image/svg+xml
ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2021, 15(2), jul-dic:139-148.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
1
Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro-UFRRJ. Seropédica, RJ- Brasil
*Corresponding author: raquel83vet@gmail.com
Raquel de Oliveira Simões: https://orcid.org/0000-0001-5130-3341
Valéria da Silva Carneiro: https://orcid.org/0000-0003-4682-9431
José Luis Luque: https://orcid.org/0000-0003-3515-1127
1*1 1
Raquel de Oliveira Simões; Valéria da Silva Carneiro& José Luis Luque
ABSTRACT
Keywords:
birds – Cestoda – Nematoda –
parasite ecology – prevalence – parasite richness
The domestic chicken,
Gallus gallus domesticus
Linnaeus, 1758, is an important component of the
agribusiness segment, and Brazil is one of the world's largest broiler producers and exporters. The present
study aimed to characterize the composition and structure of the helminth community of backyard
chickens,
G. g. domesticus
,
in Seropédica, Rio de Janeiro, Brazil. Fifty-five adult chickens were studied.
The overall helminth species richness was 12. The nematodes
Capillaria
sp. and
Heterakis gallinarum
(Schrank, 1788),
recovered from small intestine and cecum, respectively, presented the highest
prevalence and mean abundance. In addition, these species presented the highest values of frequency of
dominance. The helminth species
Amoebotaenia cuneata
(von Linstow, 1872)
– Raillietina tetragona
(Molin, 1958)
;
and
Davainea proglottina
(Davaine, 1860) –
A. cuneata
;
and
H. gallinarum – Capillaria
sp. showed significant positive correlation between their abundance and prevalence.
Gongylonema
ingluvicola
Ransom, 1904 and
H. gallinarum
showed significant correlation between host sex and
helminth abundance, while there was no correlation between host sex and helminth prevalence. The
knowledge of helminth community structure in free-range chickens is important to adopt better measures
for control and prevention of helminth infections.
Neotropical Helminthology
139
doi:10.24039/rnh20211521196
HELMINTH COMMUNITY OF BACKYARD CHICKENS (
GALLUS GALLUS DOMESTICUS
LINNAEUS, 1758)
IN SEROPÉDICA, RIO DE JANEIRO, BRAZIL
COMUNIDADE DE HELMINTOS DE FRANGOS DE QUINTAL
(GALLUS GALLUS DOMESTICUS
LINNAEUS, 1758)
EM SEROPÉDICA, RIO DE JANEIRO, BRASIL
COMUNIDAD DE HELMINTOS DE POLLOS CASEROS (
GALLUS GALLUS DOMESTICUS
LINNAEUS, 1758) EN SEROPÉDICA, RIO DE JANEIRO, BRASIL
D
D
D
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140
RESUMO
Palavras-chaves:
aves – Cestoda – Nematoda – ecologia parasitária – prevalência – riqueza parasitaria
As galinhas domésticas
Gallus gallus
domesticus
Linnaeus, 1758, são um importante componente do
segmento do agronegócio, e o Brasil é um dos maiores produtores e exportadores de frangos de corte. O
presente estudo teve como objetivo caracterizar a estrutura da comunidade componente de helmintos de
galinhas de fundo de quintal,
G. g. domesticu
s, em Seropédica, Rio de Janeiro, Brasil. Foram estudados 55
frangos adultos. A riqueza total de helmintos foi de 12 espécies. Os nematoides
Capillaria
sp. e
Heterakis
gallinarum
(Schrank, 1788),
encontrados no intestino delgado e ceco, respectivamente, foram as espécies
mais prevalentes e com maior abundância média e foram consideradas espécies centrais. Além disso,
essas espécies apresentaram alta frequência de dominância e dominância relativa média. Os pares de
espécies de helmintos
Amoebotaenia cuneata
(von Linstow, 1872) -
Raillietina tetragona
(Molin, 1958);
Davainea proglottina
(Davaine, 1860) -
A. cuneata
e
H. gallinarum
-
Capillaria
sp. mostraram correlação
positiva significativa entre abundância média e prevalência parasitária.
Gongylonema ingluvicola
Ransom, 1904
and
H. gallinarum
mostraram correlação significativa entre sexo do hospedeiro e
abundância de helminto, enquanto que não houve correlação no sexo do hospedeiro e a prevalência destes.
O conhecimento da estrutura da comunidade de helmintos em frangos criados no quintal é importante para
a adoção de medidas de controle e prevenção de helmintos.
Neotropical Helminthology, 2021, 15(2), jul-dic
Simões
et al.
RESUMEN
Palabras clave:
aves – Cestoda – Nematoda – ecología parasitaria – prevalência – riqueza parasitaria
Las gallinas domésticas,
Gallus gallus domesticus
Linnaeus, 1758
,
son un componente importante del
segmento de la agroindustria y Brasil es uno de los mayores productores y exportadores de pollos. El
presente estudio tuvo como objetivo caracterizar la estructura comunitaria de helmintos de pollos criados
en corrales,
G. g. domesticus
, en Seropédica, Rio de Janeiro, Brasil. Se estudiaron 55 aves adultas. La
riqueza total de helmintos fue de 12 especies.
Capillaria
sp. y
Heterakis gallinarum
(Schrank, 1788),
que
se encontraron en el intestino delgado y ciego intestinal, respectivamente, fueron las especies más
prevalentes con mayor abundancia promedio y fueron consideradas especies centrales. Además, estas
especies mostraron los valores mayores de frecuencia de dominancia y de dominancia relativa media. Los
pares de especies de helmintos,
Amoebotaenia cuneata
(von Linstow, 1872)
- Raillietina tetragona
(Molin, 1958);
Davainea proglottina
(Davaine, 1860)
- A. cuneata
y
H. gallinarum - Capillaria
sp.
mostraron una correlación positiva significativa entre la abundancia media y la prevalencia de parásitos.
Gongylonema ingluvicola
Ransom, 1904 y
H. gallinarum
mostraron una correlación significativa entre el
sexo del huésped y la abundancia de helmintos, mientras que no hubo correlación entre el sexo del
huésped y la prevalencia de helmintos. El conocimiento de la estructura de la comunidad de helmintos en
los pollos criados en corrales es importante para la adopción de medidas de prevención y control de
helmintos.
The domestic chicken,
Gallus gallus domesticus
Linnaeus
,
1758, is an important component of the
agribusiness segment, and Brazil is one of the
world's largest broiler producers and exporters
INTRODUCTION
(ABPA, 2020). There is high demand for chicken
meat and eggs due to high nutritional value and
affordable price (Geraldo
et al
., 2020). In the past
decade, the market of organic, healthy, and
sustainable products and contingent of consumers
concerned about animal welfare have both
increased (Miao
et al.
, 2005; Alsaffar, 2016).
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Chickens under free-range production typically
show signs of calmness and comfort (Bogdanov,
1997). However, chickens reared freely are more
exposed to helminths than those kept in
confinement (Cardozo & Yamamura, 2004;
Lozano
et al.
, 2019), since they have direct contact
with soil, and free access to different areas and food
items (Gomes
et al.
, 2009). A high burden of
gastrointestinal helminths can decrease
productivity by increasing mortality, causing
economic losses to breeders (Ruff, 1999).
In Brazil, many studies have reported the
occurrence of helminths in
G. g. domesticus
in
different regions and breeding systems (Grisi &
Cravalho, 1974; Quadros
et al.
, 2015; Silva
et al.
,
2016; Silva
et al.
, 2018; Brandão-Simões
et al
.,
2020). However, little is known about the helminth
community structure of
G. g. domesticus
in this
condition (Silva
et al.
, 2016, 2018). Studies of
parasites through an ecological approach, to detect
possible patterns in the organization and
composition of parasite populations, can be
relevant to understand the distribution of the
pathogen species in different breeding systems.
Moreover, it can assist helminthic control
strategies and contribute to develop biosafety
programs. Here, we characterize the composition
and structure of the helminth component
community of backyard chickens
in Seropédica,
Rio de Janeiro, Brazil.
Host and parasitological procedures
Fifty-five sexually mature
G. g. domesticus
were
purchased dead during 1999-2000. The study was
carried out in Seropédica (22° 44′ 29″S, 43° 42′
19″W), state of Rio de Janeiro, Brazil. The
chickens were subjected to procedures in
accordance with standard international
parasitological guidelines (Yazwinski
et al.
, 2003).
The gastrointestinal tract, eyeball, trachea, lungs,
kidneys, and bursa of Fabricius were examined.
The helminths were washed in saline solution
(0.85% NaCl) and fixed in AFA (2% acetic acid,
3% formaldehyde and 95% ethanol). For
microscopic studies, nematodes were cleared in
lactophenol and cestodes were stained with
chlorhydric carmine. The helminth parasites were
identified according to Yamaguti (1961), Khalil
et
al.
(1994), Vicente
et al.
(1995) and Shmidt (1986),
along with specific papers.
Data analysis
To analyze the helminth community structure, we
considered prevalence, mean intensity and mean
abundance of each species using the procedures
described by Bush et al. (1997). Statistical analyses
were performed only for the parasite species with
prevalence higher than 10%.
The frequency of dominance and the Berger-Parker
index of each parasite species were calculated
according to Rohde
et al.
(1995) and Magurran
(2004).
Species richness, helminth richness at the
infracommunity level and Brillouin's diversity
index (log10) were calculated. The parasite
infracommunity species were classified as: a)
central species (present in more than one-third of
the hosts); b) secondary species (present in one- to
two-thirds of the hosts); and c) satellite species
(present in less than a third of the hosts) (Bush &
Holmes, 1986).
Mann-Whitney
U
test values and chi-square
analysis were used for comparison of parasite
abundance and prevalence, respectively, and
between host sex (Zar, 1999). These analyses were
performed following the recommendations of
Wilkinson (1990) using the SYSTAT™ statistical
software.
The possible relationships between prevalence and
abundance between pairs of concurrent species
were determined using the chi-square test and
Spearman rank correlation coefficient,
respectively (Ludwig & Reynolds, 1988).
Statistical significance was considered at
P
< 0.05.
All ecological terminology was used according to
Bush
et al.
(1997).
Ethic aspects
All national and institutional guidelines for use of
animals were followed. All chickens were
purchased died.
141
MATERIALES AND METHODS
Helminth community of backyard chickens
Neotropical Helminthology, 2021, 15(2), jul-dic
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142
The overall helminth richness was 12 species. The
helminth richness at the infracommunity level
ranged of 1 to 10, with a mean of 5.2 ± 2.2. Fifty-
three hosts (96%) presented two or more helminth
species.
A total of 10,708 specimens were collected, with
mean abundance of 194.7 ± 283.9. Nematodes
were the most abundant, with 7 species
representing 60.7% of all parasite specimens
collected. All chickens examined were parasitized
by at least one species of nematode and 85.7% (47)
were parasitized by cestodes. Trematodes were not
found. The nematode
Capillaria
Zeder, 1800 was
not identified to the species level as cestode
Raillietina
Fuhrmann, 1920 due to the low quality
of the morphological characteristics, such as scolex
and mature proglottids, of the specimens collected.
RESULTS
The nematodes
Capillaria
sp. and
Heterakis
gallinarum
(Schrank, 1788), recovered from the
small intestine and cecum, respectively, presented
the highest values of prevalence and mean
abundance and were considered central species
(Table 1). In addition, these species presented the
highest values of frequency of dominance and
Berger-Parker index (Table 2); while the cestode
Raillietina
sp. presented the highest value of mean
intensity and was considered a secondary species
along with the cestode
Amoebotaenia cuneata
(von
Linstow, 1872) and the nematodes
Gongylonema
ingluvicola
Ransom, 1904
and
Oxyspirura
mansoni
. (Cobbold, 1879) (Table 2). Secondary
species were found in the small intestine, crop and
eye.
Tetrameres confusa
Travassos, 1917
showed
the lowest values of prevalence, mean intensity and
abundance
(Table 1). The Brillouin index for
helminth infracommunities had mean value of 0.43
± 0.19 and maximum diversity of 0.78.
Simões
et al.
Table 1.
Prevalence (P), mean intensity (MI), and mean abundance (MA) followed by standard error, community
status (CS) and site of infection (SI) of helminth parasites of
Gallus gallus. domesticus
from Seropédica, Rio de
Janeiro, Brazil.
Helminth species
P (%)
MI
MA
CS
*
SI
CESTODA
Amoebotaenia cuneata
41
.
8
45
.
4
+
99
.
9
19
.
0
+
67
.
6
S
Small Intestine
Davainea
proglottina
30
.
9
37
.
2
+
53
.
0
11
.
5
+
33
.
7
Sa
Small Intestine
Raillietina tetragona
32
.
3
16
.
5
+
29
.
2
5
.
4
+
18
.
2
Sa
Small Intestine
Raillietina echinobothrida
27
.
3
17
.
5
+
22
.
4
4
.
8
+
13
.
9
Sa
Small Intestine
Raillietina
sp.
43
.
6
81
.
9
+
253
.
3
35
.
7
+
170
.
3
S
Small
Intestine
NEMATODA
Ascaridia galli
21
.
8
37
.
6
+
65
.
7
8
.
2
+
33
.
6
Sa
Small Intestine
Capillaria
sp.
90
.
9
46
.
0
+
83
.
7
41
.
8
+
80
.
9
C
Small
Intestine
Cheilospirura hamulosa
25
.
4
8
.
9
+
13
.
2
2
.
2
+
7
.
6
Sa
Ventricle
Gongylonema ingluvicola
49
.
1
7
.
0
+
8
.
2
3
.
4
+
6
.
7
S
Crop
Heterakis gallinarum
72
.
7
63
.
1
+
122
.
8
45
.
9
+
108
.
1
C
Cecum
Oxyspirura mansoni
56
.
4
27
.
7
+
36
.
2
15
.
6
+
30
.
4
S
Eye
Tetrameres confusa
23
.
6
4
.
1
+
4
.
4
1
.
0
+
2
.
7
Sa
Proventriculum
* Central species (C). Secondary species (S) and Satellite species (Sa).
Neotropical Helminthology, 2021, 15(2), jul-dic
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143
Table 2.
Frequency of dominance and Berger Parker Index values (BPI) of the helminth species from
Gallus gallus
domesticus
in the municipality of Seropédica. Rio de Janeiro, Brazil.
Helminth species
Frequency of dominance
BPI
CESTODA
Amoebotaenia
cuneata
5
0.08
+
0.1
6
Davainea proglottina
2
0.05
+
0.12
Raillietina tetragona
2
0.0
4
+
0.
10
Raillietina echinobothrida
3
0.04
+
0.1
4
Raillietina
sp.
7
0.1
2
+
0.24
NEMATODA
Ascaridia galli
1
0.02
+
0.09
Capillaria
sp
.
13
0.25
+
0.2
2
Cheilospirura
hamulosa
0
0.01
+
0.03
Gongylonema ingluvicola
0
0.0
3
+
0.06
Heterakis gallinarum
15
0.2
3
+
0.2
4
Oxyspirura mansoni
7
0.12
+
0.21
Tetrameres confusa
0
0.0
1
+
0.03
2
Table 3.
Mann-Whitney
U
test values (Z, value of the normal U test approximation) and Chi square () to evaluate the
relationship between the sex of
Gallus domesticus
and the abundance and prevalence of the components of its
parasitic community (
P
= level of significance).
Helm
inth species
Z
P
c
2
P
CESTODA
Amoebotaenia cuneata
-
0.1
8
0.8
6
0.15
0.
70
Davainea proglottina
-
0.7
2
0.47
0.02
0.89
Raillietina tetragona
-
0.3
7
0.71
0.02
0.89
Raillietina echinobothrida
-
1.53
0.1
3
0.23
0.63
Raillietina
sp.
-
0.4
7
0.6
4
0.09
0.76
NEMATODA
Ascaridia galli
-
0.26
0.79
0.22
0.64
Capillaria
sp.
-
1.8
5
0.06
0.01
0.94
Cheilospirura hamulosa
-
0.7
1
0.4
8
0.06
0.8
1
Gongylonema ingluvicola
-
2.1
1
*
0.0
4
0.96
0.3
3
Heterakis gallinarum
-
2.01
*
0.04
0.02
0.8
9
Oxyspirura mansoni
-
1.4
1
0.1
6
0.09
0.76
Tetrameres confusa
-
0.8
5
0.
40
0.12
0.7
3
*Significant Value
Helminth community of backyard chickens
Neotropical Helminthology, 2021, 15(2), jul-dic
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144
Gongylonema ingluvicula
and
H. gallinarum
showed significant correlation between host sex
and helminth abundance, while there was no
correlation between host sex and helminths
prevalence (Table 3).
The following pairs of concurrent helminths
showed significant positive correlation between
their abundance and prevalence, respectively:
Amoebotaenia cuneata – Raillietina tetragona
2
(Molin, 1858)
(
rs
= 0.37;
P
= 0.006/= 8.59;
P
=
0.004),
Davainea proglottina
(Davaine, 1860)
–
A.
2
cuneata
(
rs
= 0.46;
P
< 0.001/= 3.53;
P
= 0.049);
and
H. gallinarum – Capillaria
sp. (
r
= 0.39;
P
=
s
2
0.003/= 5.6;
P
= 0.024). The pair
R. tetragona
–
Ascaridia galli
showed significant correlation only
2
between abundance (
r
= 0.37;
P
= 0.005/= 2.22;
s
P
= 0.136).
Several studies of the characteristics of the
helminth communities of
G. g. domesticus
have
been performed worldwide (Schou
et al.
, 2007;
Idika
et al
., 2016; Slimane, 2016; Berhe
et al.
,
2019; Sarba
et al
., 2019, among others). In Brazil,
most studies have focused only on the description
of the helminth fauna (Costa & Freitas, 1959; Grisi
& Carvalho, 1974; Gomes
et al.
, 2009; Siqueira &
Marques, 2016). More recently, knowledge about
the helminth community structure of chickens
raised in different production systems has
increased, mainly in the state of São Paulo (Silva
et
al.
, 2016; 2018). In contrast, there are few reports
of the helminth community structure of
G. g.
domesticus
in the state of Rio de Janeiro (Grisi &
Carvalho, 1974; Gomes
et al.
, 2009). The
composition and structure of the helminth
community of a specific host population
correspond to a pool of available parasite species in
a specific locality. Moreover, the structure and
composition of a helminth community can vary
due to biotic and abiotic factors, such as
environmental changes, parasite control, host
behavior and age, among others (Poulin, 2007;
Santoro
et al.
, 2012; Simões
et al.
, 2016; Cardoso
et al.
, 2019).
Grisi & Cravalho (1974) reported 13 species of
helminths in
G. g. domesticus
in Seropédica,
DISCUSSION
similar to the present study, in which we found 12
species in the same locality. However, some
species differed between the studies. The species
Syngamus trachea
(Montagu, 1811)
, Heterakis
brevispiculum
Gendre, 1911,
Capillaria collaris
(Linstow, 1873)
and
C. obsignata
Madsen, 1945
were not found in our study, although we found
nematodes belonging to the genus
Capillaria.
Unfortunately, the specific identification was not
possible. Moreover, we collected two species of
cestodes (
Davainea proglottina
and
Amoebotaenia
cuneata
) that were not reported by Grisi &
Carvalho (1974). Neither study found trematodes.
In contrast, Silva
et al.
(2016, 2018) reported
trematodes in different regions of São Paulo state.
These differences have also been observed in
chickens from African and Asian countries (Berhe
et al.
, 2019; Chege
et al.
, 2015; Junaidu
et al.
,
2014; Schou
et al.
, 2007). Additionally, nematodes
and cestodes have been reported with more
frequency than trematodes in the component
helminth community in chickens by many
researchers around the world (Sarba
et al.
, 2019;
Idika
et al
., 2016; Slimane, 2016; Hussen
et al.
,
2012). Variation in environmental conditions can
favor or disfavor the presence of intermediate hosts
responsible for cestode and trematode transmission
and can also influence the occurrence of these
species in the helminth community of the definitive
host.
In the present study, all chickens were infected with
the nematodes
H. gallinarum
and
Capillaria
sp.,
and both were the more prevalent (central species),
with high frequency of dominance and mean
values of Berger-Parker index in the helminth
community. Similar findings were also observed
by Gomes
et al.
(2009), Siqueira & Marques (2016)
and Silva
et al.
(2018) in chickens reared in
extensive, semi-intensive and/or intensive
systems. Parasites with a direct life cycle have a
higher probability of infecting definitive hosts
since there is no intermediate host. In addition, the
high fertility of these female nematodes increases
the likelihood of host infection due to more eggs
eliminated in the environment. The chickens in the
present study were raised free outdoors and
allowed to find food by foraging in the surface soil
layer. Thus, these factors can partly explain the
high prevalence of nematodes in the helminth
community.
Simões
et al.
Neotropical Helminthology, 2021, 15(2), jul-dic
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145
The influence of host sex on the helminth
abundance has been observed in different helminth
community structures (Simões
et al.
, 2014; Wendt
et al.
, 2018). The influence of female chickens was
observed regarding two nematodes species (
H.
gallinarum
and
Capillaria
sp.). However, this
result must be viewed with caution, since the
proportion of female chickens used in the study
was much greater than of males (10: 1). In addition,
many studies of the helminth community of
G. g.
domesticus
have not reported significant
differences in helminth infection rate between male
and female animals (Poulsen
et al.
, 2000;
Abdelqader
et al.
, 2008; Ebrahimi
et al.
, 2014).
The positive correlation of abundance and
prevalence between pairs of cestodes and
nematodes may be related to the similarities of their
life cycle. The cestodes
R. tetragona
,
A. cuneata
and
D. proglottina
need an intermediate host, such
as an ant, beetle or fly; earthworm; and slug
respectively (Acha & Szyfres, 2003; Taylor
et al.
,
2017). One of the food items collected by the
chicken was small animals found in the soil.
Similarly, this can explain the positive correlation
with nematodes, which have a direct life cycle and
oral infection.
Free-range chickens are exposed to more parasites
than those reared in intensive systems (Ruff, 1999;
Lozano
et al.
, 2019) due to the direct contact with
soil and intermediate hosts. Tapeworms are
frequently encountered in the chickens in these
production systems and most species cause low
pathogenicity (Ruff, 1999). However,
R. tetragona
and
D. proglottina
are more
pathogenic, reducing
the performance of parasitized animals (Ruff,
1999; Nnadi & George, 2010). Moreover,
parasitism by
Capillaria
spp. can also cause
production losses (Ruff, 1999). Seasonality and
other collection areas should be considered in
future studies to measure the heterogeneity and
stability of the parasite helminth community.
Knowledge of the helminth community structure in
backyard chickens can be relevant to allow
breeders to adopt better measures for control and
prevention of helminths. Moreover, other variables
like climate conditions, hygiene, age, and animal
density should also be considered since they may
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