ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2018, 12(2), jul-dic:187-193.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
A NEW SPECIE OF BRANCHIURA (CRUSTACEA: ARGULIDAE) PARASITE OF ARAPAIMA GIGAS
SCHINZ, 1822 FROM BRAZILIAN AMAZON
UMA NOVA ESPÉCIE DE BRANCHIURA (CRUSTACEA: ARGULIDAE) PARASITA DO ARAPAIMA
GIGAS SCHINZ, 1822 (OSTEOGLOSSIFORMES: ARAPAIMATIDAE) DA AMAZÔNIA BRASILEIRA
UNA NUEVA ESPECIE DE BRANCHIURA (CRUSTACEA: ARGULIDAE) PARÁSITA DEL ARAPAIMA
GIGAS SCHINZ, 1822 (OSTEOGLOSSIFORMES: ARAPAIMATIDAE) DE LA AMAZONÍA
BRASILEÑA
Amanda Karen Silva de Souza & José Celso de Oliveira Malta, Fish Parasite Laboratory, Campus II, Instituto Nacional de
Pesquisas da Amazônia, Inpa. Av. André Araújo, 2.936 - Petrópolis - CEP 69.067-375 - Manaus – Amazonas.
*Corresponding author: E-mail: atjsouza15@gmail.com
Amanda Karen Silva de Souza & José Celso de Oliveira Malta
ABSTRACT
Keywords: Amazonas – Arapaima gigas – Argulus moratoi n. sp. – fish parasite
Argulus moratoi n. sp. was described from Arapaima gigas Schinz, 1822 collected in fish farms in the
municipality of Abaetetuba, Pará, and a specimen collected in the municipality of Barcelos, in the state of
Amazonas, Brazil. The new species is characterized by pronounced, deep, large, semi-rectangular and
depigmented antero-lateral depressions delimiting the frontal kidney-shaped, region, supporting rods
formed of two sclerites, first in the "J" shape and the second in "V" shape, heart shaped carapace, in the
nd
male the sexual modification of the 2 leg being a parallelogram-shaped projection directed inward, and
simple scales.
Neotropical Helminthology
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RESUMO
Palavras-chave: Amazonas – Arapaima gigas – Argulus moratoi n. sp. – parasita de peixes
Argulus moratoi n. sp. foi descrito de Arapaima gigas Schinz, 1822 coletados em pisciculturas no
município de Abaetetuba, Pará, e um espécime coletado no município de Barcelos, no estado do
Amazonas, Brasil. A nova espécie é caracterizada por apresentar depressões pronunciadas, profundas,
grandes, semi-retangulares e despigmentadas antero-laterais, delimitando a região frontal em forma de
rim, apoiando bastões formados por dois escleritos, primeiro no formato "J" e o segundo em "V". "forma,
carapaça é em forma de coração, no macho a modificação sexual da segunda perna é uma projeção em
forma de paralelogramo direcionada para dentro e espinhos simples.
Branchiura is a group of parasitic crustaceans
found as parasites on fresh and brackish water
fishes around the globe (excepting Antarctica).
Thirteen Argulus Muller, 1785 species occur in
Brazil, only five of them have been reported in the
Amazon all of freshwater environments (Souza et
al., 2018).
Modifications for different kinds of attachment are
common among parasitic crustaceans, but the
suction discs seen in most species of the Branchiura
are among the most elaborate and fascinating of
such structures. The term 'suction disc' is well-
chosen since they operate by muscle-facilitated
suction (Gresty et al., 1993). Suction discs are
found in three of the four currently recognized
genera of the Branchiura, in Argulus, Chonopeltis
Thiele, 1900, and Dipteropeltis Calman, 1912, and
it is well known that these structures are modified
first maxillae (Wilson, 1902; Thiele, 1904;
Ringuelet, 1943; Fryer, 1964).
Branchiura species are ectoparasitic crustaceans of
fish and, occasionally, of amphibians and reptiles.
Each species has a preferred area of fixation, can be
the gill or buccal cavity, the surface of the body or
the base of the fins. In the gill cavity, they attach to
the wall of the operculum or the posterior wall of
the last branchial arch, rarely in the branchial
filament, except the young individuals. Species fix
their hosts by means of first and second maxillae,
antennae, spines, hooks and teeth. In addition, the
ventral part of the carapace is concave and
functions as a suction cup which is compressed to
the body of the host by the action of the water
stream passing through the dorsal surface of the
crustacean (Malta, 1982a; 1982b; 1984, Malta &
Varella, 2009). The objective of this work was to
describe a new species of Branchiura of the genus
Argulus parasitizing an Amazonian fish.
On August 26, 2016, 85 specimens of Argulus were
collected from an Arapaima gigas (Schinz, 1822)
at a fish farm in the municipality of Abaetetuba,
state of Pará, Brazil. Argulus were fixed in ethyl
alcohol 70% later taken to the Laboratory of Fish
Parasitology of the Instituto Nacional de Pesquisas
da Amazônia - INPA.
Argulus studied by light and stereo microscopy. All
measurements are in millimeters and shown as
follows: range, minimum - maximum and
arithmetic mean (within brackets). The description
is based on the measurements of 10 adult females
and 10 males. Drawings were made in light
microscope Olympus BH-2 with camera lucida.
Types, and were deposited, in the non-insect
Invertebrate Collection of the National Research
Institute of Amazonia (INPA), Manaus, Amazonas,
Brazil. Paratypes: 10 females and 10 males (INPA -
2446).
Taxonomy
Subclass Branchiura
Order Argulidea
188
Neotropical Helminthology, 2018, 12(2), jul-dic
INTRODUCTION
MATERIAL AND METHODS
RESUMEN
Argulus moratoi n. sp. se describió de Arapaima gigas Schinz, 1822 recolectadas en piscigranjas en el
municipio de Abaetetuba, Pará, y un espécimen recolectado en el municipio de Barcelos, en el estado de
Amazonas, Brasil. La nueva especie se caracteriza por presentar depresiones antero-laterales
pronunciadas, profundas, semi-rectangulares y despigmentadas que delimitan la región frontal en forma
de riñón, barras de soporte formadas por dos escleritos, el primero en forma de "J" y el segundo en "V".
"La forma, el caparazón es en forma de corazón, en el macho, la modificación sexual de la segunda pata es
una proyección en forma de paralelogramo dirigida hacia adentro y con escalas simples.
Palabras clave: Amazonas – Arapaima gigas – Argulus moratoi n. sp. – parásito de peces
RESULTS
Souza & Malta
189
Family Argulidae Leach, 1819
Genus Argulus Müller, 1785
Argulus moratoi n. sp.
Material examined – Holotype: Female (INPA-CR
2445) form the body surface of Arapaima gigas
Schinz, 1822, in liquid medium, from a fish farm in
Abaetetuba, State of Pará, Brazil latitude: 01º 43
'05 "S, longitude: 48º 52 '57 "W.
Paratypes: 10 females and 10 males (INPA - 2446).
Description
Adult female. General body form squat (Fig. 1);
carapace sub-oval and heart shaped, comprising
about 64% of total body length. Total length range
5.1 - 3.91 (4.7) mm (based on 10 specimens)
(Figure 1). Elongated body. Milk white colored
dorsal surface with drawings formed by dots of
brown pigments. Carapace longer than wide
carapace length (cl) 3.4 - 2.72 (3.0) mm. Lateral
lobes of carapace rounded cover the margin
anterior of third leg, separated by V-shaped sinus
less than 1/5 length of carapace, with a vertical
band of dark pigments close and parallel to each
lateral end. Suckers visible in dorsal view (Figure
1).
Pronounced, deep, large, semi-rectangular and
depigmented antero-lateral depressions delimiting
the frontal region kidney-shaped (Figure 1 and 2).
Well defined interocular ribs, paired large
compound eyes, found at the same height of the
junction between the frontal region and the main
part of the carapace. Small nauplius eye Y-shaped
found on dorsal surface in center of carapace. Edge
of suction cups visible in dorsal view.
Ventral side of carapace covered with simple scales
similar the minute spinules, tending to be more
numerous anteriorly and extending along the
nd
margin of the lateral lobes to the height of the 2
pair of legs. Ventral surface of the carapace lateral
lobes with two unequal respiratory areas (Figure
2): the largest oval area, with two notches, the first
very small at the anterior margin and the second
large and well defined at the anterior lateral
margin; small respiratory area located in the
anterior margin near the anterior notch.
Thorax distended with eggs but not in carapace alae
and indistinctly 4-segmented. (Figures 1 and 2).
Thorax with drawings consisting of dots of brown
pigments across the dorsal surface, lateral margins
of the segments with a band made of dark brown
pigments that extend to form a median stripe in the
abdomen until near the distal part.
Abdomen (Figures 1 e 2) longer than broad, with a
row of simple scales near the margins on the dorsal
and ventral surface, posterior lobes tapering to
point from behind anal sinus; separated by broad
sinus about 1/3 length of abdomen. Paired
spermathecae located at middle of abdomen; furcal
rami small, located adjacent to midline at base of
anal sinus.
First antenna (Figure 4) 5 segmented. First segment
(basal segment) sclerotized, large with stout
posteriorly-projecting posterior spine. Second
segment sclerotized with anterior and medial
spines, plus large lateral hook. Terceiro segmento
com uma seta longa na porção distal. Fourth
segment fleshy, cylindrical without ornamentation.
Fifth segment fleshy, cylindrical with two posterior
setae.
Second antenna (Figures 2 e 4) with four segments.
First segment larger; remaining three thin,
cylindrical. Third segment fleshy with a terminal
simple seta. Fourth segment fleshy, cylindrical
with two posterior setae (Figure 4).
First maxillae modified into suction cups in adults.
(Figure 2). Supporting rods comprised of two
sclerites, first in the "J" shape and the second in "V"
shape (Figure 2C). Periphery of suckers fringed
with tiny spinules (Figure 2C). Retractile pre-oral
spine located midway between maxillary suckers;
tip extending to midway between post-antennal
spine when retracted. Mouth tube more than twice
as long as broad without ornamentations. Pair of
broad accessory spines located posterior to mouth-
tube on either side of midline (Figure 2).
Second maxilla 5-segmented (Figure 2) proximal
section 2-segmented; distal section 3-segmented.
Basal segment with broad bearing 3 stout, digitate
spines, usually larger space between lateral spine
and central spine. Basal plate with elevated pad
bearing coarse-pectinate scales and about three
stouts, simple setae that extend over median
posterior spine and space between central and
lateral posterior spines. Second to 4th segments
armed with simple and pectinate scales. Terminal
A new species of Branchiura
Neotropical Helminthology, 2018, 12(2), jul-dic
190
segment lacking scales and ending in a lobe and
two small claws. Pair of broad post-maxillary
spines present on ventral body surface either side of
midline (Figure 8).
Four pairs of biramous swimming legs composed
of a precoxa (protopod), coxa, basis, exopod, and
endopod. First to 4th pairs of legs biramous, of near
equal size (Figures 9 - 12). Sympods distinctly 3-
st nd
segmented. Flagellum present on 1 and 2 legs;
extending medially from origin on dorsal surface at
base of exopod. Rami and flagella armed with
th
plumose setae (Figures 9 e 10). Third and 4 legs
lacking accessory copulatory structures. Small,
simple scales present on swimming legs. Natatory
lobe on fourth leg produced laterally and armed
with simple scales and plumose setae.
Adult male. Body form similar to that of female;
carapace comprising about 65% of total length;
(Figures 13 - 17 e Table 2). Total length range 3.79
– 2.8 (3.5) mm (based on 10 specimens), they are
25% smaller than the female (Figure 13 e Tab. 2).
Cephalic appendages and first 2 pairs of legs
similar to those of female.
Small, simple scales present on swimming legs.
nd rd
Sexually dimorphic characters' present in 2 , 3
th nd
and 4 legs, all on 2 segment of sympods. Sexual
nd
modification of the 2 leg (Figure 15) is a
parallelogram-shaped projection directed inward
with simple scales. Single cup-shaped socket on
rd
posterior margin of protopod of 3 leg, located
directly above copulatory peg on anterior surface
th
of basis of 4 leg. Natatory lobes of leg 4 triangular,
with 5 plumose setae.
Abdomen (Figure 13) broader than thorax, length
range 0.8 – 1.19 (1.0) mm, comprising 28.57% of
total body length; about twice as long as broad;
posterior lobes tapering to slightly rounded points;
separated by sinus 1/3 length of abdomen. Paired
elongated testes that extend through almost the
entire abdomen; dorsal and ventral surface of
abdomen with simple scales. Furcal rami minute,
situated on dorsal side at base of anal sinus.
Etymology: The specific name "moratoi" is a
tribute to Celso Morato de Carvalho a great
biologist who dedicated his life to the study of
Amazonian herpetology.
There are described fourteen species of the genus
Argulus recorded from the Brazil (Malta, 1998;
Luque et al., 2013). Six of them, namely: A.
multicolor Stekhoven, 1937; A. pestifer Ringuelet,
1948; A. juparanaensis Lemos de Castro, 1950; A.
amazonicus Malta & Silva, 1986; A. chicomendesi
Malta & Varella, 2000 and A. angelae Souza, Porto
& Malta, 2018 have been reported in the Amazon
2017 (Malta, 1982ab;1984;Souza et al., 2018).
Argulus violaceus Thonsem, 1925 from Uruguay
and A. americanus Wilson, 1902 from USA has the
supporting rods of the first maxillae comprised of
two sclerites in the "J" shape (Wilson, 1902;
Thomsen, 1925). Argulus patagonicus Ringuelet,
1943 from Argentina has three sclerites, the J-
shaped basal, the ovoid-shaped intermediate and
the rounded terminal (Ringuelet, 1943). Argulus
carteri Cunnington, 1931 from Paraguay has too
three sclerites, the J-shaped basal and the rounded
terminals. Argulus moratoi n. sp. has two sclerites,
but the first has "J" shape and the second "V" shape.
Only the five species has sclerites basal J-shaped.
Argulus moratoi n. sp. is the fifteenth species cited
for Brazil and the seventh from Amazon region.
Argulus moratoi n. sp. is from the group of
Argulidae species in which modifications of the
legs of males occur in the second, third and fourth
pairs of legs. As A. pestifer Ringuelet, 1948 from
Argentina; A. ernsti Weibezahn & Cobo, 1964
from Venezuela; A. angelae Souza, Porto & Malta,
2018 from Brazilian Amazon. But A. moratoi n. sp.
is the unique species that the sexual modification of
nd
the 2 leg is a parallelogram-shaped projection
directed inward with simple scales.
The male of A. moratoi n. sp. has a paired elongated
testis that extend through almost the entire
abdomen; similar the A. salmini Kroyer, 1863 from
Argentina and Brazil and A. chicomendesi Malta &
Varella, 2000 from Brazilian Amazon. All the
males of Branchiura are smaller than the females.
Argulus kosus, A. fryeri Rushton-Mellor, 1994, A.
izintwala Van As & Van As, 2001, A. multipocula
Barnard, 1955 and A. angelae present pronounced
and deep antero-lateral depressions, forming a
distinct frontal region (Avenant-Oldewage, 1994;
DISCUSSION
Neotropical Helminthology, 2018, 12(2), jul-dic Souza & Malta
191
A
B
D
E
F
G
H
I
J
K
L
1mm
C
M
1 mm
1 mm
0.5 mm
0.5 mm
0.5 mm
1 mm
0.1 mm
Figure 1. A-M: Argulus moratoi sp. n. (female), A – dorsal; B – ventral; C – F legs; G – pré-oral stilet; H – bucal cone; I – maxilla 1;
J – maxilla 2; K – respiratory areas; L - antennas 1 and 2; M – caudal rami.
A new species of Branchiura
Neotropical Helminthology, 2018, 12(2), jul-dic
192
1mm
1mm
A
B
C
D
E
Figures 2. A-E: Argulus moratoi sp. n. (male), 1 – dorsal; 15-18 – legs.
Van As & Van As, 2001; Smith et al., 2005; Souza
et al., 2018). In A. angelae, the antero-lateral
depressions are delimited by the rectangular
antero-lateral depressions (Souza et al., 2018). In
A. moratoi n. sp. the anterolateral depressions are
very like those of A. angelae, are pronounced,
deep, large, and depigmented, but are semi-
rectangular and the frontal region is kidney-
shaped, not rounded.
Argulus moratoi n. sp. was described from A. gigas
of a farm fish in Brazil. The new species is
characterized by shape and drawings of the
carapace, abdomen and thorax by pronounced,
deep, large, semi-rectangular and depigmented
antero-lateral depressions delimiting the frontal
region kidney-shaped, to present supporting rods
formed of two sclerites, first in the "J" shape and
the second in "V" shape, carapace is heart shaped,
nd
in the male the sexual modification of the 2 leg is a
parallelogram-shaped projection directed inward
and simple scales.
Argulus moratoi n. sp. is the fourth Branchiura
species cited for A. gigas. The other three species
cited are: Dolops discoidalis (Bouvier, 1897)
(Malta, 1982ab; 1998; Luque et al., 2013), Argulus
sp.1 and Argulus sp.2 (Malta, 1981). Two species
were mistakenly quoted as A. gigas parasites:
Argulus chicomendes and D. carvalhoi Lemos de
Castro, 1949 and Luque et al. (2013).
The authors thank Jeffson Pereira Nobre for
collecting and donating specimens.
ACKNOWLEDGEMENT
Neotropical Helminthology, 2018, 12(2), jul-dic Souza & Malta
193
Avenant-Oldewage, A. 1994. A new species of
Argulus from kosi bay, south africa and
distribution records of the genus. Koedoe, vol.
37, pp. 89-95.
Cunnington, WA. 1931. Reports of an Expedition to
Brazil and Paraguay in 1926–27, supported
by the Trustees of the Percy Sladen Memorial
Fund and the Executive Committee of the
Carnegie Trust for Scotland. Argulidæ.
Zoological Journal of the Linnean Society,
vol. 37, pp. 259-264.
Fryer, G. 1964. Further studies on the parasitic
Crustacea of the African freshwater fishes.
Proceedings of the Zoological Society of
London, vol. 143, pp. 79-102.
Gresty, KA, Boxshall, GA & Nagasawa, K. 1993. The
fine structure and function of the cephalic
appendages of the Branchiuran parasite,
Argulus japonicus Thiele. Philosophical
Transactions of The Royal Society B
Biological Sciences, vol. 339, pp. 119-135.
Malta, JCO. 1981. Os crustáceos branquiúros e suas
interrelações com os peixes do lago
Janauacá, estado do Amazonas, Brasil.
Dissertação de mestrado. Biologia de Água
Doce e Pesca Interior, INPA, Manaus, 88p.
Malta, JCO. 1982a. Os argulídeos (Crustacea:
Argulidae) da Amazônia brasileira. Aspectos
da ecologia de Dolops discoidalis Bouvier,
1899 e D. bidentata Bouvier, 1899. Acta
Amazonica, vol. 12, pp. 521-528.
Malta, JCO. 1982b. Os argulídeos (Crustacea:
Argulidae) da Amazônia brasileira, 2.
Aspectos da ecologia de Dolops geayi
Bouvier, 1899 e Argulus juparanaensis Lemos
de Castro, 1950. Acta Amazonica, vol. 12, pp.
701-705.
Malta, JCO. 1984. Os peixes de um lago de várzea da
Amazônia Central (Lago Janauacá, rio
Solimões) e suas relações com os crustáceos
ectoparasitas (Branchiura: Argulidae). Acta
Amazonica, vol. 14, pp. 355-372.
Malta, JCO. 1998. Maxillopoda - Branchiura. In:
Yong, P. (Ed.). Catalogue of Crustacea of
Brasil. Museu Nacional, Rio de Janeiro,
p.67–74.
Malta, JCO & Varella, AMB. 2009. A Fauna de
Arthropodes da Reserva Florestal Ducke –
Estado atual do conhecimento taxonômico e
biológico. Ed. INPA. 1, pp. 17-20.
Luque, JL, Vieira, FM, Takemoto, RM, Pavanelli, GC
BIBLIOGRAPHY REFERENCES & Eiras, JC. 2013. Checklist of Crustacea
parasitizing fishes from Brazil. Check List,
vol. 9, pp. 1449-1470.
Ringuelet, R. 1943. Revision de los Argúlidos
Argentinos (Crustacea, Branchiuria): con el
catálogo de las especies Neotropicales.
Revista del Museo de la Plata. Seccion
Zoologia, vol. 3, pp. 43 - 125.
Ringuelet, R. 1948. Argúlidos del Museo de la Plata.
Revista del Museo de la Plata. Seccion
Zoologia, vol. 5, pp. 281 - 296.
Rushton-Mellor, SK. 1994. The genus Argulus
(Crustacea: Branchiura) in Africa: two new
species, A. fryeri and A. gracilis, the
previously undescribed male of A.
brachypeltis Fryer and the identity of the male
described as A. ambloplites Wilson.
Systematic Parasitology, vol. 28, pp. 23-31.
Smith, JN, Van As, LL & Van As, JG. 2005.
Redescription of Argulus multipocula
Barnard, 1955 (Crustacea: Branchiura)
collected on the west coast of South Africa.
Systematic Parasitology, vol. 60, pp. 75-80.
Souza, AKS, Porto, BP & Malta, JCO. 2017. Argulus
angelae sp. n. (Crustacea: Argulidae) parasita
de peixes da Amazônia brasileira. Iheringia
(In press).
Thiele, J. 1904. Beitra¨ge zur Morphologie der
Arg ul iden. Mitt ei lungen aus de m
Zoologischen Museum zu Berlin, vol. 2, pp.5-
51.
Thomsen, R. 1925. Argulus violaceus nov. spec.
cangrejo parásito del bagre. Physis, vol. 8, pp.
185-198.
Van As, JG & Van As, LL. 2001. Argulus izintwala n.
sp. (Crustacea: Branchiura) from lake St
Lucia, South Africa. Systematic Parasitology,
vol. 48, pp. 75–79.
Weibezahn, FH & Cobo, T. 1964. Seis argulidos
(Crustacea: Branchiura) parasitos de peces
dul ce-ac uicol as en Vene z uela, con
descripción de una nueva especie del genero
Argulus. Acta Biologica Venezuelica, vol. 4,
pp. 119-144.
Wilson, CB. 1902. North American parasitic
copepods of the family Argulidae, with a
bibliography of the group and a systematic
review of all known species. Proceedings of
the U.S. National Museum, vol. 25, pp. 635-
742.
A new species of Branchiura
Neotropical Helminthology, 2018, 12(2), jul-dic
Received November 5, 2018.
Accepted December 15, 2018.
