Neotrop. Helminthol., 8(2), 2014
2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
CYSTACANTHS OF GIGANTORHYNCHUS ECHINODISCUS (ACANTHOCEPHALA,
GIGANTORHYNCHIDAE), IN NEOTROPICAL TERMITES (ISOPTERA, TERMITIDAE)
CISTACANTOS DE GIGANTORHYNCHUS ECHINODISCUS (ACANTHOCEPHALA,
GIGANTORHYNCHIDAE), EN TERMITAS NEOTROPICALES (ISOPTERA, TERMITIDAE)
1 2 2 2
José F. R. Amato , Eliana M. Cancello , Maurício M. Rocha & Tiago F. Carrijo
Abstract
Keywords: Anteaters - Cornitermes - Gigantorhynchus lutzi - intermediate hosts - life cycles - Labiotermes - morphology
alteration - Orthognathotermes.
Suggested citation Amato, JFR, Cancello, EM, Rocha, MM & Carrijo, TF. 2014. Cystacanths of Gigantorhynchus echinodiscus
(Acanthocephala, Gigantorhynchidae), in Neotropical termites (Isoptera, Termitidae). Neotropical Helminthology, vol. 8, n°2,
jul-dec, pp. 325-338.
1Laboratório de Helmintologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul. Caixa Postal
15.014, 91501-970 Porto Alegre, Rio Grande do Sul, Brasil. Current address: Rua Cabral, 875 apt. 301, Bairro Rio Branco, 90420-121, Porto
Alegre, RS, Brasil. E-mail: josefelipeamato@gmail.com
2Museu de Zoologia da Universidade de São Paulo, Caixa Postal 42.494, 04218-970 São Paulo, SP, Brasil. E-mails: mrocha@usp.br,
ecancell@usp.br
Specimens of Labiotermes emersoni (Araujo, 1954) and Orthognathotermes heberi Raw & Egler,
1985, were collected at Parque Nacional da Serra da Canastra, State of Minas Gerais, Brazil.
Soldiers of the two species were suspected to carry larval acanthocephalan parasites due to
different sizes and shape of their heads and because some specimens had a conspicuous,
cylindrical, whitish 'body' in the hemocoel, around the digestive tract in the abdomen. The
termites showed shape alteration and light pigmentation dystrophy of the heads induced by the
larval acanthocephalans. These alterations were documented photographically and the
cystacanths described. The encysted juveniles removed from the hemocoel of infected soldier
termites and processed accordingly, were determined as Gigantorhynchus echinodiscus (Diesing,
1851). The proboscis had the typical cylindrical shape and the characteristic two distal circles of
large hooks (6+12), covered with small, almost rootless spines, and a very short neck. This is the
first record from Brazil of any species of termites infected with acanthocephalans of the genus
Gigantorhynchus Hamann, 1892 and the first record of G. echinodiscus cystacanths infecting the
intermediate host.
325
326
Resumen
Palabras clave: oso-hormiguero – Cornitermes – Gigantorhynchus lutzi – hospedero intermediário – ciclos de vida – Labiotermes –
alteración morfológica – Orthognathotermes.
Los especímenes de Labiotermes emersoni (Araujo, 1954) y Orthognathotermes heberi Raw &
Egler, 1985, se colectaron en el Parque Nacional de Serra da Canastra, Estado de Minas Gerais,
Brasil. Se sospechaba que soldados de las dos especies eran portadores de larvas de acantocéfalos
parásitos debido a diferentes tamaños y formas de la cabeza, además de un “cuerpo” blanquecino,
cilíndrico visible en el hemocele de algunos ejemplares, alrededor del tubo digestivo en el
abdomen. Los termitas mostraron alteración de forma y leve distrofia de pigmentación en sus
cabezas inducidas por los acantocéfalos larvales. Estas alteraciones se documentaron
fotográficamente y se describen los cistacantos. Las formas juveniles enquistadas retiradas del
hemocele de soldados infectados se identificaron como Gigantorhynchus echinodiscus (Diesing,
1851). Los probóscides tenían la típica forma cilíndrica y los característicos dos círculos distales
de grandes ganchos (6+12), cubiertos de pequenas espinas, casi sin raíces y un cuello muy corto.
Este es el primer registro de dos especies de termitas infectadas por acantocéfalos del género
Gigantorhynchus Hamann, 1892 y el primero registro de cistacantos de G. echinodiscus
infectando el hospedero intermediário,
INTRODUCTION studies about the effects of these helminths on
them.
Acanthocephalus aenigma Reichensperger,
1922, was described as a new species from the
hemocoel of specimens of two termite species
from the locality of Encano Alto, State of Santa
Catarina, southern Brazil (Reichensperger
1922), while Smales (1997) made a suggestion
that termites were the intermediate hosts for
Multisentis myrmecobius Smales, 1997, because
the type host, Myrmecobius fasciatus
Waterhouse, 1836, a marsupial anteater from
Australia, feeds mainly on them.
The Caribbean termite, Nasutitermes acajutlae
(Holmgren, 1910), has been the subject of
acanthocephalan (Oligacanthorhynchidae)
parasitism studies (behavior, color and shape
changes, and predation risk) (Fuller et al., 2003)
and its implications for reproductive success
(Fuller & Jeyasingh, 2004), in the U. S. Virgin
Islands. Later, Nickol et al. (2006) described the
cystacanths obtained from worker hemocoels of
N. acajutlae, subcutaneous tissues of lizards,
greater omentum of mongooses, and
mesenteries of birds from these Caribbean
islands, identifying them as Oncicola
venezuelensis Marteau, 1977. Later yet, Fuller &
Pigmentation alteration induced by larval
acanthocephalans, known as “color
dichromatism”, “depigmentation”, “non-
pigmentation”, or more properly, “pigmentation
dystrophy”, as suggested by Oetinger & Nickol
(1981), is an uncommon phenomenon. It has
been documented for North America in species
of the aquatic isopod genus Asellus Geoffroy,
1764 (Seidenberg, 1973, Camp & Huizinga,
1979, Oetinger & Nickol, 1981, 1982). The same
phenomenon was recorded for the first time in
Brazil by Amato et al. (2003), in the terrestrial
isopod genus Atlantoscia (van Name, 1940).
Termites seldom have been confirmed as
intermediate hosts for acanthocephalans, much
less were recorded with morphological and/or
behavioral alterations induced by these
parasites. Until recently, there have been only
two instances in which these isopterans have
b e e n a s s o c i a t e d i n d i r e c t l y w i t h
acanthocephalans (Reichensperger, 1922;
Smales, 1997) and only one in which these
insects have been proved to be the real
intermediate hosts and the subject of serious
Amatoet al.
Cystacanths of Gigantorhynchus in Neotropical termites
Neotrop. Helminthol., 8(2), 2014
Nickol (2011) described mature specimens of O.
venezuelensis from a road-killed feral house cat
found dead in the islands.
Adults of two of the six species of
Gigantorhynchus Hamann, 1892, considered
valid by Yamaguti (1963) and Amin [in
Crompton & Nickol (1985)] have been
collected by several authors (Table I) from their
final hosts in several regions of Brazil: 1.
Gigantorhynchus echinodiscus (Diesing, 1851)
from the giant anteater ('tamanduá-bandeira')
Myrmecophaga tridactyla Linnaeus, 1758,
commonly known in Brazil as: 'iurumi',
'jurumim', 'tamanduá-açú', 'tamanduá-cavalo',
'papa-formigas-gigante', and 'urso-formigueiro-
gigante', and Tamandua tetradactyla (Linnaeus,
1766), known as 'tamanduá-mirim'; and 2.
Gigantorhynchus lutzi Machado Filho, 1941,
from the didelphid marsupial Caluromys
philander Linnaeus, 1758, commonly known in
Brazil as 'cuíca' or 'bare-tailed woolly opossum'
in the United States (Machado Filho, 1941).
In Brazil, eggs attributed to G. echinodiscus
have been recorded in coprolites from
archaeological sites (Ferreira et al., 1989) and
the first notice about the modification of
morphology of termite soldiers by
acanthocephalans was made by Cancello
(1991).
The present paper describes the cystacanths
found in the hemocoels of soldiers of
Labiotermes emersoni (Araujo, 1954) (Figs 1
and 2) and Orthognathotermes heberi Raw &
Egler, 1985, and documents photographically,
the phenomena of shape alteration and
pigmentation dystrophy induced by larval
acanthocephalans in termites from Parque
Nacional da Serra da Canastra (P. N. Serra da
Canastra), State of Minas Gerais, Brazil, as
intermediate hosts for G. echinodiscus.
The colony of L. emersoni was sampled in an
abandoned nest of Cornitermes cumulans
(Figs 1 and 2), while the (Kollar in Pohl, 1832)
colony of O. heberi was found in a nearby area,
in its own nest. All soldier samples from the
Labiotermes colony were infected by
a c a n t h o c e p h a l a n s , w h i l e i n t h e
Orthognathotermes colony a fewer proportion
of the soldiers had a cystacanth. The termite
samples were obtained by authorized personnel,
following the Brazilian policies and guidelines
to be applied to the collection of invertebrates.
The infected individuals showed heads with
strong shape and size alteration, as well as a
whitish abdomen, perceptible to the naked eye.
Termites, together with chunks of the nests, were
collected at the P. N. Serra da Canastra (-20.249
S, -46.563 W), State of Minas Gerais, Brazil and
transported to the Laboratory of Isoptera, Museu
de Zoologia, Universidade de São Paulo
(MZUSP). Cystacanths were removed from the
abdomen of termites and released from their
envelopes and kept in distilled water to die and
evaginate the proboscis. Immediately, helminths
were fixed in A. F. A. (Ethanol, Formalin,
Glacial Acetic Acid) and later stained in
Delafield´s hematoxylin (Amato & Amato,
2010). Two specimens were processed for
Scanning Electron Microscopy (SEM) at the
'Centro de Microscopia Eletrônica (CME) –
Universidade Federal do Rio Grande do Sul -
UFRGS'. Measurements are in micrometers,
unless otherwise indicated; widths were
measured at the widest point. Proboscis hooks
from the first two circles were measured in full
profile, lengths are the straight-line between the
tip of the hook to the junction with the root;
lateral hook-like spines were measured to the
tallest point; ranges are followed by the mean in
parentheses. Voucher specimens were deposited
in the 'Coleção Helmintológica do Instituto
Oswaldo Cruz', Rio de Janeiro, RJ, Brazil
(CHIOC Catalog Nº: 37956a-o) and 'Coleção de
Invertebrados do Museu de Zoologia'
Universidade de São Paulo, SP, Brazil (MZUSP
Catalog Nº - 21.965).
Gigantorhynchus echinodiscus (Diesing, 1851)
(Figs 5 - 16)
Cystacanths from termite intermediary host.
MATERIAL AND METHODS RESULTS
327
Amatoet al.
Cystacanths of Gigantorhynchus in Neotropical termites
Description. Based on 35 specimens (17 males
and 18 females) mounted in Canada balsam and
2 specimens mounted on stubs for SEM. Trunk
widest at middle of anterior half (Fig. 5), 2.20
mm–2.94 mm (2.58 mm) long by 515–686 (596)
wide. Proboscis cylindrical (Figs 5 and 6, and
11), 784–955 (822) long by 368–686 (471) wide;
first distal circle of 6 hooks (Figs 7 and 9 -
arrows), largest, robust, 51–83 (66) long; second
distal circle of 12 hooks (Figs 7 and 9 - asterisks),
smaller than those in first circular row, 24–39
(36) long, arranged in pairs among the 6 hooks of
Figures 1-2. Nests of Cornitermes cumulans, re-colonized by Labiotermes emersoni. 1. Medium size (stage 2), entire nest,
external wall (ew). 2. Vertical section of the nest galleries (g), hive (h), pillars (p), soil (s). Figures 3-4. Orthognathotermes
heberi. 3. uninfected specimen, bar = 1 mm; and 4. infected specimen, with cystacanth of Gigantorhynchus echinodiscus
(arrow - c), bar = 1 mm.
328
Neotrop. Helminthol., 8(2), 2014
the first distal circle, roots appearing bifid from
front view (Fig. 14 - br); both rows separated by
a slight depression space (Figs 6 and 8 - s) from
the 28 longitudinal rows of almost rootless
spines, each longitudinal row with 11–13 spines;
each spine 24–31 (25) long. Neck quite short
(Fig. 6 - n), 45–75 (55) long by 340-460 (401)
wide, with two lateral sensory pits (Fig. 11 - sp),
25-45 (34) long by 30-45 (38) wide. Proboscis
receptacle divided in two portions (Fig. 11),
proximal portion (Fig. 11 - ppr) much longer and
narrower than distal portion, 442-602 (514)
long, distal portion (Fig. 11 - dpr) wider, 150-
225 (171) long by 265-400 (349) wide, single
walled (Fig. 12 – swpr). Cerebral ganglion (Figs
11 and 12 - cg), 120-185 (157) long by 50-85
(68) wide, along ventral wall of proboscis
receptacle. Lemnisci ribbon-like (Fig. 13 - lem)
0,9mm-3.21mm (1.81mm) long, sometimes
looped, sometimes reaching posterior region of
trunk, multinucleated; characteristically wider
proximally, where developing nuclei are located
before moving posteriad as lemnisci grow, this
region 0.35mm-1.00mm (0.52mm) long (Fig. 13
- lnp). Reproductive system primordial. Testes 2,
same size (Fig. 15), tandem, in posterior portion
of trunk, partially superposed, anterior testis
(Fig. 15 – at) 165-275 (206) long by 55-165
(106) wide. Developing cement glands 8 (Fig.
15 - cg), each with a single, large central nucleus,
juxtaposed to testes. Saefttigen's pouch (Fig. 15
– Sp), 80-158 (113) long; bursa retracted in all
male specimens (Fig. 15 – rb). Uterine bell (Fig.
16 - ub) 49-85 (62) long; uterus (Fig. 16 - u) 182-
253 (220) long; vagina (Fig. 16 - v) surrounded
by strong, muscular sphincter (Fig. 16 - vs), 194-
243 (218) long; muscular sphincter 97-105 (98)
long. Protonephridia not observed. Genital pore
terminal, in males (Fig. 15 - mgp) and in females
(Fig. 16 - fgp).
Figure 5. Gigantorhynchus echinodiscus, unencysted cystacanth, from Labiotermes emersoni, bar = 0.5mm.
329
Amatoet al.
Cystacanths of Gigantorhynchus in Neotropical termites
Taxonomic summary.
Intermediate host: Brazilian termites,
Labiotermes emersoni (Araujo, 1954) and
Orthognathotermes heberi Raw & Egler, 1985.
Locality: P.N. Serra da Canastra (-20.249 S, -
46.563 W), State of Minas Gerais, Brazil.
Site of infection: hemocoel of soldier termites.
Prevalence: Labiotermes emersoni – 100% of
the soldiers; Orthognathotermes heberi – 5-15%
of the soldiers.
Intensity: 1 worm/host.
Specimens deposited: Cystacanths, voucher
specimens from L. emersoni (CHIOC – 37.956a-
o); cystacanths, voucher specimens from L.
emersoni (MZUSP – 21.965).
Specimens examined: Adult specimens of G.
echinodiscus and G. lutzi borrowed from the
CHIOC: G. echinodiscus – 10.574a, d, e, and f;
Figures 6-8. Gigantorhynchus echinodiscus, unencysted cystacanth, from Labiotermes emersoni, processed for SEM. 6. entire
proboscis, neck (n), trunk (t), lateral sensory pit (white arrow – sp), and distal trunk portion (arrow showing the proboscis - trunk
limit – ntl), bar = 100 µm; 7. en face view of proboscis, first circle of 6 larger hooks (white arrows) and second circle of 12 hooks,
smaller and placed, in pairs, between the large hooks of the first circle (asterisks), bar = 100 µm; 8. lateral view of proboscis
showing the space (s) between the first two circles of large hooks and the remainder, almost rootless spines, bar = 100 µm.
330
Neotrop. Helminthol., 8(2), 2014
Figures 9-14. Gigantorhynchus echinodiscus, unencysted cystacanth, from Labiotermes emersoni. 9. en face view of proboscis,
first circle of 6 larger hooks (white arrows) and second circle of 12 hooks, smaller and placed in pairs between the large hooks of
the first circle (asterisks), bar = 50 µm; 10. lateral view of proboscis, showing almost rootless spines, bar = 100 µm; 11. lateral
view of entire proboscis, showing the characteristic proboscis receptacle divided into two portions; a distal portion (dpr), a
proximal portion (ppr), and the limit between these portions (white arrow). – ptl); the ventral cerebral ganglion (cg), one of the
lateral sensorial pit (sp), just anterior to the limit between the trunk and the neck (ptl), bar = 100 µm; 12. the proximal portion of
the single wall proboscis receptacle (swpr) and the contiguous, ventral cerebral ganglion (cg), bar = 50 µm; 13. anterior end of
trunk, showing the proximal, enlarged, nucleated portion (lnp) of the lemnisci (lem), bar = 200 µm; 14. lateral view of apical
portion of the proboscis, and the bifid root (br), root (r), and blade of one of the large hooks, bar = 50 µm.
331
G. lutzi – 15.408c, e, and f (Table I).
Remarks
All Brazilian termites examined showing
alterations induced by the acanthocephalan
parasites where soldiers, which are always fed
by the workers, although workers have not yet
been found infected.
When male and female cystacanths are
compared it is not possible to detect differences
in size or oncotaxy in the proboscis. The
lemnisci have a proximal portion wider,
showing several nuclei close together (Fig. 13 –
lnp). As the lemnisci grow the nuclei move from
the proximal portion and get distributed along
their length. The testes are always partly
superposed and located in the posterior region of
the trunk, condition observed in the adult male
specimens borrowed from the CHIOC. Due to
the fact that anteaters feed directly on termites, it
is not surprising that the life cycle of G.
echinodiscus does not include paratenic hosts.
Amatoet al.
Cystacanths of Gigantorhynchus in Neotropical termites
Figures 15-16. Gigantorhynchus echinodiscus, unencysted cystacanth, from Labiotermes emersoni. 15. posterior portion of the
trunk, showing the male reproductive system: anterior testis (at) and posterior testis (pt) of same size, tandem, and partially
superposed, as was observed in the male adult specimen examined from the CHIOC (10.574c); the incipient cement glands (cg),
the Saefftigen´s pouch (Sp), the retracted copulatory bursa (rb), and the terminal, male genital pore (mgp), bar = 100 µm; 16.
posterior portion of the trunk showing the female reproductive system: incipient ovarian balls (ob), the uterine bell (ub), the
uterus (u), the vagina (v), surrounded by the vaginal sphincter (vs), and terminal, female genital pore (fgp), bar = 100 µm.
332
Neotrop. Helminthol., 8(2), 2014
CHIOC
Nº Slide
Nº Specific
name Host1Conservation
medium Provenience2Colected
by Date Determined
by Date Observations
308
echinodiscus
?
Glycerin
?
?
?
?
? -
310
echinodiscus
Tamandua
tetradactyla
ETOH 70% -
Glycerin
Angra dos Reis, RJ
L.
Travassos
01 Nov
1913
L.
Travassos
29 Sep 1952 -
1393
echinodiscus
Myrmecophaga
sp.
Formalin 5%
Instituto
de
Bacteriologia, SP
A.
Lutz
?
L. Travassos
Feb 1917 -
1397
echinodiscus
Myrmecophaga
sp.
Formalin 5%
Instituto de
Bacteriologia, SP
O.
Dreher
?
?
? -
1398
echinodiscus
Myrmecophaga
sp.
Formalin 5%
Instituto de
Bacteriologia, SP
A. Lutz
?
L. Travassos
Feb 1917 -
1400
echinodiscus
Myrmecophaga
sp.
Formalin 5%
Instituto de
Bacteriologia, SP
A. Lutz
?
L. Travassos
? -
1401
echinodiscus
Myrmecophaga
sp.
Formalin 5%
Instituto de
Bacteriologia, SP
A. Lutz
?
L. Travassos
Feb 1917 -
1402
echinodiscus
Myrmecophaga
sp.
Formalin 5%
Instituto de
Bacteriologia, SP
A. Lutz
?
L. Travassos
01 Feb 1915 -
1403
echinodiscus
Myrmecophaga
sp.
Formalin 5%
Instituto de
Bacteriologia, SP
A. Lutz
?
L. Travassos
Feb 1917 -
1404
echinodiscus
Myrmecophaga
sp.
Formalin 5%
Instituto de
Bacteriologia, SP
?
?
?
? -
1435
echinodiscus
Myrmecophaga
tetradactyla
ETOH 70%
Museu Paulista,
Franca, SP
?
?
A. Porta
22 Mar 1905 -
1436
echinodiscus
Myrmecophaga
tetradactyla
Canada balsam
Museu Paulista,
Franca, SP
?
?
A. Porta
22 Mar 1905 -
1459
echinodiscus
Myrmecophaga
tetradactyla
ETOH 70%
Museu Paulista,
Franca, SP
O. Dreher
23 Dec 1902
A. Porta
? -
1460
echinodiscus
Myrmecophaga
tetradactyla
Canada balsam
Museu Paulista,
Franca, SP
O. Dreher
?
?
? -
1464 echinodiscus Myrmecophaga
tetradactyla ETOH 70% Museu Paulista,
Franca, SP O. Dreher ?L. Travassos ? -
1525 a-h echinodiscus Tamandua
tetradactyla Canada balsam Museu Paulista,
Franca, SP O. Dreher 23 Dec 1902 A. Porta ? -
1526 a-c echinodiscus Tamandua
tetradactyla Canada balsam Museu Paulista, SP O. Dreher 23 Dec 1902 A. Porta ? -
Table 1. List of records of Gigantorhynchus echinodiscus and G. lutzi in the COLEÇÃO HELMINTOLÓGICA DO INSTITUTO OSWALDO CRUZ (CHIOC),
Rio de Janeiro.
333
Amatoet al.
Cystacanths of Gigantorhynchus in Neotropical termites
3979
echinodiscus
Tamandua
tetradactyla
Formalin 5%
São João, MT
L. Travassos
04 Jul 1922
L. Travassos 01 Nov 1922 -
3980
echinodiscus
Tamandua
tetradactyla
Formalin 5%
São João, MT
L. Travassos
04 Jul 1922
L. Travassos 01 Nov 1922 -
6270
echinodiscus
“Tamandua
tetradactylus”
ETOH 70% -
Glycerin
Instituto Pasteur, SP
A. Carini &
J.
Maciel
17 Aug 1915
L. Travassos 01 Sep 1915 -
9190
echinodiscus
Myrmecophaga
jubata
ETOH 70%
-
Glycerin
Instituto Pasteur, SP
A. Carini
27 Mar 1905
L. Travassos ? -
9320
a-b
echinodiscus
?
Canada balsam
?
J. G. de Faria
?
L. Travassos 29 Mar 1905 -
9391
a-c
echinodiscus
Myrmecophaga
jubata
Canada balsam
Instituto Pasteur, SP
A.
Carini
29 Mar 1905
L. Travassos 29 Mar 1905 -
9749
echinodiscus
Tamandua
tetradactyla
Acetic formalin
Abaeté, PA
E. Chagas
04 Jun 1937
L. Travassos 01 Aug 1937 -
9750
echinodiscus
Tamandua
tetradactyla
Acetic formalin
Abaeté, PA
E. Chagas
04 Jun 1937
L. Travassos 01 Aug 1937 -
9914
echinodiscus
Tamandua
tetradactyla
Acetic formalin
Belém, PA
H. Lent
19 Aug 1936
J. F.T. Freitas &
H. Lent
1938 -
10574
a-f
echinodiscus
Tamandua
tetradactyla
Canada balsam
Belém, PA
H. Lent
19 Aug 1936
J. F.T. Freitas &
H. Lent
1938 -
10587
echinodiscus
Tamandua
tetradactyla
Canada balsam
Belém, PA
H. Lent
19 Aug 1936
J. F.T. Freitas &
H. Lent
1938 -
13104
lutzi
Caluromys
philander3
Acetic formalin
Aurá, Belém, PA
G. Jansen
11 Nov 1940
D. A. Machado
Filho
01 May 1941 Holotype &
Alotype not
designated
13105
lutzi
Caluromys
philander3
Acetic formalin
Aurá, Belém, PA
G. Jansen
11 Nov 1940
D. A. Machado
Filho
01 May 1941 Paratypes
15408
a-f
lutzi
Caluromys
philander3
Canada balsam
Aurá, Belém, PA
G. Jansen
11 Nov 1940
D. A. Machado
Filho
01 May 1941 Paratypes
16184
echinodiscus
Tamandua
tetradactyla
Acetic
formalin
Salobra, MS
L. Travassos &
J.
F.T. de
Freitas
29 May 1942
D. A. Machado
Filho
1946 -
17541 echinodiscus “Tamandua
tetradactyla
tetradactyla”
Acetic
formalin Linhares (Cupido
Farm), ES L. Travassos, J.
F. T. de Freitas
& H. Travassos
02 Mar 1948 D. A. Machado
Filho 01 Mar 1949 -
20039 echinodiscus “Tamandua
bandeira” Acetic
formalin State of Mato Grosso L. Travassos 29 Sep 1952 L. Travassos 29 Sep 1952 -
Table I. List of records of Gigantorhynchus echinodiscus and G. lutzi in the COLEÇÃO HELMINTOLÓGICA DO INSTITUTO OSWALDO CRUZ
(CHIOC), Rio de Janeiro (cont.).
CHIOC
Nº Slide
Nº Specific
name Host1Conservation
medium Provenience2Colected
by Date Determined
by Date Observations
334
The effects induced by acanthocephalans on
their intermediate hosts were discussed by
various authors and range from increased
conspicuousness, either by the larvae acquiring
pigmentation or by pigmentation dystrophy of
the host, which results from the interference of
the acanthocephalan with the metabolic pathway
for ommochrome pigmentation in the isopod
hosts (Oetinger & Nickol, 1982).
This was not the case in the Caribbean termite,
N. acajutlae. In the U. S. Virgin Islands Fuller et
al. (2003), Fuller & Jeyasingh (2004), and
Nickol et al. (2006) found only workers
infected. It is not clear why the workers of the
Brazilian species of termites, known to feed the
soldiers, do not get infected themselves, as only
the workers feed directly on the feces of the final
hosts, anteaters and didelphid marsupials,
although this behavior has not been observed
directly. Another interesting aspect is that in the
life cycle of G. echinodiscus there are no
paratenic hosts involved, as there are in the life
cycle of N. acajutlae in the Caribbean.
R e ichensper g e r ( 1 9 2 2 ) d e s c r i b e d
Acanthocephalus aenigma Reichensperger,
1922, as a new species based on cystacanths
from the hemocoel of specimens of two termite
species from the locality of Encano Alto, State of
Santa Catarina, Southern Brazil. One of them
was Cornitermes cumulans, the same species
that built the nests lately recolonized by
Labiotermes emersoni (Araujo, 1954) in the
P.N. Serra da Canastra (Figs 1 and 2), and found
infected by the cystacanths of G. echinodiscus
reported in the present work. According to
Nickol et al. (2006) “Nothing further is known
about this species, and usually it is considered to
be unrecognizable. Meyer (1932) assigned it to
Oligacanthorhynchus Travassos, 1915, as an
appendix. Possession of 30 proboscis hooks
instead of 36 distinguishes it from O.
venezuelensis and suggests that A. aenigma
properly should be assigned to Neoncicola
Schmidt, 1972”. In the cystacanths' description,
Reichensperger (op. cit.) mentioned that the
testes were located in the mid-trunk, unlike the
DISCUSSION
Neotrop. Helminthol., 8(2), 2014
position found in the cystacanths described in
the present work. So, there is a possibility that
the acanthocephalan found as cystacanths in the
termites from Santa Catarina, might be yet
another species. This confirms that Meyer (op.
cit.) was correct assigning the species to
Oligacanthorhynchidae, as the testes in this
family are post equatorial, but not in the
posterior region of the trunk.
Specimens of O. heberi were originally
described showing an unprecedented
dimorphism in soldiers (called by the authors
“major soldiers” and “minor soldiers”,
respectively) ─ a case of parasitism by
acanthocephalans not perceived by Raw & Egler
(1985). In 1991, Cancello published a short note
on the presence of acanthocephalan larvae in the
hemocoel of termite soldiers [Cornitermes
cumulans, Orthognathotermes sp., and
Paracornitermes sp. (today Labiotermes). Since
then, other species of termites have been
recorded with the same kind of parasites: Termes
spp., Amitermes amifer, Embiratermes
neotemicus, and Spinitermes sp.]. But,
unhappily, because the acanthocephalan larvae
found in these species, the true identity of these
larvae will have to wait to be determined.
In 2003, one of us (JFRA) received specimens of
termites fixed in ethanol from the junior authors
(normal and parasitized soldiers of O. heberi -
Figs 3 and 4 of the present paper). Rocha &
Cancello (2009, pg. 8), in the revision of
Orthognathotermes stated: “The minor soldiers
described by Raw & Egler (1985) are
individuals infested by an undetermined species
of Acanthocephala. The soldier caste is
monomorphic, contrary to the original
description”.
Six species of Gigantorhynchus were
considered valid by Yamaguti (1963) and Amin
(in Crompton & Nickol, 1985), two of which
were the first to be described to Science and from
Brazil: G. echinodiscus found i n
myrmecophagids and G. lutzi found in didelphid
marsupials (Caluromys philander (Linnaeus,
1758). Besides having different final hosts, the
Brazilian species differ by the number of hooks
335
Amatoet al.
Cystacanths of Gigantorhynchus in Neotropical termites
present in the first two circles of hooks of the
proboscis - G. echinodiscus (Figs 6-8) with the
formula (6+12) (first circle with six large hooks,
intercalated by a second circle of 12, smaller
hooks arranged in pairs among the larger hooks
of the first circle with roots appearing 'bifid' (Fig.
14) and G. lutzi with the formula 6+6 (first circle
with six large hooks also intercalated by a
second circle of six, slightly smaller, hooks.
Gigantorhynchus ortizi Sarmiento, 1954, from
Peruvian marsupials [Metachirus nudicaudatus
(Desmarest, 1817) known as 'cuíca-de-quatro-
olhos'] and for having the same large hook
formula (6+6) in the proboscis, is similar to G.
lutzi (Sarmiento 1954).
Gigantorhynchus lopezneyrai Días-Ungría,
1958 and Gigantorhynchus ungriai Antonio,
1958 were described from Venezuela, both from
myrmecophagids. The former species with the
large hook formula (4+8) (hooks in the first and
second circle, respectively), appears to be an
incorrect observation and needs to be revisited,
and the later with the same type of large hook
formula (6+12) as is found in G. echinodiscus.
Even though Días-Ungría (1958) recorded a
smaller number of large hooks in the first two
circles of the proboscis in G. lopezneirai (the
author did not show an unquestionable 'en face'
drawing of the proboscis). Antonio (1958), did
not show good illustrations of the new species,
including the proboscis, and did not present an
'en face' drawing of the proboscis, which in this
case, for having the same large hook formula as
G. echinodiscus, would have been of utmost
importance. Although the author has pointed out
specific differences in the pseudo segmentation
of the trunk, he left serious doubts about the
validity of this species. The last species to be
described for Gigantorhynchus was
Gigantorhynchus pesteri Tadros, 1966, from a
Baboon of Rhodesia, Africa. The species
described by Tadros (1966) was based only on
two immature females which had not evaginated
the proboscis. The author reported an unusual
large hook formula ─ a single crown of 4 large
hooks at the summit of the proboscis. Certainly
this species needs to be revisited.
As the present paper is the first to show the
unquestionable structure of the proboscis
through SEM images (Figs 6-8), it would be
important to look for infected termites in
Venezuela, above all, in the ranges occupied by
myrmecophagids and/or recover adults from the
intestine of 'oso melero' to process for SEM
images which could be compared with those of
the present paper.
The CHIOC does not hold any cystacanth of any
species of Gigantorhynchus from any
intermediate host. This information has been
confirmed by the examination of all 31 records
of G. echinodiscus from myrmecophagids and 1
record of G. lutzi annotated in three index cards
(CHIOC Nºs 13.104 and 13.105 in AFA, and
15.408 mounted in Canada balsam), but found
on a single host from Aurá, in the greater Belém,
State of Pará (Table 1). The oldest record of
specimens of Gigantorhynchus spp. deposited in
the CHIOC is dated of 1902 and the latest has
been recorded 1952 (Table 1). Due to the poor
condition in which the deposited specimens of
G. lutzi are, it is very important that new efforts
be made to find didelphids infected in Aurá,
Belém, PA. New efforts should also be made to
find anteaters which are near death, for any
reason, or which were recently road-killed to be
examined by helminthologists or immediately
frozen for a later necropsy by specialists, who
c o u l d c o l l e c t a n d p r e p a r e t h e s e
acanthocephalans following modern and
recommended techniques. Only then, the two
species known from Brazil could be revisited
using quality specimens.
Special thanks are due to Marcelo Knoff, curator
of the CHIOC, Instituto Oswaldo Cruz –
FIOCRUZ, Rio de Janeiro, for lending
specimens of G. echinodiscus and G. lutzi, for
providing copies of the file cards for the survey
data on the deposited specimens of both species
of Gigantorhynchus presented in Table I, for
providing literature, and for accepting voucher
specimens of cystacanths from termites to be
deposited in the CHIOC; to Philip J. Scholl,
ACKNOWLEDGEMENTS
336
Neotrop. Helminthol., 8(2), 2014
Oxford, FL, USA, for critically revising the
English version of the manuscript (at request of
JFRA); to Moisés Gallas for processing the
specimens for SEM; to Suzana B. Amato, and
Cláudia C. Marques of UFRGS (for providing
literature and kindly reading the manuscript); to
Marilia Brasil Sato of Universidade Federal
Rural do Rio de Janeiro, also for providing
literature; to
to Marta Elena Fabián
for kindly translating the Abstract into Spanish.
EMC thanks the Grant of National Council for
Scientific and Technological Development
(CNPq- Proc. 562256/2010-5). MMR and TFC
thank the São Paulo Research Foundation
(FAPESP) for the postdoctoral research
scholarships 2012/00952-9 and 2013/05610-1,
respectively.
Christian Bordereau for allowing us
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338
