ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
Volume 13, Nu mber 2 (j ul - dec 2019) Lima - Perú
Órgano ofici al de la Asoc iación Peru ana de Helmi ntologí a e Inve rtebra dos Afines (APHIA)
Neotropical Helminthology
245
Neotropical Helminthology, 2019, 13(2), jul-dic:245-252.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
DIOECOCESTUS PARONAI FUHRMANN, 1900 (CESTODA, CYCLOPHYLLIDEA) PARASITE OF
THE WHITE-TUFTED GREBE ROLLANDIA ROLLAND (QUOY AND GAIMARD,
1824)(PODICIPEDIFORMES) AND A REVIEW OF THE HOST SPECIFICITY IN DIOECOCESTIDAE
DIOECOCESTUS PARONAI FUHRMANN, 1900 (CESTODA, CYCLOPHYLLIDEA) PARÁSITO DEL
MACÁ COMÚN ROLLANDIA ROLLAND (QUOY AND GAIMARD, 1824)(PODICIPEDIFORMES) Y
REVISIÓN DE LA ESPECIFICIDAD HOSPEDATORIA EN DIOECOCESTIDAE
Ruben Daniel Tanzola1; Silvia Elizabeth Guagliardo1 & Graciela Gigola2
1Laboratorio de Parasitología 2 Cátedra de Anatomohistología - Dep. Biología, Bioquímica y Farmacia, Universidad
Nacional del Sur, San Juan 670 (8000) Bahía Blanca, Argentina.INBIOSUR/CONICET.
*Corresponding author: rtanzola@uns.edu.ar
ABSTRACT
The family Dioecocestidae Southwell, 1930 largely confined to grebes, has a confounding and poorly
known systematic composition. Most of its members are known only from their original descriptions and
were not studied since then. Based in two tapeworms with completely separate sexes, Dioecocestus
paronai Fuhrmann, 1900 was primarily consigned to Plegadis guarauna (Linnaeus 1766) as the natural
host and Buenos Aires, Argentina, as the type locality. In the present study specimens of D. paronai are
described, data on its biology and host distribution are provided. There were no significant differences in
the prevalences of males and females infesting grebes. Nor in the abundances between host sexes. The
variance/mean ratio was 0.426 and the parameter of contagion K= ─0.36, showing an underdispersed
pattern of distribution. Following its original description, not only was P. guarauna never cited again as
host of this tapeworm but the remaining six species of the genus Dioecocestus Fuhrmann, 1900 are grebe
specialists in the five continents and D. paronai was nevermore found from ibises. The white-tufted grebe
Rollandia rolland (Quoy & Gaimard, 1824) is rectified as the natural host and it is confirmed the marked
specificity of the family Dioecocestidae in grebes.
Keywords: Cestoda – Dioecocestus – Podicipediformes – Rollandia rolland
Versión Impresa: ISSN 2218-6425
Versión Electró nica: ISSN 1995 -1043
Neotropical Helminthology, 2019, 13(2), jul-dic
246
RESUMEN
La composición sistemática de la familia Dioecocestidae Southwell, 1930 ampliamente confinada a los
macáes o zampullines, es confusa y muy pobremente conocida. La mayoría de sus integrantes se conocen
solo a partir de sus descripciones originales y varias no han sido vueltas a estudiar. Dioecocestus paronai
Fuhrmann, 1900 descripta sobre la base de dos individuos con sexos completamente separados, fue
primariamente asignada a Plegadis guarauna (Linnaeus, 1766) como hospedador natural y tuvo a Buenos
Aires, Argentina como su localidad típica. En el presente estudio se describen, se aportan datos acerca de
su biología y distribución en el hospedador de especímenes adultos de D. paronai. No se hallaron
diferencias estadísticamente significativas en cuanto a la prevalencia entre sexos de los hospedadores
como tampoco entre las abundancias parasitarias. El coeficiente de dispersión varianza/media fue de
0.426 y el parámetro de contagio K= ─0.36, ambos revelaron un patrón de distribución subdisperso o
regular en la población de hospedadores. Desde su descripción original, P. guarauna nunca más fue citado
como hospedador de esta especie, además las restantes seis especies del género Dioecocestus son todas
especialistas de macáes en los cinco continentes y D. paronai nunca más fue hallado en ibises. En el
presente trabajo se rectifica al macá común Rollandia rolland (Quoy & Gaimard, 1824) como el
hospedador natural de la especie y se confirma la marcada especificidad de grupo de la familia
Dioecocestidae en macáes.
Palabras clave: Cestoda – Dioecocestus – Podicipediformes – Rollandia rolland
INTRODUCTION dioecocestids as well as aspects of the co-evolution
between cestodes and grebes. The aim of the
present study is to describe the tapeworms
Storer (2000), in his monograph on the fauna of
metazoan parasites of grebes emphasizes, among
other concepts, that the cestodes dominate the
fauna of intestinal helminths. Also, the family
Dioecocestidae Southwell, 1930 largely confined
to grebes, has a poorly known systematic
recorded from Rollandia rolland (Quoy &
Gaimard, 1824) to provide data on its biology and
host distribution and to evaluate its host specificity.
MATERIAL AND METHODS
composition. In fact, in the Storer's systematic list
of cestodes parasitizing grebes, Dioecocestus
paronai described by Fuhrmann (1900) is not
considered. Parona, who worked at Genoa, had
received from the National Museum of Buenos
Aires, two specimens of an unknown tapeworm,
apparently parasiting a white-faced ibis, Plegadis
guarauna (Linnaeus, 1766) (Ciconiiformes,
Threskiornithidae) and he forwarded them to Otto
Fuhrmann, in Neuchatel, for identification. Based
on the novel finding of the complete separation of
sexes in a tapeworm, Fuhrman proposed the genus
Dioecocestus with paronai as type species,
consigning P. guarauna as the natural host and
Buenos Aires, Argentina, as the type locality. From
its original description, not only the species was
never cited again but the remaining six species of
the genus Dioecocestus are grebe specialists in the
five continents. This fact has a significant influence
in assessing both the host specificity of the
The helminths compose a collection made in
wetlands from Buenos Aires province between
1983-2018: Chascomús lagoon (LCH) 35°35'29" S
58°01'28" W), Mar Chiquita lagoon (AMCH)
(37°46' S and 57°27' W), Villa Arias (38°52'00” S
62°05'00” W) and Los Talas ponds (LT) (34°55'44"
S and 57°43'04" W). The sample of hosts consisted
of 40 R. rolland (19 females, 19 males and 2
indeterminate). The tapeworms were preserved in
10% formalin and stained with Langeron´s
hydrochloric carmine. The identification was made
by morphology and morphometry. The
measurements are given in μm unless otherwise
indicated. For microanatomy studies, the worms
were fixed in buffered formalin, dehydrated in
ethilic alcohols, embedded in paraffin, sectioned at
5-7 μm thick and colored with hematoxylin and
Neotropical Helminthology, 2019, 13(2), jul-dic
Dioecocestus paronai parasite of Rollandia rolland
247
eosin. Microphotographs were taken with a Motic
BA 200 optical microscope. Voucher material was
deposited in the Helminthological Collection of the
Museum of La Plata (Argentina). The
variance/mean ratio (coefficient of dispersion) and
the contagion parameter, K, were determined to
assess the distribution patterns at the level of
infrapopulations. The parasitological indexes
follow Bush et al. (1997). The mean abundances
and prevalences were compared according to the
sex of the hosts using the Mann-Whitney U test,
(IBM SPSS version 23), and the Z statistic
(Morales & Pino, 1987), respectively. The level of
significance used was α= 0.05.
Ethic Aspects
Corresponding scientific hunting permits were
obtained from the Faune Direction of the
Agricultural Ministry, Buenos Aires province,
Argentina.
RESULTS
possible to quantify the number of testes. Two vas
deferens run as rectilinear conduits, from the
gonadal mass towards both margins of the
segment, passing between the excretory vessels
(Fig. 3). After enter the robust cirrus sac, they
expand to give rise an internal seminal vesicle. The
cirrus sac with strong muscular walls measures 180
in length in the middle zone of the strobila and
reaches 520 in the last proglottids. This observation
is highlighted since the testes quickly deplete their
gametes, then become rudimentary and disappear
completely from the parenchyma in the posterior
strobila. However, both the segment as a whole and
the cirrus sac, continue growing with uncertain
functional explanation (Fig. 4). The cirrus is robust
and is completely covered by spines "L" shaped
with a sharp and retrograde tooth (Figs. 5ab).
On the other hand, the female strobila has a bilobed
ovary central and dorsal to a compact vitelline
gland (Fig. 6). The vagina is a blind straight tube
that runs towards the margin. As a taxonomical
feature in dioecocestids, the vagina ends blind near
the margin and alternating irregularly along the
strobila. The gravid multilobed uterus (Fig. 7) fills
Description (based on 1 male and 1 female, fixed
and stained). The species presents the sexes
completely separated. The male has a total length
of 110 mm and a maximum width of 2.60 mm,
while the female reaches 140 mm long and 3.86
mm wide. The scolex is rudimentary, in the form of
a low anterior prominence, 450 wide, 160 long and
100 thick, probably not functional as a fixation
organ. Four primordia of circular suckers 45 in
diameter with a slender orbicular musculature and
narrow frontal medial sulcus (Fig. 1). There are
neither rostellum nor hooks. The strobila consists
of a long chain of craspedote proglottids, with a
region of maturity occupying approximately the
anterior third of the strobila, whose proglottid are
wider than long (80 x 1280 at 1 mm from the
the medulla and compresses both bands of
longitudinal musculature towards the margins,
exceeding the osmoregulatory vessels.
Embryonated eggs measure 56 x 48, have a thin
vitelline membrane and a thin embryophore that
protects a subsferic oncosphere of 32 x 24, with
three pairs of embryonic hooks of 16 in length (Fig.
8).
Taxonomic summary
Dioecocestus paronai Furhmann, 1900
(Cyclophyllidea, Dioecocestidae)
Host: Rollandia rolland (Quoy & Gaimard, 1824)
(Podicipediformes)
Location: Small intestine
Geographic localization: Several ponds and
scolex, 384 x 2440 at 8 mm from the scolex). lagoons from Buenos Aires province (Argentina)
Towards the posterior end the morphology of the
segments changes becoming longer and of
approximately quadrangular (2200 x 2600). The
male strobila presents a set of duplicated gonads in
an anterior transverse field of the medullary
parenchyma (Fig. 2). Numerous ovoid testes of 48
x 32 cluster between the longitudinal excretory
vessels. They do not form lateral fields, as in other
Dioecocestus spp., but form a single stratum that
runs posteriorly and dorsoventrally. It was not
Voucher material: One male, mounted and stained,
accession number = MLP-He 7567 (MLP
helminthological collection)
Prevalence= 82.5% (33/40) (males= 89%;
females= 79%)
Mean abundance= 1.15
Mean intensity= 1.39
Distribution on hosts: Thirteen of the birds (32,5%)
hosted a pair of adults, a male and a female in each
Neotropical Helminthology, 2019, 13(2), jul-dic
248
intestine, but the remaining, from 20 birds, were in
postmortem degradation. The worms occupied
75% of the lumen of the small intestine. The
variance/mean ratio was 0.426 and the parameter
of contagion K= ─0.36. No juvenile form or larval
stages assignable to Dioecocestus Fuhrmann, 1900
were found. In respect to the parasitological
indexes in our sample, there were not significative
differences in the prevalences of males and females
of grebes (Z= 0.588 p> 0.05). Nor in the
abundances between sexes (U Mann-Whitney=
144.00 p> 0.05).
Figures 1-5. 1. Dioecocestus paronai Fuhrmann, 1900 (in toto). Anterior end showing the rudimentary scolex and suckers. Scale-
bar= 0.1 mm. 2. Male strobila (in toto). Scale-bar= 1 mm. 3. Male genitalia terminal (detail from histological section).
Abbreviations: BC= cirrus pouch, CD= deferent duct, CEd= dorsal excretory vessel, CEv= central excretory vessel, CNP=
principal nervus chord. Scale-bar= 0.1 mm. 4. Sterile proglottid from the posterior end (in toto). Scale-bar= 1 mm. 5a. Cirrus
pouch (detail from histological section). Abbreviations: C= cirrus, MB= muscular wall of the pouch, VSi= internal seminal
vesicule. Scale-bar= 0.1 mm. 5b. tegumentary spine of the cirrus. Scale-bar= 0.01 mm.
Neotropical Helminthology, 2019, 13(2), jul-dic
Dioecocestus paronai parasite of Rollandia rolland
249
Figures 6-8. 6. Female strobila (in toto). Scale-bar= 1 mm. 7. Gravid segment (detail from histological section). Abbreviations:
H= egg, On= oncosphere, U= uterus. Scale-bar= 0.1 mm. 8. Mature egg (in toto). Abbreviations: Ef= embryophore, ME= outer
envelope, MI= inner envelope, ON= oncosphere. Scale-bar= 0.01 mm.
DISCUSSION sexes in different strobilae, although unlike the
former, they have scolex with a rostellum armed
with 30 hooks, elliptical and more voluminous
Based in two tapeworms with completely separate
sexes, Fuhrmann (1900) described D. paronai.
These worms apparently had been collected in a
white-faced ibis, P. guarauna (sic) in Buenos
Aires, Argentina. It was considered a type of a
genus, so far unknown, whose most significant
feature was the dioecy. The same year, Fuhrmann,
studied a sample of eleven tapeworms from
Podiceps collaris (sic) and Podiceps grisegena
(Boddaert, 1783) from collections of Mehlis,
Krabbe, Muller and Rudolphi, which were
designated as Taenia aspera Mehlis, 1831 and T.
lanceolata Rudolphi, 1805. Like D. paronai, these
cestodes had the peculiarity of having separate
cirrus sac, a discoidal vitelline gland and larger
eggs. Based in these differences, Fuhrmann
proposed to meet them in a new taxon nominated
Dioecocestus asper (Mehlis, 1831). Later, they
were successively described D. acotylus
Fuhrmann, 1904 in the least grebe, Tachybaptus
dominicus (Linnaeus, 1766) from South Texas,
Jamaica, Cuba, Haiti and North of Brazil, D.
novaeguineae Fuhrmann, 1914, in the Australian
little grebe, T. novaehollandiae and T. ruficollis in
New Guinea, D. fuhrmanni Linton, 1925 in the red-
necked grebe P. grisegena and P. auritus
(Linnaeus, 1758) in Alaska and Yakutia, D. fevita
Meggitt, 1933 in T. ruficollis in India and D. cablei
Neotropical Helminthology, 2019, 13(2), jul-dic
250
(Siddiqi, 1960) in the same host and site. Also,
Furhmann (1909) renamed D. novaehollandiae
(Krefft, 1871) in the little grebe T. ruficollis (Pallas,
1764) from Australia. But Ryzhikov & Tolkacheva
(1981) synonymized D. novaehollandiae with D.
asper. So, the six species cited above have the
particularity that all of them are specialists in
grebes, and four of them were described in the same
host, T. ruficollis. This situation carries to a poor
known and confounding systematic status in the
family Dioecocestidae. Storer (2000) stated that
the Australian material needs checking. Fuhrmann
(1907) ranked all dioecious species in a new
family, Acoleinidae, whose type genus, Acoleus
Fuhrmann, 1899, shared with Dioecocestus some
features of interest, especially the absence of
external vaginal opening, arrangement of the
testicular mass, two layers of parenchymatic
muscular bands and the shape of the uterus.
Ransom (1909) amended the name of the family in
question as Acoleidae which brought together the
genera Acoleus Fuhrmann, 1899, Gyrocoelia
Fuhrmann, 1899, Dioecocestus Fuhrmann, 1900,
Diplophallus Fuhrmann, 1900 and Shipleya
Fuhrmann, 1908. Later, Southwell (1930)
relocated Dioecocestus, Shipleya and Gyrocoelia
into a new family, Dioecocestidae. Yamaguti
(1959) recognized the subfamily Gyrocoeliinae for
the genera Gyrocoelia, Shipleya and Infula Burt,
1939 and Tolkacheva (1979) raised the group to the
family level, Gyrocoeliidae.
From its original description by Fuhrmann (1900),
D. paronai was nevermore found from ibises. The
present authors looked for helminths in two species
of ibises from wetlands of Buenos Aires province
(MCH, LT and CH), the white-faced ibis Plegadis
chihi (Vieillot 1817)(n= 5) and the bared-faced
ibis Phimosus infuscatus (Lichtenstein, 1823) (n=
2) but did not found any species of tapeworms.
Digiani (2000) examined the digenean and cestode
fauna of P. chihi (n= 64) from several wetlands at
Buenos Aires province and recorded by the first
time Hymenolepis megalops (Nitzch in Creplin,
1829) (Cestoda, Hymenolepididae)(10.7%
prevalence). Georgiev and Vaucher (2000)
described Chimaerula bonai ( Cestoda,
Dilepididae) based on four specimens of Ph.
infuscatus from Paraguay (100% prevalence).
Martínez-Haro et al. (2012) recorded one
individual of Cyclustera ralli (Underwood et
Dronen, 1986) Bona 1994 (Cestoda, Dilepididae)
in one P. chihi from the state of Mexico. Scheer et
al. (2019) examined the helminth assemblages of
Ph. infuscatus from Southern Brazil, from twenty-
eight birds and cited the presence of
Megalacanthus sp. (Cestoda, Dilepididae)
(89.28% prevalence). None of the mentioned
authors recorded D. paronai in ibises. This fact,
along to the present finding in 32 of 38 R. rolland
(82.5% prevalence) suggest that the white-tufted
grebe is the natural host in Argentina. Storer (2000,
p. 20) emphasized that D. paronai represents an
exception in the host specificity of the members of
Dioecocestidae as specialists of grebes. The
present finding confirm that all dioecocestids are
grebe specialists. Moreover, based on criteria about
the levels of host specificity proposed by Palm &
Caira (2008), D. paronai would be a oioxenous
species, showing a high degree of specificity.
Fuhrmann supossed that the scolex unfortunately
was degraded in both of the worms he examined
(p.50: “Der Scolex war bei beiden Exemplaren
leider abgerissen”). Ryzhikov & Tolkacheva
(1978) on the basis of the scolex morphology
divided the genus Dioecocestus into four groups
and considered D. paronai belonging to the third
one: “scolex without rostellum or suckers”. Our
observations shown that really D. paronai has four
rudimentary suckers and so, it should be grouped
into the fourth morphological group: “scolex with
suckers but no rostellum”, along D. cablei from T.
ruficollis in India.
Few measurements were recorded in Furhmann´s
original description. The tapeworms of R. rolland
were larger than the Fuhrmann's specimens (110
mm vs 70mm –males- and 140mm vs 60 mm
–females-) . However the worms described here
agree in general terms with the original description.
The presence of a rudimentary scolex without
rostellum and hooks, arrangement of the testes into
a central mass, not divided in two fields, absence of
vagina opening, inner muscle bundles well
developed in two longitudinal layers, the structure
of the cirrus sac and the cirrus are similiar in our
material, all these features allow us to confirm the
specific status.
In respect to the distribution of D. paronai within
the host population, both the coefficient of
dispersion and the contagion parameter showed a
regular or underdispersed pattern (Morales & Pino,
Neotropical Helminthology, 2019, 13(2), jul-dic
Dioecocestus paronai parasite of Rollandia rolland
251
1987). Underdispersed frecuency distributions are
uncommon among helminth parasites (Esch &
Fernandez, 2013). Have been proposed four
possible causes to explain this fenomenon. Among
them it could be that parasite recruitment rates are
equal to death rates. As we pointed above, several
tapeworms were retained in postmortem condition
suggesting that the worms died and degraded into
the gut. Here, both the immune response of the
grebes and strong intraspecific competition
between worms may occur to prevent further
infections.
The present study reports the parasitism of D.
paronai in R. rolland by the first time and confirm
the host specificity of all members in
Dioecocestidae by grebes.
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