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ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2022, 16(2), jul-dic:123-132.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
1
Instituto Nacional de Pesquisas da Amazônia – INPA, Brasil.
*Corresponding author: atjsouza15@gmail.com
Amanda Karen Silva Jtineant: https://orcid.org/0000-0001-7506-0794
Daniel Brito Porto: https://orcid.org/0000-0002-7640-7021
José Celso de Oliveira Malta: https://orcid.org/0000-0003-1496-2190
1*11
Amanda Karen Silva Jtineant; Daniel Brito Porto & José Celso de Oliveira Malta
ABSTRACT
Argulus yawewitus
sp. n. is described from pirarucu,
Arapaima gigas
(Shinz, 1822) from a fish farm in
Northeast Brazil. The characteristics that distinguish it from other species are shape of the carapace,
abdomen, respiratory areas, the ornamentation and morphology of the antena and antennule, the sexual
dimorphism that distinguishes female from male, and the flag-like protrusions on the male's second and
third pair of legs.
Neotropical Helminthology
123
DOI: http://dx.doi.org/10.24039/rnh20221621481
ARGULUS YAWEWITUS
SP. N. (CRUSTACEA: BRANCHIURA) PARASITE OF
ARAPAIMA GIGAS
(SHINZ, 1822) (OSTEOGLOSSIFORMES: ARAPAIMIDAE) FROM BRAZIL
ARGULUS YAWEWITUS
N. SP. (CRUSTACEA: BRANCHIURA) PARÁSITO DE
ARAPAIMA GIGAS
(SHINZ, 1822) (OSTEOGLOSSIFORMES: ARAPAIMATIDAE) DE BRAZIL
D
Keywords
: fish ectoparasite – freshwater Argulidae –
Argulus
yawewitus sp. n. – South America
D
D
RESUMEN
Argulus yawewitus
n. sp. se describe de pirarucu,
Arapaima gigas
(Shinz, 1822) de una piscifactoría en el
noreste de Brasil. Las características que lo distinguen de otras especies son la forma del caparazón,
abdomen, áreas respiratorias, la ornamentación y morfología de la antena, y anténula, el dimorfismo
sexual que se acentúa entre hembra y macho, y las protuberancias en forma de bandera en el segundo y
tercer par de patas del macho.
Palabras clave
: América del Sur – Argulidae de agua dulce –
Argulus
yawewitus n. sp. – ectoparásito de peces –morfología
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
124
Neotropical Helminthology, 2022, 16(2), jul-dic
INTRODUCTION
The species of Branchiura are ectoparasite
crustaceans of fish that live primarily on the outer
surface of the body and the base of the fins of their
hosts. Their larvae are free-living in at least one of
their phases: in the last larval stage they are fixed in
a host (Ringuelet, 1943). Few species of
Argulus
Müller, 1785 have been described from marine fish
and scattered reports of Branchiura on tadpoles,
salamanders and even alligators can be found
(Ringuelet, 1943; Piasecki & Avenant-Oldewage,
2008).
Branchiura species feed on blood, plasma, mucus,
or epithelial cells (Ringuelet, 1943). In the species
of the genus
Argulus
the oral apparatus consists of
two distinct parts united in their bases; the anterior
part is formed by a fine point stylus. When not in
use it is partially retracted into a sheath. Inside the
stylet there is a duct that attaches to a poison gland,
located on the bottom of this unit; this organ is
similar to the buccal apparatus of the hemiptera and
is used to pierce the fish epidermis for food
purposes. This piece is called a pre-oral spine
(Malta & Varella, 2009).
The branchiurans have a significant economic
importance due to the damage they cause to natural
populations of fishes, debilitating adult hosts and
generally killing young fish. These damages are
increased in intensive crops given the high
concentration of fish and small areas creating
optimal conditions for the development of these
and other parasites. In these environments,
populations of Branchiura species increase rapidly
and as the fish cannot escape the attacks, they
become true pests (Kabata, 1970; Souza & Malta,
2018ab).
A new species of
Argulus
is described from
pirarucu,
Arapaima gigas
(Shinz, 1822) of a fish
farm in Northeast Brazil.
Branchiurans were carefully taken from fish
captured with delicate tweezers. Eleven specimens
of
Argulus
yawewitus
n. sp. were collected on the
surface of the
A. gigas
body raised at the fish farm
of the Federal Rural University of Pernambuco,
Recife and Pernambuco state, Brazil. The
specimens were preserved in 90% ethyl alcohol
and studied with the aid of stereo and light
microscopes. Two specimens (1 male and 1 female)
were cleared in lactic acid + water 1:1
Drawings were made (with the aid of a drawing
tube).
Measurements were made with a micrometer
eyepiece and given as means followed by the range
in brackets and
in millimeters. Five females and
two males were deposited in the non-insect
Invertebrate Collection of the National Research
Institute of Amazonia (INPA), Manaus, Amazonas,
Brazil (INPA 2549 and INPA 2550).
For the external ultrastructural analysis, two
specimens, one male and one female, were
selected, underwent post-fixation in 1% OsO
4
(Osmium Tetroxide) during 3 h, followed by
dehydration in an increasing series of ethanol from
80% ethanol to 100%, and then dried in a CO
2
Critical Point device. then the Branchiura were
carefully mounted on “stubs” (metallic aluminum),
metallized with gold and analyzed under a Tescan
scanning electron microscope VEGA 3 of the
Laboratory of Animal Histology and Embryology
at the Institute of Health and Animal Production in
partnership with the Federal Rural University of
the Amazon.
Ethic aspects
: This study followed and committed
to all ethical aspects to be carried out.
Taxonomy
Phylum Arthropoda
Class Maxillopoda
Subclass Branchiura
Order Argulidea
Family Argulidae
Genus
Argulus
Müller O.F., 1785
Argulus yawewitus
sp. n
.
Material examined – Holotype adult female (INPA
- CR 2549) from the body surface of
Arapaima
gigas
in liquid medium from fish farms of the
Federal Rural University of Pernambuco, Brazil
.
Jtineant
et al.
MATERIAL AND METHODS
RESULTS
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
125
Neotropical Helminthology, 2022, 16(2), jul-dic
Adult female
(Fig. 1 - 4)
Based on ten females the body shape is rounded
(Figs 1 - 4) with paired incisions of antero-latera
carapace to form a defined frontal region and
comprising cephalon, four thoracic somites, and
abdomen. Color in alcohol-fixed is light yellow
with drawings formed by spots of light brown
pigments in the carapace and dark brown in the
abdomen. Total length (tl) 4.08-5.44 (4.69 ± 0.59);
carapace length (cl) 3.45-4.59 (3.95 ± 0.48),
carapace width (cw) 3.06-4.89 (3.99 ± 0.81).
Relations between total length / carapace length (tl
/ cl) 1.09-1.33 (1.2 ± 0.07). Cephalon longer than
wide, bearing pair of compound eyes and nauplius
eye. Compound eye bean-shaped with medial cleft
on interior margin.
Nauplius eye composed of three
ocelli, two ocelli facing anteriorly and one facing
posteriorly.
Argulus yawewitus
sp. n. parasitic of
Arapaima gigas
A
B
C
A
D
A
2
00
µ
1mm
Figure 1.
(A – F). A - Female of
Argulus yawewitus
sp. n. B – Antenna and Antenula; C and D – Cephalic Spine; E – Sucker; F –
support rods Second Maxilla.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
126
A pair of separate interocular rods originates near
the margin anterior of cephalon and extend towards
and pass between compound eyes going to the
anterior margin of the first somite of the
cephalothorax. Carapace longer than wide,
posterior margin fully covers all legs and exceeds
half of abdomen length. Suckers partially visible in
dorsal view. Lateral lobes broadly rounded,
posteriorly separated by broad sinus 1/3 length of
carapace. Abdomen wider than short, length 0.54-
0.85 (0.71 ± 0.11) and width 0.93-1,14(0.99 ±
0.09); ratio total length / length of the abdomen (tl
/la) 5.75 - 8.96 (6.74 ± 1.34), but somewhat
variable between paratypes in length-to-width ratio
ranging from 0.54-0.81. Widely rounded
abdominal lobes; rami furcal small, located next to
the midline. Small and orbicular spermatheca. The
anal sinus about a quarter of the length of the
abdomen. Light yellow colored dorsal surface with
light yellow markings
.
Eggs
Eggs
Carapace
A
B
C
D
T
h
orax
E
F
T
h
orax
Abdomen
50
µ
100
µ
100
µ
200
µ
50
µ
100
µ
Figure 2.
(A – F): A and B - Female of
Argulus yawewitus
sp. n., detail of eggs on the carapace; C and D – First legs; E – Thorax
and abdomen; and F – Natatory lobule fourth pair of legs.
Neotropical Helminthology, 2022, 16(2), jul-dic
Jtineant
et al.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
127
Neotropical Helminthology, 2022, 16(2), jul-dic
Ventral surface of the cephalic region and anterior
part of the carapace ornamented with regularly
arranged spines of similar size up to the height of
the first pair of legs. Paired respiratory areas on
ventral surface of lobes; anterior respiratory area
small and circular to ovoid; posterior respiratory
area with 4 indentations on internal margin. Thorax
indistinctly 4-segmented, with distinctive light
brown pigment spots, distended with eggs, ventral
surface ornamented with scales and dorsal surface
smooth (Fig. 2E) .
First antenna (Fig. 1B and 4A) comprising 2
sections; stout 2-segmented proximal section
possessing large spines; slender distal section with
setae. First segment bearing a stout, large,
Argulus yawewitus
sp. n. parasitic of
Arapaima gigas
1
2
A
B
C
D
E
F
100
µ
20
µ
20
µ
50
µ
20
µ
20
µ
Figure 3.
A - Female of
Argulus yawewitus
sp. n., mouth tube and second maxillae; B – Pre-oral papila; C – 1 mouth tube and 2
second maxillae; D – second maxilla basis; E – Detail of the ornamentation of the second maxillae; and F –.Scales of second
maxilla.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
128
posterior, slightly incurved spine; 2nd segment
massive, without medial spine, large hook-like
terminal spine and anterior spine, lacking hook.
Second antenna (Fig. 1B and 4A) 5-segmented,
fleshy. First 2 segments larger; remaining 3 thin,
cylindrical; basal segment bears posterior spine.
First segment bearing large, pointed posterior
spine, a tuft of setae on rounded protrusion and
terminally a large protrusion with three apical
setae. Second segment short, approximately half of
the first with a tuft of setae. Third segment the
longest with nine thin setae. Forth segment without
ornamentation. Fifth segment with three terminal
spines.
First maxilla forming large suction cup. Support
rods composed of two sclerites of a rectangular
shape (Fig. 1E and F). Anterolateral portion of
suction cup with a thin membrane. Second maxilla
5-sgemented. Basal segment subtriangular with
three rectangular teeth broad and spatulate, basal
nodule with three simple setae. Second segment
with pectinate scales in the mid-posterior portion.
Third segment smaller than the second with two
conical spines distally. Fourth flat segment, two
thirds of the length of the third segment. Fifth
segment with two claw-shaped terminal spines and
a projection.
m
Retractile pre-oral spine elongated located midway
between first maxilla; tip extending to midway
between post-antennal spine when retracted;
ventral surface of spine without scales. Mouth tube
less than twice as long as broad, with few scales
scattered around base; denticulate mandibles
visible within mouth tube. Pair of accessory spines
located between the second maxilla (Fig. 3 - A and
C).
Pair of thoracic spines located between the first pair
of legs. First to 4th pairs of legs biramous and of
near equal size; sympods indistinctly 2-segmented.
Flagellum present on 1st and 2nd legs; extending
medially from origin on dorsal surface at base of
exopod; both rami and flagella armed with 2 rows
of plumose setae. Natatory lobe on 4th leg
produced laterally. Simple scales present on
natatory legs (Fig. 2 - F).
A
B
C
D
Figure 4
. Light microscopy photo female of
Argulus yawewitus
sp. n. A – Antenna and antennule; B – natatory flagellum of the
first and second pair of legs; C - eggs in the carapace; and D – forth legs.
Neotropical Helminthology, 2022, 16(2), jul-dic
Jtineant
et al.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
129
Adult male
(Fig. 5)
Based on ten males (INPA - CR 2550). Body shape
rounded (Fig 5AB) with paired incisions of antero-
latera carapace to form defined frontal region and
comprising cephalon, four thoracic somites, and
abdomen, similar to that of female. Total length (tl)
3,6 - 3,99 (3,7 ± 0,16) mm, about 21% smaller than
female (Figura 5). Dorsal surface of yellow color
with light brown designs, softer than in females.
Elliptical carapace, slightly longer than wide.
Carapace length (cl) 2,61 - 3,21 (2,9 ± 0,22). Total
length / carapace length ratio (tl / lc) 1,2 - 1,4 (1,3 ±
0,08).
Thorax indistinctly 4-segmented, smaller,
narrower and less prominent than the female's, with
few light brown pigment spots. Abdomen sub-oval,
lobes tapering to bluntly rounded tips, separated by
sinus 1/6 length of abdomen; furcal rami small,
located adjacent to midline at base of anal sinus;
paired testes oval. Dorsally few light brown
pigment spots.
Cephalic appendages and first pairs of legs like
those of female. Second to fourth pairs of legs
modified by accessory copulatory structures.
Second leg bearing two cup-shaped covered by
simple scales on posterior face of protopod. Third
leg bearing two cup-shaped covered by simple
scales on anterior face of protopod and two cup-
shaped sockets on posterior face located directly
th
above peg on anterior surface of basis of 4 leg.
Anterior surface of basis of fourth leg bearing peg-
like structure and posterior natatory lobes fringed
with plumose setae.
Attachment area: body surface, fin base, gills and
oral cavities.
Etymology.
In the Amazon, the Branchiura are
known by the fishing community as small ray, the
specific name,
yawewitus
derived from the
“yawewit” is the Tupi, brazilian indigenous
language word for ray.
A
B
C
D
Tescles
500
µ
2
00
µ
2
00
µ
2
00
µ
1
Figure 5
. A - Male of
Argulus yawewitus
sp. n.; B - Antenna and antennule; C – Legs; D – Testicles, 1(Copulatory organ
accessory).
Neotropical Helminthology, 2022, 16(2), jul-dic
Argulus yawewitus
sp. n. parasitic of
Arapaima gigas
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
130
DISCUSSION
For Brazil, 13 species of
Argulus
are cited:
A.
nattereri
Heller, 1857;
A. elongatus
Heller, 1857;
A. salminei
Krøyer, 1863;
A. paulensis
Wilson,
1924;
A. carteri
Cunnington, 1931;
A. multicolor
Steckoven, 1937;
A. pestifer
Ringuelet, 1948;
A.
juparanaensis
Lemos de Castro, 1950;
A.
spinulosus
Silva, 1980;
A. amazonicus
Malta &
Santos-Silva, 1989;
A. chicomendesi
Malta &
Varella, 2000;
A. ybatecobe
Souza, Porto & Malta,
2017;
A. celioi
Souza, Porto & Malta, 2018. For
Amazônia six species:
A. multicolor, A. pestifer
,
A.
juparanaensis
,
A. amazonicus
,
A. chicomendesi
,
A.
ybatecobe
, and
A. celioi
.
Argulus yawewitus
sp. n.
is the second species of
Argulus
cited for
A. gigas
,
the first was
A. chicomendesi
.
The morphology of
A. yawewitus
sp. n. resembles
A. flavescens
Wilson, 1916 in its pigmentation
pattern, size and shape of the carapace, eggs
distribution in the carapace lobes, and
ornamentation of the second maxilla basal nodule.
However, whereas in
A. flavescens
the accessory
and post maxillary spines are conical, in
A.
yawewitus
n. sp. they are rectangular teeth with
rounded edges similar to
A. striatus
Cunnington,
1913.
Ventral surface of the cephalic region and anterior
part of the carapace ornamented with regularly
arranged spines, to the height of the first pair of
legs, similar to
A. vittatus
Rafinesque-Schmaltz
1814,
A. angusticeps
Cunnington, 1913 and
A.
exiguus
Cunnington 1913. The first antenna is like
A. fryeri.
According to World Register of Marine Species
(WORMS) there are 159
Argulus
species with 17
synonymised species (Walter & Boxshall, 2021).
Except for
A. japonicus
Thiele, 1900 originally
from Asia, but spread to all continents of the world
except Antarctica. There are 152 Branchiura
species in the world: four in Australia and Oceania,
eleven in Europe, 28 in South America, 35 in
Africa, 37 in Asia and 47 in North America
(Neethling & Avenant-Oldewage, 2016).
The suction cups, or so-called sucking disks,
develop from the first maxillae on each side of the
preoral sting. They have a flat rim covered by a
chitinous exoskeleton with thickenings like ribs
radiating outward. These ribs are variously broken
up into segments, which are characteristic for a
given species. They may be a series of long or short
rods, segments simulating imbricate plates, or an
elongate segment followed by a series of
overlapping plates. The number of support rods of
first maxilla varies only slightly for a given species.
They are used for identification purposes (Meehan,
1940).
The number of support rods of first maxilla in the
Argulus
species ranges from two to 35 sclerites.
Argulus melanostictus
Wilson, 1935 from the
Pacific Ocean collected in the United States and
Thailand is the species that has the highest number
of sclerites ranges from 33-35 (Meehan 1940;
Wilson, 1944). In most species the number of
sclerites ranges from 3 to 21. The minimum
number of sclerites is two and was found in two
North American species:
A
.
appendiculosus
Wilson, 1907 and
A. americanus
Wilson, 1902
(Wilson, 1904). Four species of South America:
A.
violaceus
Thomsen, 1925;
A. pestifer
Ringuelet,
1948;
A. moratoi
Souza, Porto & Malta 2019;
A.
ventanensis
Tanzola & Villegas-Ojeda, 2017
(Thomsen, 1925; Ringuelet, 1948; Souza & Malta,
2018ab; Souza
et al.,
2019; Tanzola & Villegas-
Ojeda, 2017). And no species from Africa has only
two sclerites on the support rods.
Argulus
yawewitus
sp
.
n. is the fifth species of
Argulus
that
has the minimum number (2) of support rods of the
first maxilla. They are composed of two sclerites
of a rectangular shape.
Second to fourth pairs of legs modified by
accessory copulatory structures. Second leg
bearing two cup-shaped covered by simples scales
on posterior face of protopod. Third leg bearing
two cup-shaped covered by simples scales on
anterior face of protopod and two cup-shaped
sockets on posterior face located directly above peg
th
on anterior surface of basis of 4 leg. Anterior
surface of basis of fourth leg bearing peg-like
structure and posterior natatory lobes fringed with
plumose setae.
Second to fourth pairs of legs modified by
accessory copulatory structures. Second leg
bearing two cup-shaped covered by simples scales
on posterior face of protopod. Third leg bearing
two cup-shaped covered by simples scales on
Neotropical Helminthology, 2022, 16(2), jul-dic
Jtineant
et al.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
131
anterior face of protopod and two cup-shaped
sockets on posterior face located directly above peg
th
on anterior surface of basis of 4 leg. Anterior
surface of basis of fourth leg bearing peg-like
structure and posterior natatory lobes fringed with
plumose setae.
In the male, chitinous prominences with thorns on
the legs resemble
A. giordanii
Brian, 1959. The
accessory sexual structures, flag-like protrusions,
present on legs 2 and 3 also occurred in two other
species of Argulus, were found in
A ernsti
Weibezahn & Cobo, 1964 from Venezuela, two on
the second and two on the third pair of legs, still
with different shapes (Weibezahn & Cobo, 1964).
Argulus yawewitus sp. n.
is a unique species,
among its peculiarities we can mention:
ornamentation of antennas 1 and 2, rods supporting
the first maxilla, second maxilla, ornamentation of
the buccal cone, accessory and post-maxillary
spines and ornamentation of the male's legs.
Argulus yawewitus
sp. n. may easily be
distinguished from other species of
Argulus
by a
combination of the following characters: the
format and ornamentation of the first and second
antennas position of the smaller respiratory area is
anterior to the larger one and (2) the ribs of the
suction cups are composed of 9 to 11 imbricated
plates only. In Wilson's (1904) account, there are 22
species of
Argulus
including
A. indicus
with their
respiratory areas arranged as in
A. quadristriatus
.
Among the seven species of
Argulus
known to
occur in India,
A. giganteus
and
A. indicus
have this
type of respiratory areas. In
A. kurafugu
and
A.
scutiformis
from Japanese fishes, Yamaguti &
Yamasu (1959) reported such an arrangement of
the respiratory areas. Of the above cited species,
only
A. melanostictus
,
A. pugettensis
,
A. niger
)
A.
melanostictus
and
A. giganteus
have the
arrangement of the respiratory areas combined
with the fact that the ribs of the suction cups are
exclusively formed of imbricated plates, as in the
present species. However, they differ from
A.
quadristriatus
in the much greater number of these
plates in each rib, viz., 30 in
A. melanostictus
.
The authors thank Maria do Carmo Figueiredo
Soares for collecting and donating the described
specimens of Branchiura. To Matthew Jtineant for
the English review. And to the Laboratory of
Animal Histology and Embryology at the Institute
of Health and Animal Production in partnership
with the Federal Rural University of the Amazon,
for permission to use the electron microscope for
ultrastructural visualization of the specimens
described herein.
ACKNOWLEDGEMENTS
Kabata, Z. 1970.
Diseases of fiches. Crustacea as
enemies of fiches
. Jersey City. T.F.H.
Publications. 171p.
Meehan, OL. 1940.
A review of the parasitic
Crustacea of the genus
Argulus
in the
collections of the United States National
Museum
. Proceedings of the United States
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image/svg+xml
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art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134