ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

Neotropical Helminthology, 2018, 12(1), ene-jun:71-78.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

A NEW SPECIES OF BRANCHIURA (CRUSTACEA: MAXILLOPODA) FISH PARASITE FROM THE

BRAZILIAN AMAZON

UNA NUEVA ESPECIE DE BRANCHIURA (CRUSTACEA: MAXILLOPODA) PARÁSITA DE

PECES DE LA AMAZONIA BRASILEÑA

Laboratório de Parasitologia de Peixes/ Instituto Nacional de Pesquisas da Amazônia-INPA.

Campus II, Av. André Araújo, 2.936 - Petrópolis - CEP 69.067-375 - Manaus – Amazonas, Brasil.

Tel. +55(92) 3643-3613

*corresponding author: atjsouza15@gmail.com

ABSTRACT

Argulus ybatecobe n. sp. was collected parasitizing the body surface of Potamorhina altamazonica (Cope,

1878) (Curimatidae) from Lake Poción, in the complex of lakes of Catalán, municipality of Iranduba,

Amazonas, Brazil. The new species is characterized by ovigerous ducts, extended to the lobes of the

carapace, visible in the female; a pair of spines in the anterior portion of the buccal cone near the jaws;

nd th

accessory sexual structures in the form of a flag in the 2 and 4 pair of legs of the male; second leg with

three structures similar to a flag and the third leg with a rounded structure and caudal branches with long

arrows.

Neotropical Helminthology

Amanda Karen Silva de Souza ; Daniel Brito Porto & José Celso de Oliveira Malta

Key words: Argulidae – sh parasites – River Solimões

RESUMO

Argulus ybatecobe n. sp. foi coletado parasitando a superfície corporal de Potamorhyna altamazonica

(Cope, 1878) do lago Poção, no complexo de lagos do Catalão, município de Iranduba, Amazonas, Brasil.

A nova espécie é caracterizada por dutos ovígeros, estendidos aos lóbulos da carapaça, visíveis na fêmea;

um par de espinhos na porção anterior do cone bucal próximo às mandíbulas; estruturas sexuais acessórias

em forma de bandeira no 2º e 4º par de pernas do macho; segunda perna com três estruturas parecidas com

uma bandeira e a terceira perna com uma estrutura em forma arredondada e ramos caudais com setas

longas.

Palavras-chave: Argulidae – parasitas de peixes – Rio Solimões

Neotropical Helminthology, 2018, 12(1), ene-jun

INTRODUCTION

RESUMEN

Argulus ybatecobe n. sp. fue colectado parasitando la superficie corporal de Potamorhyna altamazonica

(Cope, 1878) del lago Poción, en el complejo de lagos del Catalán, municipio de Iranduba, Amazonas,

Brasil. La nueva especie se caracteriza por ductos ovígeros, extendidos a los lóbulos del caparazón,

visibles en la hembra; un par de espinas en la porción anterior del cono bucal cerca de las mandíbulas;

estructuras sexuales accesorias en forma de bandera en el 2º y 4º par de patas del macho; segunda pata con

tres estructuras parecidas a una bandera y la tercera pata con una estructura en forma redondeada y ramas

caudales con flechas largas.

complex, Iranduba municipality, Amazonas,

Brazil, located between the Negro and Solimões

rivers (03 º 010'04"S; 59 º 054`45" W). Samples

were collected in November 2016, license SISBIO-

6531958 and CEUA – 036/2016. Fishes were

harvested with gill netting. Argulids were

removed, fixed in 70 % ethanol and studied by light

and stereo microscopy.

Temporary glycerin slides were prepared. All

measurements are in millimeters. Drawings were

made in light microscope Olympus BH-2 with

camera lucid. Types, fixed in 70% ethanol, were

deposited in the non-insect Invertebrate Collection

of the National Research Institute of Amazonia

(Female - INPA CR 2291 and Male – INPA CR

2292) Manaus, Amazonas, Brazil.

Argulus ybatecobe n. sp.

Material examined – Holotype adult female (INPA

- CR 2291 and male INPA - CR 2292) from the

body surface of Potamorhyna altamazonica Cope,

1878, from Catalão floodplain lakes complex,

located between the Negro and Solimões rivers

0 0

03 10`04” S 59 54`45” W, State of Amazonas,

Brazil.

Female (Figs. 1 – 11)

Total length 2.8 (Figs. 1 and 2). Elongated body.

Carapace's translucent beige surface with

ovigerous ducts of dense, irregular and brown

Branchiura are ectoparasites both able to attach to

the freshwater fish species slippery bodies and

swim freely to find themselves another host.

Nearly 210 species are known and they belong to

four genera: Argulus Muller, 1785; Dolops

Audouin, 1837; Chonopeltis Thiele 1900 and

Dipteropeltis Calman, 1912 (Martin & Davis,

2001). Branchiura are ectoparasites mainly found

on freshwater fish and yet some species of Argulus

have been described on marine fishes. There are

scattered reports on Branchiura species being

found on tadpoles, salamanders and even alligators

(Ringuelet, 1943; Piasecki & Avenant-Oldewage,

2008).

Thirteen Argulus species occur in Brazil (Malta,

1998; Luque et al., 2013). Five 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 (Malta, 1982; 1983;1984;

1998; Malta & Silva 1986; Malta & Varella, 2000),

have been reported in the Amazon. The present

study includes a description of one new species

from the Amazon, Brazil.

One female and one male of Argulus ybatecobe n.

sp. collected in Lake Poção, in the Catalão

Palabras clave: Argulidae – parásitos de peces – Río Solimões

MATERIAL AND METHODS

RESULTS

Souza et al.

Neotropical Helminthology, 2018, 12(1), ene-jun

all segments bearing short setae; fourth segment

terminating in group of apical spines. Pair of post-

antennal spines rounded on ventral surface of

cephalothorax on either side of midline.

First maxilla forming large suction cups;

supporting rods with 4 - 7 sclerites (Figure 12), rod

elements similar in form; rim of suction cups with a

fringe of setae from anterolateral portion. Second

maxillae (Figure 11) with of 5 segments; basal

plate ornamented with 3 posteriorly directed sharp

teeth and long antero-lateral process, 4 - 5 conical

spines in basal segment nodule; 2 segment with

pectinated scales in the mid-distal portion; 3 and

4th segments very short, with pectinated scales; 5

segment with a spine and two conical structures

with rounded edges (Figs. 8 and 9).

Retractile pre-oral spine, without scales, located

midway between maxillary suckers. Mouth tube of

moderate length, usually not reaching thoracic

accessory spines, bearing a pair of simple spines on

its anterior margin. Denticulate mandibles visible

within mouth-tube (Figure 2).

Pair of accessory spines located between maxillae

(Figure 2) and pair of thoracic spines posterior to

the maxillae (Figure 2). First to 4 pair of legs are

biramous (Figure 6) and nearly equal-sized;

sympods 2-segmented (precoxa, coxa, basis,

exopod, and endopod) exopods and endopods with

plumose setae; no flagellum; legs with simple

scales in the middle ventral portion, rami bearing

long plumose setae. Natatory lobe on 4 leg

(coxopodite expansion) with five plumose setae.

Male (Figures 12 - 16)

Total length 2.92 mm. Surface of translucent beige

carapace, but with a softer and dense coloration

than that in females. Carapace heart-shaped,

slightly more wide than long. Carapace length 1.42

mm (Table 1). Frontal region (Figure 12) more

defined than in females. Lateral lobes broadly

rounded (Figure 12) separated by large V-shaped

sinus less than 1/2 the length of the carapace similar

to females'. Similar duct structure smaller and less

dense than female's. Respiratory areas (Figure 7)

visible only in the ventral region of the carapace.

Thorax (Figure 12) smaller, narrower and less

prominent than the females' with four well defined

somites. Dorsal surface with two irregular

color, the structure of which resembles a tree (Figs.

1 and 2). Carapace more long than wide. Carapace

length 1.7, total length / carapace length (tl / cl) 1.6

ratio. Absent side grooves. Edge of suction cups

visible in dorsal view (Figures 1 and 2). Well

defined interocular ribs. Large paired compound

eyes in anterior third of the body (Figure 1).

Nauplius eye located on dorsal surface near the

center of carapace. Ventral surface of anterior

frontal region armed with numerous, similar-sized

sharply pointed regularly arranged spines beyond

anterior margin of larger respiratory area (Figure

7).

Lateral lobes broadly rounded, extending

posteriorly to cover base of 2 pair of legs (Figures

1 and 2) separated by large V-shaped sinus less than

1/2 the length of the carapace. Carapace length /

width (cl/w) ratio of 0.9. Respiratory areas consist

of a smaller, anterior ovoid “area ” and a larger,

posterior "J-shaped" “area” (Figure 7) gently

defined on the ventral surface of the lobes, little

visible in dorsal view.

Thorax (Figs. 1 and 2) distended with large eggs

and smooth indistinctly 4-segmented ventral

surface. Dorsal surface displaying three

longitudinal bands, the two lateral ones being

formed by irregular patches and the central one

with no patches.

Abdomen more long than wide, length (Figs. 1 and

2) 0.73 and width 0.39. Posterior lobes taper into

sharp tips, separated by sinus, encompassing

nearly 55% of total abdomen length. Spinules in

the dorsal and ventral portions located below the

spermathecae. Caudal rami long, slender, basal in

anal sinus Paired spermathecae small and .

orbicular (Figs. 1 and 2).

First antenna (Figure 10) comprising 2 sections;

the first section is 2-segmented, the broad proximal

and, the slender distal one with a large spine; and

the second section is 4-segmented with setae. First

segment bearing a large rounded posterior spine

and two rounded elevations; second segment

possessing anterior spine with small hook; slender

hook-like terminal spine; two rounded medial

spines. Distal section of antenna comprising 4

segments; terminal section with group of apical

spines. Second antenna (Figure 10) 4-segmented;

first segment with inconspicuous posterior spine;

A new species of Branchiura of the Brazilian Amazon

Figures 1 – 2. Argulus ybatecobe sp. n.; 1 – Dorsal female; 2 – Ventral female (Bar=1.0mm).

Neotropical Helminthology, 2018, 12(1), ene-jun Souza et al.

sinus lanceolate on posterior extremities. Well

defined posterior sinus, with about 42% of the total

length of the abdomen. Large caudal. On each side

of the midline of the abdomen there are pigments

forming small dark spots.

First to fourth pair of biramous legs (swimming

legs, thoracic legs, thoracopods, pereopods) are

nearly equal-sized; sympods 2-segmented

longitudinal bands, the lateral ones being formed

by small circular patches less evident than the

female's.

Abdomen (Figure 12) rectangular slightly more

long than wide. Abdomen width 0.39. Abdomen

length 0.91. Pair of well-defined testicles in the

same format as the abdomen, occupying nearly

90% of the abdominal area. Lobes with the anal

Figures 3-11. Argulus ybatecobe sp. n., 3 – respiratory area (Bar=1.0mm); 4 – 7 legs female (Bar=1.0mm); 8 – maxilla

1(Bar=0.1mm); 9 maxilla 2 (Bar=1.0mm); 10 – distal portion maxilla 2 (Bar=0.1mm); and 11 - Antennas.

Neotropical Helminthology, 2018, 12(1), ene-jun A new species of Branchiura of the Brazilian Amazon

10 11

of legs include a strong anterior projection with a

median aperture having the inner "U" shape

covering the gonopore Natatory lobes are short .

and rectangular bearing four plumose setae.

Area of attachment: body surface, fins base, gills

and buccal cavities.

Etymology: The specific name Argulus ybatecobe

refers to the structure that resembles a tree formed

by ducts in the carapace lobes, where eggs are

stored, the name derives from the Tupi-Guarani

language (ybá = tree + tecobe = life), tree of life.

(precoxa, coxa, basis, exopod, and endopod)

exopods and endopods with plumose setae (Figure

13 - 16). First pair of legs like the females.

nd rd th

Secondary sexual modifications on 2 , 3 and 4

pair of legs.

Accessory copulatory structures on second leg

consist of three flag-like protrusions (Figure 14 and

15). Third leg with one rounded flag-like

protrusion (Figure 16). Fourth leg with peg process

on anterior side modified at the point of opposition

of the cup-shaped elevation (accessory copulatory

structure). Modifications of the male's fourth pair

Figures 12 – 16: 12 – Dorsal male Argulus ybatecobe sp. n. (Bar=1.0mm); Legs Male, 13- leg 1; 14 – leg 2; 15 – leg 3; and 16 – leg

4(Bar=1.0mm).

Neotropical Helminthology, 2018, 12(1), ene-jun Souza et al.

DISCUSSION spines in the anterior portion near the mouth,

nd rd th

accessory flag-like sexual structures on 2 3 , 4

legs. Second leg has three flag-like structures and

the third leg one rounded flag-like structure in the

male. Caudal rami with long setae and a pair of

spines in the anterior portion near the mouth.

Argulus ybatecobe n. sp. is the sixth species of the

genus Argulus cited for the Amazon. Argulus

ybatecobe is like A. chicomendesi Malta & Varella,

2000. But it differs because it is smaller, by the

presence of spines in the ventral region of the

carapace between the first and second maxilla, in

the form of respiratory areas, in the accessory

copulatory structure of the second, third and fourth

legs of the male and in the tree-shaped ovigerous

ducts,, evident in the lobes of the carapace.

Accessory sexual structures in flag-like form on 2

rd th

3 , 4 legs also occurred in two other species, A.

ernsti Weibezahn & Cobo, 1964 from Venezuela,

two flag-like structures in flag-like form ion the

second and two in the third pair of legs with

different shapes (Weibezahn & Cobo, 1964). And

A. smalei Avennant-Oldewage & Oldewage, 1995

from South Africa, on posterior face of 2 leg flat

disc covered by pectinate scales. Two bulbous and

flag-like protrusions covered by scales on anterior

face of 3 leg (Avennant-Oldewage & Oldewage,

1995). On Argulus ybatecobe n. sp. the structures

on second leg consist of three flag-like protusions

and, on the third leg one rounded flag-like

protrusion.

The mouth tube of Argulus fryeri Rushton-Mellor,

1994 from Lake Turkana, Kenya, Africa, bears a

pair of accessory spines located posterior to mouth-

tube. Argulus gracilis Rushton-Mellor, 1994 from

Lake Tanganyika exhibits a pair of accessory

spines located on either side of labium (Rushton-

Mellor, 1994). Argulus ybatecobe n. sp. also

displays a pair of simple spines on its anterior

margin of mouth tube.

Carapace slightly more long than broad like A.

pestifer Ringuelet, 1948. But partly covering the

second pair of legs in A. ybatecobe being like A.

chicomendesi (Malta & Varella, 2000). In Argulus

ybatecobe n. sp. duct is seen to store eggs (observed

for egg storage) in the carapace lobes, a unique

characteristic not observed in other species already

described.

Argulus ybatecobe n. sp. is characterized by

ovigerous ducts, extending to the carapace lobes,

visible in the female. By the presence of a pair of

Avenant-Oldewage, A & Oldewage, WH. 1995. A

new species of Argulus (Crustacea:

Branchiura) from a bony fish in Algoa Bay,

South Africa. South African Journal of

Zoology, vol. 30, pp. 197-199.

Luque, JL, Vieira, FM, Takemoto, RM, Pavanelli,

GC & Eiras, JC. 2013. Checklist of

Crustacea parasitizing fishes of Brazil.

Checklist, vol. 9, pp. 1449–1470.

Malta, JCO. 1982. 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. 1983. Os argulídeos (Crustacea:

Argulidae) da Amazônia brasileira.

Aspectos da ecologia de Argulus multicolor

Stekhoven, 1899 e A. pestifer Ringuelet,

1948. Acta Amazonica, vol. 13, pp. 489-

496.

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 & Silva, ENS. 1986. Argulus

amazonicus n. sp., crustáceo parasito de

p e i x e s d a A m a z ô n i a b r a s i l e i r a

(Branchiura: Argulidae). Amazoniana, vol.

9, pp. 485-492.

Malta, JCO. 1998. Maxilipoda – Branchiura. In:

Young, Y. (Ed). Catalogue of Crustacea of

Brazil. Museu Nacional, Rio de Janeiro. pp.

67-74.

Malta, JCO & Varella, AMB. 2000. Argulus

chicomendesi n. sp. (Crustacea:

Argulidae) parasita de peixes da Amazônia

brasileira. Acta amazonica, vol. 30, pp.

BIBLIOGRAPHIC REFERENCES

Neotropical Helminthology, 2018, 12(1), ene-jun A new species of Branchiura of the Brazilian Amazon

(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.

Weibezahn, FH & Cobo, T. 1964. Seis argulidos

(Crustacea: Branchiura) parásitos de peces

dulce-acuícolas en Venezuela, con

descripción de una nueva especie del

g e n e ro Argulus. A ct a B i o l o g i c a

Venezuelica, vol. 4, pp. 119–144.

481–498.

Martin, W & Davis, GE. 2001. An Updated

Classification of the Recent Crustacea.

Natural History Museum of Los Angeles

County. Contributions in Science Series 39,

pp. 1-124.

Piasecki, WT & Avenant-Oldewage, A. 2008.

Diseases caused by Crustacea. In: Eiras J,

Segner J, Wahli T & Kapoor, BG. Fish

disease. Science Publisher, Enfield, NH. pp.

1113–1198.

Ringuelet, R. 1943. Revision de los Argúlidos

Argentinos (Crustacea, Branchiura): con el

catálogo de las especies Neotropicales.

Revista del Museo de la Plata. Seccion

Zoologia, vol. 3, pp. 43-99.

Rushton-Mellor, SK. 1994. The genus Argulus

Received February 22, 2018.

Accepted April 6, 2018.

Neotropical Helminthology, 2018, 12(1), ene-jun Souza et al.