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New species of
Urocleidoides
Neotropical Helminthology (Lima). Vol. 17, N
º
2, jul - dic 2023
Neotropical Helminthology
Neotropical Helminthology, 2023, vol. 17 (2), 117-124
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
OCCURRENCE OF
CONTRACAECUM PELAGICUM
(JOHNSTON & MAWSON
1942) (NEMATODA: ANISAKIDAE) IN MAGELLANIC PENGUIN (
SPHENISCUS
MAGELLANICUS
(FORSTER, 1837)) COLLECTED FROM NORTHEAST BRAZIL,
WITH AN UPDATE ON ITS DISTRIBUTION IN THE COUNTRY
PRESENCIA DE
CONTRACAECUM PELAGICUM
(JOHNSTON & MAWSON 1942)
(NEMATODA: ANISAKIDAE) EN EL PINGÜINO MAGALLÁNICO (
SPHENISCUS
MAGELLANICUS
(FORSTER, 1837)) RECOLECTADO DEL NORESTE DE BRASIL,
CON ACTUALIZACIÓN DE SU DISTRIBUCIÓN EN EL PAÍS
OCORRÊNCIA DE
CONTRACAECUMPELAGICUM
(JOHNSTON & MAWSON
1942) (NEMATODA: ANISAKIDAE) EM PINGUIM-DE-MAGALHÃES (
SPHENISCUS
MAGELLANICUS
(FORSTER, 1837)) COLETADO DO NORDESTE DO BRASIL,
COM ATUALIZAÇÃO DE SUA DISTRIBUIÇÃO NO PAÍS
André Mota Alves
1,2
, João Carlos Gomes Borges
3,4,5
, Jociery Einhardt Vergara Parente
3
, Weslania Souza Inacio
da Silva
2,6
, João Victor de Jesus
2,6
, Michelle Evangelista Soares
2,6
& Victor Fernando Santana Lima
1,2,6,7*
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.24039/rnh20231721598
Volume 17, Number 2 (jul - dec) 2023
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
1
Programa de Pós-graduação em Biologia Parasitária, Universidade Federal de Sergipe, São Cristóvão - SE, Brazil
2
Laboratório de Doenças Parasitárias dos Animais, Universidade Federal de Sergipe, Nossa Senhora da Glória - SE, Brazil.
3
Fundação Mamíferos Aquáticos. São Cristóvão, SE, Brazil. Guimarães Peixoto, Recife, PE, Brazil.
4
Programa de Pós-Graduação em Ecologia e Monitoramento Ambiental. Universidade Federal da Paraíba. Rio Tinto, PB,
Brazil.
5
Grupo de Pesquisa em Mamíferos Aquáticos Amazônicos. Instituto de Desenvolvimento Sustentável Mamirauá. Bexiga, Tefé,
AM, Brazil.
6
Departamento de Medicina Veterinária, Universidade Federal de Sergipe, Nossa Senhora da Glória- SE, Brazil.
7
Programa de Pós-graduação em Ciências Aplicadas a Saúde, Universidade Federal de Sergipe, Lagarto - SE, Brazil.
* Corresponding author victor.fslima@gmail.com
André Mota Alves:
https://orcid.org/0000-0002-9150-5287
João Carlos Gomes Borges:
https://orcid.org/0000-0002-0033-6781
Jociery Einhardt Vergara Parente:
https://orcid.org/0000-0002-7125-5874
Weslania Souza Inacio da Silva:
https://orcid.org/0000-0003-4393-544X
João Victor de Jesus:
https://orcid.org/0000-0001-8786-0713
Michelle Evangelista Soares:
https://orcid.org/0009-0000-3311-8484
Victor Fernando Santana Lima:
https://orcid.org/0000-0002-7255-0664
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et al.
ABSTRACT
Te study identifed
Contracaecum pelagicum
(Johnston & Mawson 1942) as a parasite found in
Sphenicus magellanicus
(Forster, 1837), and a low
sampling of infected hosts was observed, with a prevalence of 33.3%, average intensity
of 6/host, and mean abundance of 2±3.46. Tis occurrence is uncommon in the Northeast region of Brazil, where
previous records indicate a higher presence in the southern region of the country. Tis contributes to the understanding
of the geographic distribution of the parasite. Anisakids, such as
C. pelagicum
, have a complex life cycle involving
aquatic invertebrates, fshes, and seabirds. Te presence of this parasite may indicate ecological interactions in the marine
ecosystem of the region. It is important to report the discovery to relevant authorities and institutions to monitor and
control the presence of the parasite. Tese fndings are relevant to the health and conservation of seabirds and the study
of marine ecosystems in Northeast Brazil.
Keywords:
Anisakids – Aquatic vertebrates – Geographic distribution – Northeast Brazil – Waterbird
RESUMEN
El estudio identifcó a
Contracaecum pelagicum
(Johnston & Mawson 1942) como un parásito encontrado en
Sphenicus
magellanicus
(Forster, 1837), y se observó una baja muestra de hospedadores infectados, con una prevalencia del 33,3%,
intensidad media de 6/hospedador y abundancia media de 2±3,46. Esta ocurrencia es poco común en la región noreste
de Brasil, donde los registros anteriores indican una mayor presencia en la región sur del país. Esto contribuye a la
comprensión de la distribución geográfca del parásito. Los anisákidos, como
C. pelagicum
, tienen un ciclo de vida
complejo que involucra invertebrados acuáticos, peces y aves marinas. La presencia de este parásito puede indicar
interacciones ecológicas en el ecosistema marino de la región. Es importante informar el descubrimiento a las autoridades
e instituciones pertinentes para monitorear y controlar la presencia del parásito. Estos hallazgos son relevantes para la
salud y conservación de las aves marinas y el estudio de los ecosistemas marinos en el noreste de Brasil.
Palabras clave:
Anisáquidos – Vertebrados acuáticos – Distribución geográfca –Nordeste de Brasil – Aves acuáticas
RESUMO
O estudo identifcou
Contracaecum
pelagicum
(Johnston & Mawson 1942) como um parasita encontrado em
Sphenicus
magellanicus
(Forster, 1837), e foi observada uma baixa amostragem de hospedeiros infectados, com prevalência de
33,3%, intensidade média de 6/hospedeiro e abundância média de 2±3,46. Essa ocorrência é incomum na região
Nordeste do Brasil, onde registros anteriores indicam uma presença maior na região sul do país. Isso contribui para
a compreensão da distribuição geográfca do parasita. Anisakídeos, como o
C. pelagicum
, possuem um ciclo de vida
complexo envolvendo invertebrados aquáticos, peixes e aves marinhas. A presença desse parasita pode indicar interações
ecológicas no ecossistema marinho da região. É importante relatar a descoberta às autoridades e instituições relevantes
para monitorar e controlar a presença do parasita. Essas descobertas são relevantes para a saúde e conservação das aves
marinhas e o estudo dos ecossistemas marinhos no Nordeste do Brasil.
Palavras-chave:
Anisaquídeos – Vertebrados aquáticos – Distribuição geográfca – Nordeste do Brasil – Aves aquáticas
INTRODUCTION
Penguins are marine birds exclusive to the oceans that
have adapted their wings into fippers to suit their
aquatic lifestyle. All species are restricted to the southern
hemisphere. Tese birds are highly adapted to the marine
environment, undertaking long-distance migrations in
search of food and breeding sites. In Brazil, the most
frequently sighted species on the coast is the Magellanic
penguin -
Spheniscus magellanicus
(Forster, 1837), and
migrates from its breeding colonies in the Patagonia
region, by ocean currents, in search of abundant food on
the Brazilian continental shelf (ICMBio, 2010).
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Occurrence of
Contracaecum pelagicum
in magellanic penguin
Neotropical Helminthology (Lima). Vol. 17, N
º
2, jul - dic 2023
Magellanic penguins are marine birds that inhabit the
coasts of Chile, Argentina, and the Falkland Islands in
South America. Tey are excellent swimmers and during
the southern hemisphere winter, they move along marine
currents in search of prey such as fshes, cephalopods,
and crustaceans, albeit in smaller quantities. (Pinto
et al
.,
2007; Ederli
et al
., 2009; Prado
et al
., 2011; Borges
et al
.,
2014; Campos
et al
., 2015; Tamiasso
et al
., 2018).
In Brazil, the occurrence of Magellanic penguins shows
annual seasonality, with individuals staying in colonies
in southern South America from mid-September to
mid-April. Adult penguins then begin their migration
northward, utilizing the continental shelf (Putz
et al
.,
2007). Juveniles have a later migration, appearing in
June and remaining in Brazilian waters until November
(Petry & Fonseca 2002, Mäder
et al
., 2010), and they can
wander at sea for up to four years.
Contracaecum pelagicum
(Johnston & Mawson, 1942)
is an anisakid nematode that uses crustaceans and fshes
as intermediate hosts, and is found in its adult form
parasitizing the digestive tract of a variety of vertebrate
animals, including mammals and seabirds, with penguins
being among their defnitive hosts (Saad
et al
., 2012;
Santos
et al
., 2013).
In the case of Magellanic penguins, it is known that
this parasite can be detrimental to their health, causing
infammation, ulceration, and gastrointestinal lesions,
weakening their immune system and leaving the animal
vulnerable to predation and other diseases, which directly
impacts their survival (Yáñez
et al
., 2012; Campos
et al
.,
2013; Tamiasso
et al
., 2018).
Te occurrence of
C. pelagicum
has been reported in studies
throughout the country; however, there is no available
data on the occurrence of
C. pelagicum
in
S. magellanicus
in northeastern Brazil. Terefore, the present study aimed
to report the frst record for the region, contributing to
an update on the localities where the occurrence of this
parasite is known in the country for this penguin species.
MATERIAL AND METHODS
From July to August 2015, three juvenile specimens of
Magellanic penguin (
S.
magellanicus
) were found stranded
and dead in the coastal regions of the states of Bahia (two
specimens collected: -11.46359, -37.35242; -11.58831,
-37.43504) and Sergipe (one specimen collected:
-11.12005, -37.13713), specifcally in Mangue Seco and
Aracaju, respectively. Te specimens had an average length
of approximately 45 cm and weighed 4.0 kg.
All animals underwent necropsy, during which
gastrointestinal content was collected by technicians
from the Fundação Mamíferos Aquáticos (FMA). During
the analysis of the biological material, six nematodes were
visualized and collected from a single specimen of
S.
magellanicus
. Te parasites were then placed in Eppendorf
tubes with 70° ethyl alcohol and sent for identifcation
to the Laboratory of Animal Parasitic Diseases at the
Universidade Federal de Sergipe, Sertão campus.
For morphological identifcation, the nematodes were
clarifed in Lactophenol to facilitate the visualization
of their structures, and subsequently illustrated. Te
analyzed material is duly stored in the bank of biological
samples curated by the Aquatic Mammals Foundation.
Taxonomic classifcation was arranged, and illustrations
were made using a light microscope to aid in
morphological characterization. Te illustrations were
prepared and converted into vector images using GIMP
2.10.34 software. Te nematodes were morphologically
identifed according to Ederli
et al
. (2009), and, Borges
et al
. (2014).
All the research was carried out within ethical aspects,
being carried out in partnership with the Aquatic
Mammals Foundation (FMA). Te material of animal
origin referring to the carcasses of the penguins was
previously collected by the FMA, which has legal
permission to work in the collection and rescue of
stranded animals.
RESULTS AND DISCUSSION
Te parasite was identifed as
Contracaecum pelagicum
(Fig. 1) and showed a prevalence of 33.3%, mean
intensity of 6/host, and mean abundance of 2±3.46.
Te nematodes were identifed based on morphological
observations of adult forms under light microscopy,
which is detailed below:
Superfamily Ascaridoidea Baird, 1853
Family Anisakidae Railliet & Henry, 1912
Subfamily Anisakinae Chabaud, 1965
Genus
Contracaecum
Railliet & Henry, 1912
Species
Contracaecum pelagicum
Johnston & Mawson,
1942
Description of the Male: Nematodes clearly visible, easily
distinguishable from the gastrointestinal content, ranging
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from 1-2cm in length, reddish in color. Body transversely
striated, especially at the anterior and posterior ends.
Te anterior region has a cephalic collar with anteriorly
directed cuticular edges, with three well-developed lips,
one dorsal lip, and two ventrolateral lips with three
bifurcated triangular interlabia present (Fig. 1B). Deirids
not prominent. Inverted intestinal cecum, presence of
ventricular appendix, and posterior region ventrally
curved (Fig. 1A) with a conical caudal extremity (Fig.
1C) containing 25-31 pairs of pre-cloacal papillae, the
frst 18 proximal pairs being well visible. Tree pairs of
pre-cloacal papillae. Seven pairs of post-cloacal papillae: 2
large subventral para-cloacal pairs located side by side, 2
subventral pairs, 2 sublateral pairs, and 1 pair of phasmids
near the distal sublateral pair of papillae. Distal end of the
spicule tapered and pointed (Fig. 1D, arrow).
Figure 1.
Contracaecum pelagicum
collected from
Sphenicus magellanicus
in the northeastern coast of Brazil; A - morphotype
of the collected adult male, highlighting the intestinal cecum (ic) and the ventricular appendix (va); B - detail of the
anterior region with emphasis on the well-developed lips, highlighting one of the interlabia (il) and the excretory pore (ep);
C - Detail of the posterior region highlighting the tail and caudal papillae; D - Detail of the adult male spicules.
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Contracaecum pelagicum
in magellanic penguin
Neotropical Helminthology (Lima). Vol. 17, N
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Te occurrence of
C. pelagicum
in
S. magellanicus
is a
common phenomenon in Brazil, with several records
over the years (Table 1).
Table 1.
Records of
Contracaecum pelagicum
in
Sphenicus magellanicus
in Brazilian jurisdiction waters.
Location in BrazilReference
Baia de Guanabara, RJSantos (1984)
litoral de vitória, ESEderli
et al
. (2009)
Pedrinhas, Ilha Comprida, Costa Sul do estado de São Paulo, SPPadro
et al
. (2011)
Litoral norte de São Paulo, SPRezende
et al
. (2013)
Costa do Rio de Janeiro, RJCampos
et al
. (2013)
Rio de Janeiro, RJBorges
et al
. (2014)
Baixada litorânea do estado do Rio de janeiro, RJCampos
et al
. (2015)
Pontal do Paraná e Matinhos, costa do estado do Paraná, PRAltrão
et al
. (2017)
Pontal do Sul, Paraná, PRVahoni
et al
. (2018)
Costa do Espiriro Santo, ESTamiasso
et al
. (2018)
Litoral do Estado do Rio de Janeiro, RJMutzenbecher
et al
. (2022)
In the present study, the sampling was low, with only one
host infected by the nematode. However, despite previous
records, the data indicate that there are no documented
occurrences of
C. pelagicum
in
S. magellanicus
in the
northeastern region of Brazil. So far, fndings of this
parasite along the Brazilian coast have been more frequent
in the southern region of the country. Terefore, this
study represents the frst record of the presence of this
parasitic nematode in the northeastern coastal region,
contributing to updating the distribution of
C. pelagicum
in this host species along the Brazilian coast.
Anisakids are zoonotic, and in the environment, the
life cycle of these nematodes involves the participation
of aquatic invertebrates and fshes as intermediate hosts
in the food chain. Additionally, fshes play an additional
role as paratenic hosts, contributing to the dissemination
and amplifcation of infection until the parasite reaches a
defnitive host, such as piscivorous birds and mammals,
in which they reach the adult form (Bicudo
et al
., 2005;
Saad
et al
., 2012). Recent studies on the northeastern coast
of Brazil show a high presence of anisakid nematodes,
including larvae of the
Contracaecum
genus, although
they have shown lower prevalence compared to other taxa
of Anisakiidae (see Alves
et al
., 2020; dos Santos Ferreira
et al
., 2020).
Contracaecum pelagicum
is a nematode found parasitizing
various species of seabirds and appears to have a wide
geographic distribution, as it has already been described
in Australia occurring in the Black-browed albatross
(
Diomedea melanophris
Temmick, 1828) and other birds
such as the brown booby (
Sula leucogaster
Boddaert,
1783) (Silva
et al
., 2005). In Brazil, according to the data
presented in Table 1, the occurrence of this nematode
has been frequent in populations of
S. magellanicus
. Tis
diversity of birds as fnal hosts may indicate that this
nematode has low specifcity, requiring its defnitive host
to be only a piscivorous bird
.
Te occurrence of this species in northeastern Brazil can
be considered an interesting fnding for several reasons:
1- Geographic distribution: Te identifcation of
C. pelagicum
in northeastern Brazil may indicate an
expansion of the geographic distribution of this species. It
is possible that favorable environmental conditions have
allowed the parasite to establish itself in a new area.
2- Fauna monitoring: Te discovery of
C. pelagicum
may
be relevant for monitoring the health and well-being of
seabirds in northeastern Brazil. Tese parasites can cause
health problems in birds, such as intestinal infammation
and obstruction, afecting their reproduction and survival.
3- Marine ecosystem: Te presence of
C. pelagicum
may
indicate complex ecological interactions in the marine
ecosystem of the region. Te parasite typically infects fsh
and crustaceans, which serve as intermediate hosts, before
being consumed by seabirds. Tis can provide insights
into food chains and relationships between diferent
species in the area.
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It is important to report this occurrence to relevant
authorities and research institutions, such as animal health
agencies and marine fauna research institutes. Tese
experts will be able to further investigate the signifcance
of this discovery and take appropriate measures, if
necessary, to monitor and control the presence of the
parasite.
Te presence of
C. pelagicum
in northeastern Brazil can
indicate diferent scenarios. It is possible that this parasite
has been recently introduced to the region, possibly by
migratory birds that feed along the northeastern coast.
Another possibility is that the parasite was already present
but went unnoticed until now, with this being the frst
time it has been detected and reported. Te detection of
C. pelagicum
is important for understanding the health of
seabirds and the overall health of the marine ecosystem.
Additionally, it is relevant to monitor the presence of
this parasite, as it may have impacts on the conservation
and management of seabirds, especially those that are
considered endangered.
In conclusion, the analysis of available data and records
indicates that the occurrence of
C. pelagicum
in
S.
magellanicus
, the Magellanic penguin, in the northeastern
region of Brazil is an unprecedented event. Although this
parasite has been previously reported along the Brazilian
coast, fndings have been more common in the southern
region of the country. Terefore, this new occurrence
represents the frst record of the presence of
C. pelagicum
in the northeastern region, signifcantly contributing
to the understanding and updating of the geographic
distribution of this parasite in this host species along the
Brazilian coast. Tese fndings are of great importance
for monitoring the health and conservation of seabirds,
as well as for the study of marine ecosystems in the
northeastern region of Brazil.
ACKNOWLEDGMENTS
We appreciate the support of the Fundação Mamíferos
Aquáticos and Petrobras. SubRegional Program for
Stranding and Abnormal Activity Monitoring is
conducted by Petrobras, as a mitigating measure of the
Federal Environmental Licensing conducted by the
Brazilian Environmental Agency IBAMA. Te authors
are grateful to the Graduate Program in Ecology and
Environmental Monitoring, Federal University of
Paraíba. Te Projeto Viva o Peixe-Boi-Marinho of the
Aquatic Mammal Foundation, sponsored by Petrobras
through the Petrobras Socioenvironmental Program.
Author contributions
:
CRediT (Contributor Roles
Taxonomy)
AMA
= André Mota Alves
JCGB
= João Carlos Gomes Borges
JEVP
= Jociery Einhardt Vergara Parente
WSIS
= Weslania Souza Inacio da Silva
JVJ
= João Victor de Jesus
MES
= Michelle Evangelista Soares
VFSL
= Victor Fernando Santana Lima
Conceptualization
: AMA, VFSL
Data curation
: JCGB, JEVP
Formal Analysis
: AMA, JCGB, VFSL
Funding acquisition
: AMA, JCGB, JEVP, WSIS, JVJ,
MES, VFSL
Investigation
: AMA, WSIS, JVJ, MES
Methodology
: AMA, JCGB, VFSL
Project administration
: JCGB, VFSL
Resources
: AMA, JCGB, JEVP, WSIS, JVJ, MES, VFSL
Software
: AMA
Supervision
: JCGB, VFSL
Validation
: JCGB, JEVP, VFSL
Visualization
: AMA, JCGB, JEVP, WSIS, JVJ, MES,
VFSL
Writing – original draft
: AMA, VFSL
Writing – review & editing
: AMA, JCGB, JEVP, VFSL
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Contracaecum pelagicum
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BIBLIOGRAPHIC REFERENCES
Altrão, C.S., de Paula, A. A., Tavares, M., Ott, P. H., & Silva-Souza, Â. T. (2017). Population structure of the nematode
Contracaecum pelagicum
Johnston & Mawson, 1942 during the winter migration of the Magellanic penguin
Spheniscus magellanicus
(Forster, 1781) in southern Brazil.
Oecologia Australis
, 21, 62-71.
Alves, A.M., Souza, G.T.R., Takemoto, R.M., Melo, C.M., Madi, R.R., & Jeraldo, V.L.S. (2020). Anisakidae Skrjabin
& Karokhin, 1945 and Raphidascarididae Hartwich, 1954 nematodes in lutjanidae (Pisces: Perciformes) from the
Brazilian Northeast Coast.
Brazilian Journal of Biology, 80
, 255–265.
Bicudo, A.J.A., Tavares, L.E.R., & Luque, J.L. (2005). Larvas de Anisakidae (Nematoda: Ascaridoidea) parasitas da
cabrinha
Prionotus punctatus
(Bloch, 1793) (Osteichthyes: Triglidae) do litoral do estado do Rio de Janeiro, Brasil.
Revista Brasileira de Parasitologia Veterinária, 14
, 109-118.
Borges, J.N., Santos, H.L.C., Brandão, M.L., Santos, E.G.N., dos, Miranda, D.F. de, Balthazar, D.A., Luque, J.L., &
Santos, C.P. (2014). Molecular and morphological characterization of
Contracaecum pelagicum
(Nematoda)
parasitizing
Spheniscus magellanicus
(Chordata) from Brazilian waters.
Revista brasileira de parasitologia veterinária
,
23, 74–79.
Campos, S.D., Pereira, B.B.N., Siciliano, S., Costa, C.H.C., Almosny, N.R., & Brener, B. (2013).
Contracaecum
pelagicum
and
C. plagiaticium
(Nematoda: Anisakidae) infection in Magellanic penguins (Sphenisciformes:
Spheniscidae) on the coast of Rio de Janeiro State.
Pesquisa Veterinária Brasileira, 33
, 89-93.
Campos, S., Almosny, N.R., Siciliano, S., Costa, C.H., & Brener, B. (2015). Co-infecção e aspectos morfométricos de
Contracaecum pelagicum
(Nematoda: Anisakidae) e
Cardiocephaloides physalis
(Digenea: Strigeidae) em pinguim-
de-Magalhães na baixada litorânea do Rio de Janeiro.
Enciclopédia Biosfera, 11
, 1646-1652.
dos Santos Ferreira, A.P., Rojas, N.T., Queiroz, S.C., Vidal, L.G.P., Fonseca, F.T.B., da Silva Júnior, V.A., Luque, J.L., &
Oliveira, J.B. (2020).
Parasitic infestations and infections in marine fsh (Actinopterygii: Lutjanidae and Mullidae)
marketed in Brazil – an animal and human health issue
.
Archives of Veterinary Science, 25
, 66-79.
Ederli, N.B., Oliveira, F.C.R., Monteiro, C.M., Silveira, L.S., & Rodrigues, M.L.A. (2009). Ocorrência de
Contracaecum
pelagicum
Johnston & Mawson, 1942 (Nematoda, Anisakidae), em pinguim-de-magalhães (
Spheniscus magellanicus
Forster, 1781) (Aves, Spheniscidae) no litoral do Espírito Santo.
Arquivo Brasileiro de Medicina Veterinária e
Zootecnia, 61
, 1006-1008.
ICMBio. (2010).
Projeto Nacional de Monitoramento de Pinguim-de-Magalhães (Spheniscus magellanicus)
. 36 p.
Mäder, A., Sander, M., & Casa, J.R.G. (2010).
Ciclo sazonal de mortalidade do pinguim-de-magalhaes, Spheniscus
magellanicus infuenciado por fatores antrópicos e climáticos na costa do Rio Grande do Sul, Brasil
.
Revista Brasileira
de Ornitologia, 18
, 228-233.
Mutzenbecher, L., de Mattos Jr, D.G., dos Reis, M.G., & Barros, L.A. (2022). Helmintos em pinguins–de–magalhães
(
Spheniscus magellanicus
) resgatados no litoral do estado do Rio de Janeiro. PUBVET, 16, a1055.
Petry, M.V., & Fonseca, V.S. (2002).
Efects of human activities in the marine enviroment on seabirds along the coast of Rio
Grande do Sul, Brazil
.
Ornitología Neotropical, 13
, 137-142.
Pinto, M.B.L.C., Siciliano, S., & Di Beneditto, A.P.M. (2007).
Stomach contentes of the Magellanic Penguin Spheniscus
magellanicus from the Northern distribution limit on the Atlantic coast of Brazil
.
Marine
Ornithology, 35
, 77-78.
Prado, M.I.B., de M, dos Santos-Lopes, A.R., & da Silva, R.J. (2011). Fauna de helmintos del pingüino de magallanes
(
Spheniscus magellanicus
Foster, 1781) de la Ilha Comprida, costa sur, Estado de São Paulo, Brasil.
Neotropical
Helminthology, 5
, 50-55.
Pütz, K., Ingham, R.J., & Smith, J.G. (2007). Winter migration of Magellanic penguins (
Spheniscus magellanicus
) from
the southern most distributional range.
Marine Biology, 152
, 1227–1235.
Rezende, G.C., Baldassin, P., Gallo, H., & Silva, R.J. (2013). Ecological aspects of helminth fauna of Magellanic
penguins,
Spheniscus magellanicus
(Aves: Spheniscidae), from the Northern Coast of the State of São Paulo, Brazil.
Brazilian Journal of Biology, 73
, 61-66.
image/svg+xml
124
Neotropical Helminthology (Lima). Vol. 17, N
º
2, jul - dic 2023
Mota Alves
et al.
Saad, C.D.R, Vieira, F.M., & Luque, J.L. (2012). Larvae of Anisakidae Skrjabin & Karokhin, 1945 (Nematoda,
Ascaridoidea) in
Lophius gastrophysus
Miranda-Ribeiro, 1915 (Actinopterygii, Lophiidae) from the coastal zone
of the state of Rio de Janeiro, Brazil.
Neotropical
Helminthology, 6
, 159-177.
Santos, C.P., Borges, J.N., Fernandes, E., da S & Pizani, A.P.C.L. (2013).
Nematoda
. In: Pavanelli, G.C, Takemoto,
R.M., Eiras, J.C. (Org).
Parasitologia de peixes de água doce do Brasil
. Eduem.
Silva, R.J., Raso, T.F., Faria, P.J., & Campos, F.P. (2005). Occurrence of
Contracaecum pelagicum J
ohnston & Mawson
1942 (Nematoda, Anisakidae) in
Sula leucogaster
Boddaert 1783 (Pelecaniformes, Sulidae).
Arquivo Brasileiro De
Medicina Veterinária e zootecnia, 57
, 565–567.
Tamiasso, N.V., Zocatelli, T.F., Martins, M.S.S., de Avelar, B.R., Martins, I.V.F., & Nunes, L.D.C. (2018). Identifcation
of parasites and gross fndings in magellanic penguins in Espírito Santo, Brazil.
Archives of Veterinary Science, 23
,
77-85.
Vanhoni, M. S., Arná, G. M., Sprenger, L. K., Vieira, D. L., Luis, L. W., & Molento, M. B. (2018). Occurrence of
gastrointestinal parasites in
Spheniscus magellanicus
(Foster, 1781) located in Pontal do Sul, PR, Brazil.
Arquivo
Brasileiro de Medicina Veterinária e Zootecnia, 70,
491-496.
Yáñez, F., Fernández, Í., Campos, V.V., Mansilla, M., Valenzuela, A., González, H., Rodríguez, C., Rivas, M., Alveal, K.,
& Oyarzún, C. (2017). First pathological report of parasitic gastric ulceration in Humboldt penguin (
Spheniscus
humboldti
) along the coast of south-central Chile.
Latin American Journal of Aquatic Research, 40
, 448-452.
Received July 10, 2023.
Accepted September 13, 2023
.