga for his valuable collaboration
in the taxonomical review of Maritrema species and Dr. Mike Kin-
sella for the critical reading of the manuscript. Fieldwork was con-
ducted in a Protected Natural Area of Chubut Province with permits
from the Secretaría de Turismo y Áreas Protegidas. This study was
supported by ANPCyT (PICT01374), UNLP (N 628) and PIP CON-
ICET to F. Cremonte. Authors are members of CONICET.
Caballero C.E., Ibáñez H.N. 1970. Estudios helmintológicos de la
República de Perú. I. Dos especies de Trematoda de la fami-
lia Microphallidae Travassos, 1920 que parasitan Aves. An-
nales del Instituto de Biologia de la Universidad Nacional
Autónoma de Mexico, Serie Zoologie, 41, 29–38.
Cremonte F., Martorelli S.R. 1998. Description of a new species of
Maritrema (Digenea: Microphallidae) from Larus domini-
canus (Aves: Laridae) in Buenos Aires coast, Argentina. Folia
Parasitologica, 45, 230–232.
Deblock S. 1971. Contribution à l’étude des Microphallidae Travas-
sos, 1920. XXIV. Tentative de phylogénie et de taxonomic.
Bulletin du Museum Naturelle d’Histoire Naturelle, 3ème
Serie, Zoologie, 7, 353–468.
Deblock S. 1975. Contribution à l’étude des Microphallidae Travas-
sos, 1920 (Trematoda) XXX. A propos d’espèces décrites –
au Japon par S. Yamaguti C. – Maritrema eroliae et le genre
Pseudospelotrema. Annales de Parasitologie Humaine et
Comparée, 50, 45– 54.
Deblock S. 2008. Family Microphallidae Ward, 1901. In: (Eds. R.A.
Bray, D.I. Gibson and A. Jones) Keys to the Trematoda. Vol.
3. CABI Publishing, Wallingford, U.K., 451–495.
Deblock S., Canaris A.G. 1992. Contribution à l’étude des Micro-
phallidae Travassos, 1920 (Trematoda). XLIII- De six espèces
(Accepted February 23, 2012)
d’Afrique du sud dont une d’un genere nouveau. Annales de
Parasitologie Humaine et Comparée, 67, 204–218.
Deblock S., Canaris A.G. 1996. Microphallidae, Trematoda: XLVIII.
Quatre Maritrema du grupe Eroliae parasites d’Oiseaux aus-
traliens. Parasite, 4, 357–361.
Diaz J.I., Cremonte F. 2010. Development from metacercaria to adult
of a new species of Maritrema (Digenea: Microphallidae) par-
asitic in Kelp Gull, Larus dominicanus, from Patagonian
coast, Argentina. Journal of Parasitology, 96, 740–745. DOI:
Diaz J.I., Cremonte F., Navone G.T. 2011. Helminths of the Kelp
Gull, Larus dominicanus, from the northern coast of Patago-
nia and their relationships with diet and behaviour of the host.
Parasitology Research, 109, 1555–1563. DOI:10.1007/s004
Etchegoin J.A., Martorelli S.R. 1997. Description of a new species of
Maritrema (Digenea: Microphallidae) from Mar Chiquita
coastal lagoon (Buenos Aires, Argentina) with notes on its life
cycle. Journal of Parasitology, 83, 709–713. DOI: 10.2307/
Gilardoni C., Etchegoin J.A., Diaz J.I., Iturate C., Cremonte F. 2011.
A survey of larval digeneans in the commonest intertidal
snails from northern Patagonian coast, Argentina. Acta Para-
sitologica, 56, 163–179. DOI: 10.2478/s11686-011-0021-2.
La Sala L., Martorelli S.R., Alda P., Marcotegui P. 2009. Some dige-
neans from Olrog’s Gull Larus atlanticus Olrog, 1958 (Aves:
Laridae) from the Bahía Blanca Estuary, Argentina. Compa-
rative Parasitology, 76, 113–116. DOI: 10.1654/4389.1.
Lunaschi L.I., Cremonte F., Drago F.B. 2007. Checklist of digenean
parasites of birds from Argentina. Zootaxa, 1403, 1–36.
Prévot G., Bartoli P., Deblock S. 1976. Cycle biologique de Mari-
trema misenensis (A. Palombi, 1940) n. comb. (Trematoda
Microphallidae Travassos, 1920) du midi de la France. An-
nales de Parasitologie Humaine et Comparée, 51, 433–446.
Yamaguti S. 1939. Studies on the helminth fauna of Japan. Part 25.
Trematodes of birds. IV. Japanese Journal of Zoology, 8, 129–
Yamaguti S. 1971. Synopsis of digenetic trematodes of vertebrates.
1st Ed. Keigaku Publishing Co., Tokyo, Japan, 1074 pp.
Yamaguti S. 1975. A synoptical review of the life history of digenetic
trematodes of vertebrates, with a special reference to the mor-
phology of their larval forms. Keigaku Publishing Co., Tokyo,
Japan, 590 pp.