ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2020, 14(2), jul-dic:199-206.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
OCCURRENCE OF HETERAKIS GALLINARUM (SCHRANK, 1788) (NEMATODA: HETERAKIDAE)
IN GALLUS GALLUS DOMESTICUS LINNAEUS, 1758 IN VITORIA, ESPIRITO SANTO, BRAZIL
OCURRENCIA DE HETERAKIS GALLINARUM (SCHRANK, 1788) (NEMATODA: HETERAKIDAE)
EN GALLUS GALLUS DOMESTICUS LINNAEUS, 1758 EN VITORIA, ESPIRITO SANTO, BRASIL
1Programa de Pós-Graduação em Parasitologia, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil.
2Laboratório de Helmintologia Animal, Departamento de Patologia, Universidade Federal do Espírito Santo, Vitória, Espírito
Santo, Brasil.
*Corresponding author: marianabio.brandao@gmail.com
1,2,* 1 2
Mariana Brandão Simões ; Alan Lane de Melo & Narcisa Imaculada Brant Moreira
Neotropical Helminthology
199
doi:10.24039/rnh2020142794
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Volume14,Number2(jul-dec)2020
ABSTRACT
Heterakis Dujardin, 1845 is a nematode parasite of birds with cosmopolitan distribution. In Brazil, there
are reports of 14 species occurring in different species of domestic and wild birds. Among the reported
species, Heterakis gallinarum (Schrank, 1788) presents a potential threat to commercial breeding sites as
it is a vector of Histomonas meleagridis Smith, 1895. The Trichomonadida protozoans causing
histomoniasis in birds represent critical infection that can be lethal and cause catastrophic economic
losses. The present study reports the occurrence of H. gallinarum in the caecum of free-range chicken
(Gallus gallus domesticus Linnaeus, 1758) sold at a street market in Vitoria, Espirito Santo, Brazil. The
three male and three female specimens found were studied and illustrated.
Keywords: Nematodes – Histomonas meleagridis – histomoniasis – morphology – taxonomy – life cycle
RESUMO
Heterakis Dujardin, 1845 é um nematódeo parasito de aves e de distribuição cosmopolita. No Brasil são
reportadas 14 espécies decorrentes de diferentes espécies domesticadas e selvagens. Entre as espécies já
publicadas, Heterakis gallinarum (Schrank, 1788) apresenta ameaça para os criadores comerciais de aves
pois é um vetor potencial para Histomonas meleagridis Smith, 1895, um protozoário Trichomonadida
causador da histomoníase em ave, uma severa infecção que pode ser letal e causar perdas econômicas
catastróficas. O presente estudo apresenta a ocorrência de Heterakis gallinarum em ceco intestinal de uma
galinha (Gallus gallus domesticus Linnaeus, 1758) comercializada num grande centro comercial de
Vitória, Espírito Santo, Brasil. Três machos e três fêmeas são descritos e ilustrados neste estudo.
Palavras-chave: Nematódeos – Histomonas meleagridis – histomoníase – morfologia – taxonomia – ciclo de vida
INTRODUCTION
200
RESUMEN
Palabras clave: Nematodos – Histomonas meleagridis – histomoniasis – morfología – taxonomía – ciclo de vida
Heterakis Dujardin, 1845 es un nemátodo que parasita las aves y presenta distribución cosmopolita. En
Brasil, se registran 14 especies que ocurren en diferentes especies domesticadas y silvestres. Entre las
especies reportadas, Heterakis gallinarum (Schrank, 1788) representa una amenaza potencial para los
criaderos comerciales ya que es un vector de Histomonas meleagridis Smith, 1895, protozoario
Trichomonadida que causa histomoniasis en las aves, una infección grave que puede ser letal y causar
pérdidas económicas catastróficas. El presente estudio regsitra la ocurrencia de H. gallinarum en el ciego
de pollos de corral (Gallus gallus domesticus Linnaeus, 1758) vendidos en un gran centro comercial de
Vitoria, Espirito Santo, Brasil. En este estudio se describen e ilustran los tres ejemplares machos y tres
hembras encontrados.
Neotropical Helminthology, 2020, 14(2), jul-dic
infections are often deadly (Cupo & Beckstead,
2019).
This parasite thrives in hosts such as Numida
m e l e a g r i s (Lin naeus, 1758 ) (h e lmete d
guineafowl), Phasianus colchicus Linnaeus, 1758
(common pheasant), and G. gallus domesticus
Linnaeus, 1758 (chicken), while in other host
species there seems to be no adaptation efficiency
(Lund & Chute, 1974). The prophylaxis to prevent
this helminthiasis is also critical in avoiding the
transmission of Trichomonadida protozoan
Histomonas meleagridis Smith, 1895, which
causes histomoniasis in birds, another critical
infection that can be lethal and cause significant
economic losses, because H. gallinarum is a vector
species for this pathogen. Birds reared under
improper space conditions are at higher risk of
infection by these parasites (Cupo & Beckstead,
2019).
Regarding the nematode lifecycle, non-embryonic
fertilized eggs are eliminated by the females in the
host's caecum and are passed with the feces.
Depending on environmental conditions
(temperature and soil), the larvae can develop
inside the egg (Saunders et al., 2000). These eggs
can remain infectious for several years until they
are ingested by a new definitive (birds), paratenic
or transport (earthworms - mainly Lumbricus
Linnaeus, 1758 and Eisenia Michaelsen, 1900 and
flies) hosts that may be consumed by the birds. The
oviposition by the fertilized adult females starts
between 24 up to 35 days.
Therefore, a better understanding and disclosure
the presence of the parasites in different birds from
Nematodes of the genus Heterakis Dujardin, 1845
are common and generalist parasites (Mendoça,
1953; Inglis, 1967; Cupo & Beckstead, 2019).
According to Vicente et al. (1993, 1995), 14
species of Heterakis were reported in different
Brazilian birds [(Heterakis alata Schneider, 1866;
Heterakis arquata (Schneider, 1866); Heterakis
brasiliana Linstow, 1899; Heterakis brevispiculum
Gendre 1911; Heterakis dispar (Schrank, 1790),
Heterakis gallinarum (Schrank, 1788), Heterakis
ibanezi (Freitas, Vicente & Santos, 1969);
Heterakis mackeruensis von Linstow, 1906;
Heterakis macabuensis Vicente & Santos, 1967;
Heterakos nattereri Travassos 1923; Heterakis
p s o p h i a e Tra vass os, 1913 ; He t e ra k i s
valdemucronata (Molin, 1860); Heterakis
spiculatus (Cobbold, 1861); and Heterakis inglisi
Vicente, Pinto & Noronha, 1993].
Heterakis gallinarum was registered in Gallus
gallus domesticus Linnaeus, 1758 in all regions of
Brazil, in addition to registers in other bird's
species in different locations in the country (Table
1).
There are also records of H. gallinarum infections
in other countries, mainly in poultry production
systems. The parasite was registered in Denmark,
Germany, and the United States of America
(Valadão, 2018). It is commonly found within the
caecum of captive birds (Madsen, 1950)
occasionally provoking bleeding in the intestinal
mucosa thus causing serious inconvenience for
breeders of slaughter birds, considering that severe
Brandão-Simões et al.
The present survey reports the occurrence of H.
gallinarum in a bird commercialized at the
metropolitan region of Vitoria, Espirito Santo,
Brazil.
other locations can promote prevention and
improve the morphological and evolutionary study
of the nematode.
201
Table 1. Species of birds reported with Heterakis gallinarum in different localities of Brazil.
Bird species
Common name
Regions
Cairina moschata domesticus
(Donkin, 1989)
Muscovy ducks Southeast: MG
Mid West: DF
Chrysolophus pictus
(Linnaeus,
1758)
Golden pheasant Southeast: SP
Crypturellus noctivagus
(Wied,
1820)
Yellow-legged tinamou Southeast: ES
Crypturellus undulates
(Temminck, 1815)
Undulated tinamou Southeast:
MG
Mid West: MT
Crypturellus variegatus
(Gmelin,
1789)
Variegated tinamou Southeast: ES
Meleagris gallopavo
Linnaeus, 1758
Wild turkey Southeast: MG
Mid West: DF
South: PR, RS
Nothura maculosa
(Temminck, 1815)
Spotted nothura Southeast: SP
Numida meleagris
(Linnaeus, 1758)
Helmeted guineafowl North: RO
South: RS
Pavo cristatus
Linnaeus,
1758
Indian peafowl Southeast: SP
Mid West: GO
Phasianus colchicus
Linnaeus,
1758
Common pheasant Southeast: SP
Rhynchotus rufescens
(Temminck, 1815)
Red-winged tinamou Southeast: SP
Tinamus solitaries
(Vieillot, 1819)
Solitary tinamou Southeast: ES, RJ
North: PA
Source: Boroviec et al. (2020), Ramos et al. (2018), Vicente et al. (1993) and Vicente et al. (1995).
MATERIAL AND METHODS After clarification with Aman's lactophenol, the
nematodes were mounted on a microscope slide,
examined by a light microscope and their
morphological characters measured using TSView
6.1 (Tucsen Imaging Technology Co. Limited).
Drawings were made with CorelDraw® Home &
Student Suite X8. The identification of the
parasites was performed by using the taxonomic
keys proposed by Vicente et al. (1995) and
Anderson et al. (2009). The measurement units for
the structures are given in micrometers unless
otherwise specified. CHIOC 38924 a-b: Heterakis
gallinarum (male = a; female = b).
Ethis aspects: The authors declare no conflict of
interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation
A female of G. gallus domesticus acquired at the
metropolitan region of Vitoria, Espirito Santo, in
December 2019, was used for the study. After
cervical dislocation euthanasia followed by
exsanguination, as stated by the CFMV (2012),
digestive tract (which was separated into parts),
lungs, heart, kidneys, and liver were removed and
placed separately in Petri dishes containing 0.85%
saline.
E a c h o r g a n w a s i n s p e c t e d u s i n g a
stereomicroscope. The existing nematodes were
collected, fixed in 10% hot formalin, and later
transferred to 70% ethanol.
Neotropical Helminthology, 2020, 14(2), jul-dic Heterakis gallinarum in Gallus gallus domesticus
Ascaris gallinae Gmelin, 1790
Heterakis gallinae Gmelin, 1970
Ascaris vesicularis Froelich, 1791
Heterakis vesicularis Dujardin, 1845
Heterakis papilosa Railliet, 1885.
Male: (N=3) Length 6.64 mm (5.48–7.28) by
308.08 (403.90–251.65) wide. Pharynx 54.75
(51.87–57.62) long. Nerve ring 210.10
(160.35–293.64) and excretory pore 365.64
(319.36–411.93) from cephalic apex. Esophagus
681.84 (585.07–739.72) long and bulb 186.06
(178.40–190.29) long by 182.76 (159.52–197.48)
wide. Present caudal alae, 368.70 (191.10–472.44)
long by 161.84 (87.66–200.32) wide. Precloacal
chitinous-rimmed sucker (Fig. 1, 2) 56.42
(34.11–70.99) long by 36.08 (31.42–38.95) wide,
located 185.71 (111.98–231.81) from the cloaca
and 689.27 (650.84–712.93) from the posterior
end. Unequal spicules (Fig. 1), larger 1.41 mm
( 0 . 9 7 5 – 2 . 0 8 0 ) , a n d s m a l l e r 6 2 5 . 3 9
(472.35–784.45) long. Eleven pairs of caudal
papillae present and 2 unpaired: 2 pairs aside of the
sucker; 1 sessile and 1 pedunculated pairs of
precloacal papillae; 3 pedunculated and 1 sessile
pairs of adcloacal papillae; 2 pedunculated and 1
sessile pairs plus 2 unpaired postcloacal papillae
(Fig. 2). Slender tail with a pointed tip 227.40
(169.08–262.34) long (Fig. 1, 2).
of data; in the writing of the manuscript, or in the
decision to publish the results. The experimental
procedures were conducted in accordance to
institutional ethical guidelines.
Six specimens of nematodes (3 females and 3
males) found in the caecum of G. gallus domesticus
from Vitoria, Espirito Santo, Brazil were identified
as H. gallinarum.
Heterakis gallinarum (Schrank, 1788) Madsen,
1949
Diagnosis general. Robust body, whitish color,
transversal ridges. Cephalic end with 3 round lips
not connected by lateral lobes. Interlabia and labial
tooth absent. One cephalic papilla on each lip.
Esophagus relatively long, with a posterior bulb
with a valve. Males shorter than females.
Precloacal chitinous-rimmed sucker, caudal alae
can be found together ventrally. The tail has short
pedunculated and sessile papillae in pairs. Spicules
unequal in size, similar in shape. Vulva near to half
body. Uterus anfidelphic and didelphic.
Synonymies
Ascaris gallinarus Schrank, 1788
RESULTS
202
Figure 1. Heterakis gallinarum, male. Posterior end: spicules.
Neotropical Helminthology, 2020, 14(2), jul-dic Brandão-Simões et al.
opening 4.14 mm (1.99–5.64) from anterior end
(Fig. 4A, 4B). Muscular and robust ovijector,
divided in two, larger 741.27 (947.01–535.54) long
and smaller 279.85 (133.90–425.80) long (Fig.
4B). Ellipsoidal, unembryonated, but different
stages are observed, 101.17 (36.51–145.80) long
by 59.25 (22.85–83.43) wide. Few pigmented
eggs. Slender tail 0.9 mm (0.44–1.19) long.
Female: (N=3) Length 10.17 mm (9.31–10.92) by
392.62 (325.88–452) wide (Fig. 3, 4A). Pharynx
49.62 (34.92–73.54) (Fig. 3) long. Nerve ring and
excretory pore located (Fig. 3) 212.42
(151.57–287.51) and 489.30 (419.31–530.50)
from anterior end, respectively. Esophagus (Fig. 3,
4A) 770.74 (704.42–854.10) long and robust bulb
263.90 (232.24–290.55) long by 237.59
(222.98–261.48) wide (Fig. 3, 4A). Simple vulvar
203
Figure 2. Heterakis gallinarum, male. Posterior end, ventral view. pcr: precloacal chitinous-rimmed sucker; es: spicules
(terminal portion); pre: precloacal papillae; ad: adcloacal papillae; pos: postcloacal papillae; clo: cloaca.
Figure 3. Heterakis gallinarum, female anterior portion, ventral view.
Neotropical Helminthology, 2020, 14(2), jul-dic Heterakis gallinarum in Gallus gallus domesticus
1923) has a greater amount of postcloacal papillae
(8 pairs) and a shorter distance from the sucker to
the anus (42 µm x 689.27 µm).
Another taxonomic characteristic observed in
Heterakis which can be used while identifying
species is the s-shaped curvature of the larger
spicule at the end of the cloaca (Madsen, 1949,
1950), as observed in H. gallinarum (Fig. 1), but
not found in Heterakis isolonche (Ramos et al.,
1953) nor Heterakis dispar (Cupo & Beckstead,
2019). The species also show differences in spicule
sizes, about 0.99 / 2.20 mm in H. isolonche and
0.55 / 0.73 mm in H. dispar, compared to the 1,410
/ 0.625 mm of H. gallinarum.
Furthermore, it was found that the females had
eggs at different stages of development, but no
larvae. These findings corroborate by Saunders et
al. (2000) that H. gallinarum eliminates non-
embryonic eggs in the external environment, where
the larvae development occurs.
The authors would like to thank Yasmin Madureira
and Blima Fux for review this text; to the staff and
In this study, the identification of the parasite was
performed by morphological comparison,
considering that molecular analysis using
mitochondrial sequences that could assist in the
process of identifying the species and building a
Heterakis phylogeny is not well established (Wang
et al., 2016; Cupo & Beckstead, 2019).
In the current paper, the specimens analyzed,
present the general characteristics described for the
species, such as bulb length and position, presence
and positioning of the precloacal sucker, spicules
size, and caudal papillae projection in caudal alae.
The comparison of spicule structures and lengths,
the position and number of caudal papillae, the
relative length of sucker in relation to the cloacal
aperture, and the length of the tail in the male are
suitable taxonomic characters to differentiate
species within the genus Heterakis (Iglis, 1967).
Under this criterion, the species found differs from
H. ibanezi (Freitas et al., 1969) by the arrangement
of the papillae, which presents 2 pairs of adcloacal
papillae and 6 postcloacal papillae, while the
specimen analyzed by this study displays twice as
many papillae. Besides, H. nattereri (Travassos,
DISCUSSION
204
A B
Figure 4. Heterakis gallinarum, female. A. Vulvar opening (arrow) and ovijectors B. Vulva and ovijector: detail.
ACKNOWLEDGMENTS
Neotropical Helminthology, 2020, 14(2), jul-dic Brandão-Simões et al.
trainees of the Laboratório de Helmintologia
Animal of Universidade Federal do Espírito Santo
and Laboratório de Biologia de Trematoda of
Universidade Federal de Minas Gerais for the help
in some the procedures. This research was funded
by Conselho Nacional de Desenvolvimento
Cientifico e Tecnológico, CNPq and for Research
Scholarship (ALM), and, in part, by the Fundação
de Amparo à Pesquisa do Estado de Minas Gerais
(Minas Gerais' Research Support Foundation)
(FAPEMIG) and for Scholarship (MBS).
205
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