Neotrop. Helminthol., 5(1), 2011
2011 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
Resumen
Abstract
ORIGINAL ARTICLE/ ARTÍCULO ORIGINAL
HELMINTHFAUNA OF MAGELLANIC PENGUIN (SPHENISCUS MAGELLANICUS FOSTER,
1781) PROCEEDING FROM ILHA COMPRIDA, SOUTH COAST, STATE OF SÃO PAULO,
BRAZIL
FAUNA DE HELMINTOS DEL PINGÜINO DE MAGALLANES (SPHENISCUS MAGELLANICUS
FOSTER, 1781) DE LA ILHA COMPRIDA, COSTA SUR, ESTADO DE SÃO PAULO, BRASIL
1 1 2
Maria Izabel Barbosa de Medeiros do Prado , Ana Rita dos Santos-Lopes & Reinaldo José da Silva
1Instituto de Pesquisas Cananéia IPeC, Cananéia, São Paulo, Brazil.
2UNESP - Univ Estadual Paulista, Campus de Botucatu, Instituto de Biociências de Departamento de
Parasitologia, Botucatu, São Paulo, Brazil.
iza0@hotmail.com
Suggested citation: do Prado, M.I.B.M., Santos-Lópes, A.R. & da Silva, R.J. 2011. Helminthfauna of Magellanic
Penguin (Spheniscus magellanicus Foster, 1781) proceeding from Ilha Comprida, South Coast, State of São
Paulo, Brazil. Neotropical Helminthology, vol. 5, n° 1, pp. 50-55.
The present study aims to identify the helminth fauna of Spheniscus magellanicus Foster, 1781 from the
municipality of Ilha Comprida, southern São Paulo State. A total of 28 individuals were analyzed,
resulting in an identification of three helminth species: Contracaecum pelagicum Johnston &
Mawson, 1942, Cardiocephaloides physalis Sudarikov, 1959 and Tetrabotrium lutzi Parona, 1901.
Contracaecum pelagicum and C. physalis were core species, while T. lutzi was considered a satellite
species. All individuals examined were infected with at least one species (overall prevalence = 100%).
The host specimens were all juveniles and the infection may be associated with food items eaten during
migration to the Brazilian Coast.
Key-words: Cestoda - Helminthes - Nematoda - Marine birds - Parasitic diseases - Trematoda.
Este estudio tuvo como objetivo identificar los helmintos parásitos de Spheniscus magellanicus Foster,
1781 de la municipalidad de Ilha Comprida, a lo largo de la costa sur de Sao Paulo, Brasil. Un total de
28 individuos fueron analizados, dando como resultado la identificación de tres especies de helmintos:
Contracaecum pelagicum Johnston & Mawson, 1942, Cardiocephaloides physalis Sudarikov, 1959 y
Tetrabothrium lutzi Parona, 1901. Contracaecum pelagicum y C. physalis se caracterizan como
especies core, mientras que T. lutzi se considera una especie satélite. Todos los individuos examinados
estaban infectados con al menos una especie, con una prevalencia del 100%. Los especímenes
hospedadores fueron todos juveniles y el patrón de la infección puede estar asociado con la
alimentación durante la migración a la costa brasileña.
Palabras clave: Aves marinas - Cestoda - Enfermedades parasitarias - Helmintos - Nematoda - Trematoda.
50
INTRODUCTION
Penguins are birds, exclusively oceanic, which
modified its wings in flaps adapting to the aquatic
way of life. All species are restricted to the southern
hemisphere (Sick, 1997). On the coast of South
America and its islands there are seven penguin
species, three of them endemic and belonging to
the genus Spheniscus Brisson, 1760. Species of this
genus live further to the north than the other
representatives of the group. Spheniscus
magellanicus Foster, 1781 is the largest and most
abundant species, reproducing in coast of
Argentina, Chile and Falkland Islands in the period
between November and January, spending short
breaks in the sea for food. After the reproductive
season, about the end of February, the annual
migration begins towards the Brazilian coast. This
migration occurs through ocean currents and aims
to increase the abundance of foraging, which also
leads to an increased diversity of foraging (Sick,
1997; Gilpin, 2007).
The majority of population that reaches the
Brazilian Coast is of young penguins. It is common
to find individuals dead on the beaches during the
winter, some specimens reaching the northeast
coast of Brazil. Some factors may be associated
with and worsen the killing of these birds,
including: climate change resulting in changes in
streams and incorrect route of migration of animals
(Sick, 1997), population increases, which may lead
to an increase of young people killed, once there is
a bigger number of birds born and with more
individuals there is a greater competition for food;
and overfishing, the human action that causes
animals to seek food farther from the coast, leading
to ingestion of a diet different from the usual,
resulting in nutritional deficiency of nestlings and
young penguins (González-Acuña et al., 2008).
The host-parasite relationship occurs in an
interspecific way and may affect the life of the host.
In many cases, it remains invisible until the
parasites reach epidemic proportions and interfere
in the host abundance. However, the study of
helminths of a complex life cycle provides
important information about the hosts, such as diet,
migratory routes, foraging areas (Campbell et al.,
1980; Marcogliese, 2004).
The analysis of ecological aspects of parasite-host
is poorly investigated, but the focus on this area is
increasing. Because they have diversified diet,
seabirds are important objects of study and they
may be hosts of helminths in different trophic levels
(Esch & Fernandez, 1993). In Brazil there are few
studies about helminth parasites of marine birds,
although they occur in the country and many of
them use the Brazilian Coast as a feeding ground,
including the species S. magellanicus.
Helminthological studies involving this species are
not very abundant; among them there are the works
of Díaz (2006) and González-Acuña et al. (2008).
In Brazil, they are further reduced, because these
birds are restricted to the south portion of the
country. Studies on the helminthfauna of S.
magellanicus were conducted with host collected
from Rio Grande do Sul (Bassi et al., 2008), Rio de
Janeiro (Pinto et al., 2007) and Espírito Santo State
(Ederli et al., 2009).
This study aims to identify endoparasites contained
in the digestive tract of S. magellanicus that
migrates to the Brazilian Coast at the time of
reproductive rest.
MATERIALS AND METHODS
Penguins (n = 28) were collected on the beaches of
Pedrinhas, municipality of Ilha Comprida, southern
coast of São Paulo, from July to September 2008.
The studied specimens were found dead but the
total sample showed good storage conditions and
were kept frozen at - 5 °C. The animals underwent a
biometrics prior to necropsy, recording the total
length of the body, beak, wing, foot and body
circumference. Necropsies were done at Instituto
de Pesquisas de Cananéia (IPeC) in Cananéia
municipality and the helminths collected were
analyzed at the Laboratório de Parasitologia de
An imais S ilvestr es, De partame nto de
Parasitologia, Instituto de Biociências, Unesp,
Botucatu municipality, São Paulo State, Brazil.
Nematodes were collected, fixed in heated AFA
solution, and for identification, were cleared with
lactophenol. The identification was based on
Yamaguti (1961), Vicente et al. (1995) and Diaz
(2006). The cestodes and trematodes were fixed in
cold AFA solution under coverslip pressure and
Helminthfauna of Spheniscus magellanicus Do Prado et al.
51
then were stained with carmine and cleared in
eugenol or creosote. The identification of cestodes
was based on Diaz (2006) and trematodes on
Travassos et al. (1969), Yamaguti (1971) and Diaz
(2006).
All collected helminths were deposited in the
Coleção Helmintológica do Instituto de
Biociências de Botucatu (CHIBB), Universidade
Estadual Paulista, municipality of Botucatu, São
Paulo State, Brazil.
Prevalence, mean intensity of infection and mean
abundance were calculated according to Bush et al.
(1997).
RESULTS
All individuals (n = 28) studied were parasitized
(overall prevalence = 100%), and a total of 3811
parasites was recovered. The mean intensity of
infection was 146.6 ± 19.4. All hosts were
juveniles, and their biometrics presented as
follows: body length - 44.6 ± 3.4 cm,
circumference of the body - 38.3 ± 2.1 cm, wing
length - 16.6 ± 2.5 cm, length of the nozzle - 5.4 ±
0.5 cm and length of the foot - 11 ± 0.7 cm.
The helminthfauna S. magellanicus was composed
only by three species: Contracaecum pelagicum
Johnston & Mawson, 1942 (Nematoda),
Cardiocephaloides physalis Sudarikov, 1959
(Digenea) and Tetrabothrium lutzi Parona, 1901
(Cestoda). All species were found in the digestive
tract, distributed between the stomach and small
intestine (Table 1).
Contracaecum pelagicum was found in the
stomach and small intestine of the studied birds. In
the first organ it was found in abundance,
occupying its entire length, making a total of 2435
individuals among 23 hosts. In the small intestine,
relative abundance was lower, since it was found
only 727 individuals in 21 hosts. Considering both
site of infection, the prevalence was 96.4%, with
high mean abundance and mean intensity of
infection. Cardiocephaloides physalis was found
only in the small intestine and there were 460
individuals among 19 hosts. This species occurred
in high prevalence but low abundance and intensity
of infection. Tetrabothrium lutzi, in the same way
of C. physalis, was located exclusively in the small
intestine, more specifically in the duodenum. It
was found 189 individuals in 10 hosts (Table 1).
DISCUSSION
This study evaluated the helminth fauna of S.
magellanicus from the municipality of Ilha
Comprida, São Paulo State, Brazil. Among the
three helminth species found, two of them were
core species (C. pelagicum and C. physalis) and
one was satellite (T. lutzi), as defined by Bush et al.
(1997). All specimens studied were infected with at
least one species of helminth, a fact also noted by
Diaz (2006). However, studies with S.
magellanicus in Chile (66.6%) (González-Acuña et
al., 2008) do not found a high prevalence as
reported in this study.
Contracaecum pelagicum showed high prevalence
and mean intensity of infection as observed in the
studies of Pazos (2006) and Díaz et al. (2000). This
nematode can infect several hosts and it was first
recorded in black brow albatross (Diomedea
melanophris Temmick, 1828) in Australia and
since then the infection was reported in other
seabirds as brown booby (Sula leucogaster
Boddaert, 1783) (Silva et al., 2005). In Brazil, this
parasite was identified in populations of S.
magellanicus from various regions, such as Rio
Grande do Sul (Bassi et al., 2008) and Espírito
Santo (Ederli et al., 2009) and has been found
distributed between the stomach and intestine.
Larvae of C. pellagicum were found in fish (Timi,
2003) and cephalopods (Cremonte & Laurenti,
2005 apud Diaz, 2006), preys that serve as food for
these birds and, therefore, act in the transmission of
this parasite to birds. During the pelagic time, S.
magellanicus presents changes in eating patterns
and the main food items are cephalopods,
Argonauta nodosa Lightfoot, 1786, Loligo plei
Blainville, 1823 and Loligo sanpaulensis
Brakoniecki, 1984 (Pinto et al., 2007). This change
creates a nutritional deficiency making juvenile
weaker and more propense to death (Pinto et al.,
2007, González-Acuña et al., 2008), which would
explain the high mortality rate of individuals that
reach the coast (Pinto et al., 2007).
For C. physalis, prevalence also was high, but the
mean intensity of infection was low in comparison
to data presented by Díaz (2006), in which a high
prevalence (55.6%) and intensity of infection (153)
was observed. This genus has very similar
morphology between their representatives and it is
composed by seven species (Dubois, 1968).
Among the birds, their hosts are distributed in three
families Laridae, Anatidae and Procellaridae
Neotrop. Helminthol., 5(1), 2011
52
Table 1. Prevalence, intensity of infection, abundance and site of infection of the helminths collected in Spheniscus
magellanicus (n = 28) from the municipality of Ilha Comprida, southern coast, State of São Paulo, Brazil.
*Numbers in the first column is the accession number of voucher species in CHIBB - Coleção Helmintológica of the
Instituto de Biociências, Universidade Estadual Paulista; TNP, total number of parasites; P, prevalence; MII, mean
intensity of infection; MA, mean abundance; SI, site of infection; SE , standard error.
(Dubois, 1968; Abdel-Aal et al., 2004). The larvae
of trematodes have been reported parasitizing the
eyes of Engraulis anchoita Hubbs et Marinni,
1935, fish that represents a major part of the diet of
S. magellanicus (Timi et al., 1999).
Regarding T. lutzi the prevalence was 36%, which
conflicts with studies conducted in regions of
Argentina. In individuals of the region of the
Peninsula Valdes, this cestode had a high
prevalence (85.6%) and average intensity of
infection (521) (Díaz, 2006). This cestode is one of
the most representatives of poultry helminths,
parasit izing five orders : pre y items,
Pelecaniformes, Charadriiformes, Gaviformes and
Sphenisciformes (Hoberg, 1989). For the genus
Spheniscus, we have five species of tetrabothriids
described and only two of these species were
reported infecting S. magellanicus: T. lutzi and
Tetrabothrius eudyptidis Loennberg, 1896.
Analysis of stomachal contents allowed
determining the diet of these animals and it was
observed that there is a change in the diet following
the action of fishing industries and latitudinal
variation (Frere et al., 1996; Putz et al., 2001).
The diet is no longer composed mostly by fish,
being replaced for cephalopods. The effort to find
food by parents increases, the amount of food given
to the offspring decreases and beyond that,
digestion of the offspring becomes more difficult.
These variations produce changes in the nutritional
development of the nestlings and juveniles,
resulting in death or physical weakness (Pinto et
al., 2007; González-Acuña et al., 2008).
A final analysis that can be done about the parasite
community of S. magellanicus is related to the
concepts of interactive and isolationist
communities (Holmes, 1987). Typically,
endothermic hosts harbor interactive communities
of parasites and ectothermic hosts provides home to
isolationist communities, but this does not happen
with the helminth species of S. magellanicus,
which presents isolationist communities. This
could be related to factors such as limited diet,
pelagic habit and simple digestive tract (few niches
to be occupied) (Díaz, 2006). This study
corroborates the data obtained by Díaz (2006),
mainly in relation to the diet change. Consuming
fewer items, the diversity of helminths is low and
these species do not interact.
Helminthfauna of Spheniscus magellanicus Do Prado et al.
53
,
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Received April 5, 2011.
Accepted May 28, 2011.
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Maria Izabel Barbosa de Medeiros do Prado
Instituto de Pesquisas Cananéia IPeC, Cananéia,
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E-mail/Correo electrónico:
iza0@hotmail.com
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