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ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
RESEARCH NOTE / NOTA CIENTIFICA
NEW FRESHWATER FISH HOSTS OF GORDIIDS (NEMATOMORPHA) LARVAE IN THE SOUTH
OF CHILE
NUEVOS PECES DULCEACUICOLAS HOSPEDEROS DE LARVAS DE GORDIACEOS
(NEMATOMORPHA) EN EL SUR DE CHILE
Instituto de Parasitología, Facultad de Medicina, Edificio de Ciencias Biomédicas, IslaTeja, Universidad Austral de Chile,
Valdivia, Chile
*Corresponding author: ptorres@uach.cl
PatricioTorres-Hevia: https://orcid.org./0000-0002-9882-0183
1*
PatricioTorres-Hevia
Neotropical Helminthology
79
doi:10.24039/rnh20201511026
Neotropical Helminthology, 2021, 15(1), ene-jun:79-84.
D
ABSTRACT
Keywords:
Aplochiton
– Chile – fish – Nematomorpha – parasites –
Trichomycterus
Nematomorpha Vejdovsky, 1886 includes most of its species in the taxon Gordiida, presenting a
freshwater free-living adult and a parasitic larval stage that live in some aquatic invertebrates, amphibians
and fish. Present results documented morphological characteristics of unencysted and encysted larvae of
gordiids in the intestines of two new freshwater fish hosts,
Aplochiton zebra
Jenyns, 1842
(Osmeriformes, Galaxiidae) and
Trichomycterus areolatus
Valenciennes, 1846 (Siluriformes:
Trichomycteridae), in the south of Chile.
RESUMEN
Palabras clave:
Aplochiton
– Chile – Nematomorpha – parásitos – peces –
Trichomycterus
Nematomorpha Vejdovsky, 1886 incluye la mayoría de sus especies en el taxón Gordiida, incluyendo un
estado adulto de vida libre dulceacuícola y un estado larvario parasítico que vive en algunos invertebrados
acuáticos, anfibios y peces. Los resultados del presente estudio documentan las características
morfológicas de larvas enquistadas y no enquistadas de gordiáceos en dos nuevos peces hospederos
dulceacuícolas,
Aplochiton zebra
Jenyns, 1842 (Osmeriformes, Galaxiidae) y
Trichomycterus areolatus
Valenciennes, 1846 (Siluriformes, Trichomycteridae), en el sur de Chile.
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80
The Phylum Nematomorpha Vejdovsky,1886
includes around 350 species distributed in the
Gordiida, with freshwater species, and
Nectonematida taxa with five marine species
(Hanelt
et al
., 2005; Szmygiel
et al.
, 2014).
Gordiida species, commonly called horsehair
worms, in their adult stage reproduce in freshwater
environments where they lay eggs that develop into
larvae (Hanelt
et al
., 2005). The larvae hatch and
establish as parasites after being ingested by
paratenic hosts, including aquatic insects
(Coleoptera, Diptera, Trichoptera and
Ephemeroptera), snails, annelids, crustaceans
(amphipods and copepods), amphibians and fish.
In these hosts, larvae secrete a cystic wall when
located in their tissues or body cavity (Poinar &
Doelman, 1974; Hanelt & Janovy, 2003; Hanelt
et
al
., 2012). Aquatic insects predated by terrestrial
arthropods (orthopterans, coleopterans and
mantids) are infected by the larval stage. As they
develop into their adul stage, host behavior is
manipulated by the parasite so that they look for
and jumps into water; here, the parasite abandon
their host to mate (Bolek & Coggins, 2002; Hanelt
& Janovy, 2003; Hanelt
et al
., 2012; Barquin
et al
.,
2015).
The records of encysted or unencysted gordiids in
fish are scarce and are related to natural infections
by
G. aquaticus
in
Misgurnus fossilis
(Linnaeus,
1758),
Lampetra
fluviatili
s (Linnaeus, 1758),
Lampetra planeri
(Bloch, 1784),
Thymallus
thymallus
(Linnaeus, 1758),
Phoxinus phoxinus
(Linnaeus, 1758), and
Salmo
sp. (Villot, 1881; Von
Linstow, 1898; Malmqvist & Moravec, 1978), as
well as infections by
Gordius
sp. in
Barbatula
barbatula
(Linnaeus, 1758) (syn.
Barbatulus
barbatulus
),
Rutilus rutilus
(Linnaeus, 1758),
Leuciscus idus
(Linnaeus, 1758), and
Carassius
carassius
(Linnaeus, 1758) (Zhokhov &
Molodozhnikova, 2008), in Europe. Additionally,
the experimental infection by
Gordius robustus
Leidy, 1851,
P. varius
and
Chordodes morgani
Montgomery, 1898 has been verified in
Notropis
stramineus
(Cope, 1865) (syn.
Notropis
ludibundus
) in the USA (Hanelt & Janovy, 2003).
Natural infections by unidentified gordiid cysts
was identified in
Galaxias
vulgaris
Stokell, 1949
and
Gobiomorphus breviceps
(Stokell, 1939) in
INTRODUCTION
New Zealand (Blair, 1983), and in
Galaxias
maculatus
(Jenyns, 1842) in Chile (Torres
et al
.,
2017).
The objective of this research note is to report and
describe the morphology of gordiid larvae in two
new fish hosts in the Lingue River and Riñihue
Lake, in the south of Chile.
During January 2014 and 2015, 12 fish were
collected distributed in four
Aplochiton zebra
Jenyns, 1842 (Osmeriformes, Galaxiidae) [three in
the Lingue River (39°26´60´´S; 73°13´60´´W):
one female and two with undetermined sex (US),
with 9.3-10.6 cm of body length (BL) and 1 female
with 10.8 cm BL in the Riñihue Lake (39°50´36´´S;
72°17´39´´W)], and eight
Trichomycterus
areolatus
Valenciennes,1846 (Siluriformes:
Trichomycteridae) [three females in the Lingue
River with 6.0-6.9 cm BL and two females and 3
males in the Riñihue Lake with 4.5-6.7 cm BL]. All
the fish were caught, with authorization from the
Subsecretaria de Pesca y Acuicultura (Resolution
No. 2430/2013), by electric fishing and taken alive
to the Institute of Parasitology, kept in aquariums at
4°C until dissection and examination within 48 hr
after its capture.
Gordiids were searched in the stomach, intestines,
liver, spleen and gonads. The stomach and
intestines were opened longitudinally and cut into
2-3 cm long sections. With the contents of the
stomach and intestines of each section,
preparations were made between slides and
coverslips and observing in a light microscope with
40X and 100X. Subsequently, each section was
placed between slides and coverslips adding saline
solution with slight compression, examining with a
light microscope. The other organs were minced
and then made preparations between slides and
coverslips with slight compression, observing
under the microscope. Number of encysted and
unencysted larvae of gordiids was determined. The
morphological characteristics registered
correspond to those proposed by Hanelt & Janovy
(2002). Voucher specimens were deposited in the
Collection of the Museo de Zoología, Universidad
Neotropical Helminthology, 2021, 15(1), ene-jun
MATERIAL AND METHODS
Torres-Hevia
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81
de Concepción, Chile.
Ethic aspects
: The research adhered to ethical
aimed at reducing the minimum possible damage
to the animals under study as well as the application
of biosafety standards in field and laboratory work.
The number of infected / examined fish (range of
parasite number / infected fish) was as follows for
each host and locality:
A. zebra
: Lingue River 1/1
(280 unencysted larvae), Riñihue Lake 2/3 (7-11
encysted larvae );
T. areolatus
: Lingue River 2/3
(7-12 encysted larvae), Riñihue Lake 5/5 (1-122
encysted and unencysted larvae). All gordiids were
alive in the intestines of the hosts. Table 1 and Fig.1
show the morphological characteristics of encysted
and unencysted larvae.
In other studies, in
G.vulgaris
and
G.cotidianus
,
encysted larvae have been recorded in the
intestines, esophagus, stomach, and liver (Blair,
RESULTS ANS DISCUSSION
1983), in
T. thymallus
and an unidentified species
of
Salmo
(Villot, 1881) and
N. ludibundus
(Hanelt
& Janovy, 2003) in intestines; and in
G. maculatus
in intestines and liver (Torres
et al
., 2017). For
Gordius robustus
,
P. varius
and
C. morgani
in
experimental infections of
N. stramineus
, the
encysted larvae were found in the intestines,
observing a similar response from the host,
including the formation of granulomas around the
cysts, which in some cases could destroy them
(Hanelt & Janovy, 2003). In
G. maculatus
, the
presence of inflammatory infiltrate associated with
gordiid encysted larvae was not observed,
however, although most of them were viable, a
smaller proportion showed dead larvae (Torres
et
al
., 2017).
The characteristics of unencysted larvae
(measurements of the preseptum and postseptum,
the absence of longer outer hooks on the outer ring
of the preseptum, and the presence of only one
terminal spine in the postseptum) and encysted
ones (larvae folded twice without spines on the
preseptum and encysted larvae length) in both
hosts (Table 1) suggest they correspond to the
Gordius
genus according to the descriptions of the
Neotropical Helminthology, 2021, 15(1), ene-jun
Table 1
. Morphological characteristics (mean and range in µm) of larvae and cysts of gordiids in
Aplochiton zebra
12
Jenyns, 1842 and
Trichomycterus areolatus
Valenciennes, 1846 from Lingue River and Riñihue Lake in the south
of Chile.
Characteristics
A. zebra
1
A. zebra
2
T. areolatus
1
T. areolatus
2
Unencysted l
arvae
n
=
5
n
=
8
n
=
7
Preseptum length
39.5 (30
-
45)
44.7 (16
-
59)
35.2
(19
-
44)
Preseptum width
17.8 (14
-
20)
17.0
(11
-
22)
16.9
(11
-
21)
Postseptum length
100.4 (62
-
121)
97.2 (19
-
161)
83.1
(45
-
110)
Postseptum width
16.2 (14
-
18)
14.9 (9
-
20)
16.3
(9
-
21
)
Stylet length
21.9 (17
-
31)
23.6 (11
-
35)
17.4
(10
-
21)
Stylet width
6.9 (5
-
9)
10.6 (9
-
14)
4.9
(4
-
7
)
Pseudointestine length
28.5 (18
-
39)
31.2 (18
-
46)
30.9
(20
-
38
)
Pseudointestine width
19.8 (12
-
27)
10.6 (9
-
14)
9.8 (8
-
12)
Encyst larvae
n
=
6
n
=
5
Total length
52.5 (40
-
70)
66.5
(49
-
98)
Total width
41.7
(30
-
55)
26.1
(19
-
41)
Cyst wall length
13.1 (9
-
18)
14.3
(8
-
22)
Cyst wall width
13.8 (9
-
19)
3.2
(2
-
6)
Cyst larva length
26.5 (21
-
35)
37.9
(28
-
54)
Cyst larva width
14.1 (10
-
18)
19.8
(15
-
28)
Cyst larval folding
2
2
Gordiids (Nematomorpha) larvae in fish
image/svg+xml
82
unencysted and encysted
Gordius
spp. larvae in the
northern hemisphere (Hanel & Janovy, 2002;
Szmygiel
et al
., 2014; Harkins
et al
., 2016).
Previously, in the Valdivia River basin, where the
Riñihue Lake is located, a female of
Gordius
genus
was registered, which could correspond to
G.
robustus
(Schmidt-Rhaesa, 2016).
The new hosts of gordiids consume different prey
through which they could acquire the infection, for
example,
A. zebra
is a consumer of chironomids,
Ephemeroptera or Trichoptera while
T. areolatus
consumes gastropods, oligochaetes, small
crustaceans and insects, such as Ephemeroptera
(Ruiz & Marchant, 2004), all groups registered as
paratenic hosts (Poinar & Doelman,1974; Hanelt &
Janovy, 2003; Hanelt
et al
., 2012).
In Chile, nematomorphs have been scarcely
investigated, describing only seven species in their
adult stage, among them
Beatogordius latastei
(Camerano, 1895),
Neochordodes talensis
Figure 1
. A. Unencysted larva of gordiid found in the intestine of
Aplochiton zebra
from Lingue River (arrow: terminal spine). B.
Unencysted larva of gordiid found in the intestine of
A. zebra
from Riñihue Lake. C. Encysted larva found in the intestine of
Trichomycterus areolatus
from Lingue River. D. Encysted larva found in the intestine of
T. areolatus
from Riñihue Lake (arrow:
terminal spine). Abbreviations: Pre = preseptum. Po = postseptum. Ps = pseudointestine. S = stylet.
Neotropical Helminthology, 2021, 15(1), ene-jun
Torres-Hevia
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83
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Calling behavior of male
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domesticus
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(Nematomorpha:
Gordiida)
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Zealand Journal of Zoology, vol. 10, pp.
341-343.
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species.
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Hanelt, B & Janovy, J. 2002.
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The author is indebted with Raul Arriagada for the
technical support in the field and Claire Evans for
the English revision of the manuscript.This study
was supported by the parasite diversity and
zoonosis transmitted by aquatic organisms
program (DID 1201002).
ACKNOWLEDGMENTS
Neotropical Helminthology, 2021, 15(1), ene-jun
Gordiids (Nematomorpha) larvae in fish
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Received February 10, 2021.
Accepted March 6, 2021.
Neotropical Helminthology, 2021, 15(1), ene-jun
Torres-Hevia