ORIGINAL ARTICLE /ARTÍCULO ORIGINAL

BIODIVERSITY OF MONOGENOIDEANS FROM RED PIRANHA PYGOCENTRUS

NATTERERI (KNER, 1958) (CHARACIFORMES: SERRASALMIDAE) IN CENTRAL

AMAZONIA: OCCURRENCE AND TAXONOMY

BIODIVERSIDAD DE MONOGENÓIDEOS DE LA PIRAÑA ROJA PYGOCENTRUS

NATTERERI (KNER, 1958) (CHARACIFORMES: SERRASALMIDAE) EN LA

AMAZONÍA CENTRAL: OCURRENCIA Y TAXONOMÍA

1,2 1

Aprigio Mota Morais & José Celso de Oliveira Malta

1INPA – National Research Institute of Amazonia, Fish Parasitology and Pathology Laboratory, Manaus, AM.

2"Superior level personnel improvement coordination (CAPES)" "Post-doctoral national program" (PNPD).

Corresponding author: e-mail aprigio.mota@inpa.gov.br or aprigiomota@yahoo.com.br

CEP 69011-970 Phone (55) (092) 3643-3378.

Neotropical Helminthology, 2015, 9(2), jul-dec: 265-276.

ABSTRACT

Keywords: fish ectoparasites - floodplain lakes - Pygocentrus nattereri - Solimões River.

The present paper describes the fauna of Monogenoidea parasitizing Pygocentrus nattereri

(Kner, 1958) : Namely, captured in six Solimões River floodplain lakes in Central Amazonia

Baixio, Preto, Iauara, Ananá, Campina and Maracá, located between the cities of Manaus and

Coari, Brazil. It adds information to the earlier described species, and cites new records. Three

hundred and fifty-five (355) P. nattereri specimens were captured during the months of March,

June, September and December 2008. They were collected and identified: 50,987

monogenoidean specimens, in seven genera and sixteen species. A new species of Anacanthorus

Mizelle and Price, 1965 was found, yet its number of individuals was too small to enable a

detailed description. This study presents the first record of a new Gyrodactylidae species

parasitizing P. nattereri. The large diversity of Monogenoidea species, which utilize P. nattereri

as their host, points out to the major role this species of fish plays in maintaining the diversity in

the floodplain lakes in Central Amazonia.

265

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

INTRODUCTION

266

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015

The biodiversity of Amazonian fishes is

significantly high and relatively well studied

with respect to other Brazilian River Basins.

But, in face of the large diversity of fishes

being found, the knowledge on parasite species

as well as their life cycles, still has much to be

further investigated (Thatcher, 2006; Silva-

Souza et al., 2006).

In the past few years, fish parasites have been

recognized as a major component of the Global

diversity (Poulin & Morand, 2004). Despite

this recognition having been intensified by

several, current scientific studies, there are

signs indicating parasites to keep on being an

underestimated component of the total

biodiversity in many parts of the world (Luque

& Poulin, 2007).

Fish parasite species must be treated as an

integrating and important component of the

natural communities, not only because they

represent a substantial part of the species

biodiversity and biomass (Poulin & Morand,

2004). But also on account of the indirect and

direct influence they exert on the community

framework and free living species relative

abundance, respectively (Wood et al., 2007).

In Amazonia, with over 3000 fish species

described, a little less than 300 fish metazoan

parasite species are known. A modest

evaluation estimating each fish species to be

harboring at least fifteen species of those

organisms comes up to at least 45000 parasite

species, and thus, 44700 of them still remain to

be described for science (Malta & Varella,

2006; Thatcher, 2006).

Therefore, a lot of fish parasite species still

remain to be collected and identified, despite

the ever fewer, remaining taxonomists and

systemats (Brooks, 2000). Since parasites can

only be studied following the species scientific

recognition, biodiversity estimations for any

geographical area are not always a true picture

of their actual diversity (Overstreet, 1997;

Poulin & Morand, 2004; Eiras et al., 2010).

RESUMEN

Palabras clave: Ectoparásitos de peces - lagos inundables - Pygocentrus nattereri - Río Amazonas.

Fue descrita la fauna de parásitos de la clase Monogenoidea en Pygocentrus nattereri capturados

en seis lagos inundables del río Amazonas en la Amazonía Central: Baixio Negro Iauara, Ananá,

Campina y Maracá, localizados entre las ciudades de Manaus y Coari, Brasil. Fueron adicionadas

informaciones a las descripciones originales de las especies ya descritas y fueron citadas nuevas

ocurrencias. Fueron capturados 355 P. nattereri durante los meses de marzo, junio, septiembre y

diciembre de 2008. Los peces median 15,4 cm ± 3,5 y pesaban 230,9 g ± 2,7. Fueron colectados y

determinados, hasta el menor taxón posible 50,987 especímenes de Monogenoidea, divididos en

siete géneros y 16 especies. Fue encontrada una nueva especie de Anacanthorus sp., sin embargo

el número de individuos fue muy bajo para hacer la descripción correspondiente. Fue realizado el

primer registro de una especie de la familia Gyrodactylidae parasitando P. nattereri. La gran

diversidad de especies de Monogenoidea que utilizan a P. nattereri como huésped indica la

importancia del rol que esta especie de pez posee para mantener la biodiversidad en los lagos

inundables de la Amazonía Central.

Morais & Malta

Taxonomical studies addressing the discovery

of new species and their occurrences represent

both a major contribution to the knowledge on

the biodiversity of any determined area as well

as the basis for other parasite ecology studies

such as environmental management, biotic

integrity and river basins conservation (Luque

& Poulin, 2007).

Considering the importance of fish parasites as

key biodiversity components, the knowledge

pertaining to whether their number is

decreasing or not in a determined environment,

becomes crucial when one undertakes

environmental management and conservation

actions. Moreover, these organisms may be

utilized as indicators of the stability being

found at a given environment (Poulin, 2004;

Luque & Poulin, 2007).

Amongst the countless number of Amazonian

fish species, Pygocentrus nattereri (Kner,

1958) commonly known as red piranha, stands

out. It harbors a considerable number of

parasite species that utilize it as an

intermediary, paratenic and definitive host.

Furthermore, it plays a determinant role as a

sustainer of several parasite species, which

contributes directly on increasing their local

biodiversity (Boeger & Thatcher, 1988;

Morais et al., 2014).

The present study aims to carry out the

characterization of the Monogenoidea fauna

from P. nattereri. Fish specimens were

captured at Central Amazonian floodplain

lakes, every parasite species was identified,

new occurrences were recorded and the

geographical distribution was widened.

Six floodplain lakes located on the Solimões

River banks, were sampled: Baixio

267

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015

(03°17'27,2” S/60°04'29,6” O); Preto

(03°21'17,1” S/ 60°37'28,6” O); Iauara

(03°36'39,2” S/ 61°16'33,0” O); Ananá

( 0 3 ° 5 3 ' 5 4 , 8 ” S / 6 1 ° 4 0 ' 1 8 , 4 ” O ) ,

Campina,(03°46'15,8” S/ 62°20'10,3” O) and

Maracá (03°50'32,8” S/ 62°34'32,4” O), All

located between the cities of Manaus and Coari

in the state of Amazonas (Figure 1).

Four quarterly trips were undertaken in March,

June, September and December 2008. The

fishing effort was standardized in all sampling

sites, through the use of gill nets. The nets

staying time in the water was of approximately

10 h per lake, day and evening periods, with

two fish groundings every five hours.

A necropsy record was filed for each fish

specimen. Necropsies were performed in the

field following an adapted protocol from the

Fish Parasitology and Pathology Laboratory at

the National Research Institute of Amazonia

(LPP-INPA) described in Morais et al. (2011).

All monogenoidean specimens found were

collected, fixed and prepared following a

specific methodology (Amato et al., 1991;

Kritsky et al., 1995; Kritsky & Stockwell,

2005). Drawings were made with the aid of a

light optical microscope with phase contrast

using a camera lucida and digitalized on a

“Kanvus Life 127 - TB-LIFE 127” digitalizing

table.

The photomicrography of the smaller

specimens was done with an optical

microscope and those of the larger ones with a

stereoscope microscope with a coupled digital

camera. All measurements and scales were

made with the aid of . All an ocular micrometer

measures are in micrometers or millimeters

with the means between brackets. When that

did not occur, the corresponding unit was

indicated.

The types and voucher material were deposited

at the non-insect invertebrate collection of

Biodiversity of monogenoideans from Pygocentrus nattereri

MATERIAL AND METHODS

268

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Morais & Malta

INPA in Manaus. Voucher numbers are

recorded following the species number

between brackets.

Three hundred fifty-five (355) P. nattereri

captured at six floodplain lakes in Central

Amazonia, were collected and examined. Fish

specimen measured 15.4cm ± 3.5 and weighed

230.9g ± 2.7. We collected and identified

50,987 Monogenoidea class specimens

included in the seven genera and 16 species

related below.

Seven, Amphithecium Boeger & Kritsky 1988

genus, species: A. brachycirrum Boeger &

Kritsky 1988(INPA 611, 612); A. calycinum

Boeger & Kritsky, 1988; A. camelum Boeger &

Kritsky 1988 (INPA 603, 604); A. catalaoensis

Boeger & Kritsky, 1988; A. falcatum Boeger &

Kritsky, 1988 (INPA 608, 609); A. junki

Boeger & Kritsky 1988 (INPA 610) and A.

microphalum Kritsky, Boeger & Jégu 1997

(INPA 605).

Four, Anacanthorus Mizelli & Price 1965

genus, species: A. thatcheri Boeger & Kritsky,

1988 (INPA 606, 607); A. reginae Boeger &

Kritsky 1988 (INPA 615, 616, 617); A.

stachophallus Kritsky, Boeger & Van Every,

1992 and Anacanthorus sp (INPA 618).

One, Enallotecium Boeger & Kritsky, 1988

genus, species: E. aegidatum Boeger &

Kritsky, 1988 (INPA 602) and one,

Nothotecium Boeger & Kritsky, 1988 genus,

species: N. mizellei Boeger & Kritsky, 1988

(INPA 598, 599).

One, Nothozothecium Boeger & Kritsky, 1988

genus, species: N. penetrarum Boeger &

Kritsky, 1988 (INPA 600, 601). One,

Rhinoxenus Kritsky, Boeger & Thatcher, 1988

genus, species: R. piranhus Kritsky, Boeger &

Thatcher, 1988 (INPA 613, 614) was the only

species occurring in the nostrils. One,

Gyrodactylidae family; Gyrodactylus

Nordmann, 1832 genus, species: Gyrodactylus

sp (INPA 619).

All, Monogenoidea species morphometric

measures and morphological characters

presented in this study are similar to those

found in: Boeger and Kritsky (1988); Kritsky

et al. (1988) Kritsky et al. (1992); Kritsky et al.

(1996); Kritsky et al. (1997a); Kritsky et al.

(1997b); Kritsky et al. (1998) and Viana

(2007) mainly body measures and sclerotized

structures (Table 1 and Figure 2).

Amphithecium falcatum resembles A.

calcynum in the haptor sclerotized structures

possessing non scythe-shaped terminations on

the accessory piece. However, A. falcatum

possesses sliced cirrus ending whereas this

structure shows to be really sharp-pointed in A.

calcynum.

Amphithecium camelum is the only species of

the genus that possesses a dorsal protuberance

on its runk that gives rise to its name. Its t

anchors and bars are visibly different and its

vitellaria are laterally fringed. The copulatory

complex structure points out a relationship

with A. cataloensis. Two morphological forms

are recognized for A. camelum, the “Amazonas

form” and the “Rondônia form”. The form

found in this study was that of “Amazonas”

which presents substantially different

structures such as larger copulatory complex,

bars and hooks when compared to the “

Rondônia form”.

Amphithecium cataloensis resembled A.

camelum in the copulatory complex

morphology and long anchor shafts. However,

it differed from A. camelum by the absence of a

slit ventral bar, and on account of presenting a

longer rod on the hook. Amphithecium junki

has anchors similar to those of A. cataloensis,

but differing by possessing a blade-shaped

cirrus branch, in addition to hooks with rods or

RESULTS

269

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015

wings on the shorter anchor.

Amphithecium microphalum is the only

species that shows an anteromedially

posterodorsal retrocession on the ventral bar.

The copulatory complex is smaller than that of

all other species found, which originated its

specific name.

Anacanthorus reginae differs from all other

earlier described Anacanthorus species by

possessing, on the accessory piece, a variable

expansion in the sub-terminal region. It is

apparently related with the haptor and hooks

comparati v e morphology - b a s ed A .

neotropicalis.

Only five specimens of Anacanthorus sp. were

collected, which is an insufficient number to

enable a thorough description. However, it has

a hood-like basal prominence on the cirrus and

a small, triangular sclerotized protuberance on

the median region of the accessory piece, are

its marking characteristics. The analyzed

specimens do not fit into any described

species, but are related with A. reginae, yet the

differences both on the cirrus and accessory

piece distinguish it from the other species of

the genus.

Enallotecium aegidatum differs from

Enallotecium cornutum and E. umbelliferum

by having anchors with lengthened shafts and

points of short duration. It differs from E.

variabilum by possessing a more distal and

robust rod and a less developed protuberance

on the accessory piece and the dorsal anchor

being slightly smaller than the ventral one.

Rhinoxenus piranhus has the presence of the

dorsal anchor modified in one hook-shaped

sclerite and the absence of a dorsal bar as its

marking characters. Rhinoxenus piranhus

resembles R. arientinus by presenting only

ventral bars and modified dorsal anchor, yet

they differ on the presence of two pairs of

hooks located on two lateral lobules of the

trunk and two sclerotized edges present only in

R. arientinus.

The number of Gyrodactylus sp. samples was

insufficient to enable making a thorough

description; the specimens found were located

on the host's body surface.

Biodiversity of monogenoideans from Pygocentrus nattereri

Figure 1. Study area geographical localization in Central Amazonia – AM.

63º0'0'W

4º0'0''S

5º0'0''S

62º0'0'W

61º0'0'W

60º0'0'W

Monogenoidea

Species

Body

lenght

Body wider

width

Haptorial

lenght

Haptorial

width

Pharingeal

diameter

Ventral

anchor lenght

Ventral bar Dorsal bar Cirrus

lenght

Acessory piece

lenght

Dorsal

spine

Superficial

bar

Amphithecium

brachycirrum

210 (199-

222)

64 (52-75) 42 (39-46) 54 (52-59) 15 (11-17) 28 (24-30) 29 (28-33) 29 (28-31) 16 (13-21) 12 (8-15) - -

Amphithecium

calycinum

203 (195-

215)

60 (53-72) 40 (38-44) 54 (52-58) 12 (10-14) 28 (24-29) 30 (26-33) 28 (27-31) 17 (12-20) 12 (9-14) - -

Amphithecium

camelum

392 (339-

482)

50 (45-53) 52 (49-60) 70 (64-81) 23 (18-25) 46 (40-50) 42 (38-45) 32 (28-33) 50 (49-55) 30 (28-37) - -

Amphithecium

cataloensis

390 (282-

361)

89 (71-96) 20 (18-22) 77 (62-90) 19 (16-22) 70 (69-75) 44 (39-49) 43 (38-51) 53 (52-55) 35 (33-38) - -

Amphithecium

falcatum

230 (195-

239)

81 (52-85) 42 (35-39) 62 (55-70) 16 (12-18) 26 (25-30) 27 (26-30) 26 (26-28) 38 (30-41) 31 (22-36) - -

Amphithecium

junki

240 (189-

265)

68 (42-75) 49 (35-52) 62 (52-75) 14 (10-16) 43 (39-45) 36 (33-38) 36 (32-37) 28 (25-30) 24 (22-29) - -

Amphithecium

microphalum

350 (340-

399)

125 (95-

135)

67 (64-70) 85 (80-92) 23 (19-25) 40 (38-42) 47 (43-49) 35 (33-37) 18 (16-20) 14 (11-16) - -

Anacanthorus

reginae

450 (290-

490)

120 (90-

135)

51 (48-65) 85 (49-110) 30 (22-33) - - - 70 (59-75) 60 (48-65) - -

Anacanthorus

thatcheri

700 (620-

704)

130 (125-

150)

60 (57-75) 131 (110-

155)

39 (36-42) - - - 80 (70-91) 80 (75-94) - -

Anacanthorus

stachophallus

575 (560-

625)

155 (125-

182)

80 (75-90) 115 (110-

117)

39 (36-41) - - - 60 (57-61) 58 (57-59) - -

Anacanthorus

sp.

690 (600-

700)

50 (55-73) 125 (115-

145)

131 (110-

155)

42 (39-50) - - - 88 (73-98) 86 (71-90) - -

Enallotecium

aegidatum

230 (214-

246)

69 (67-95) 40 (37-49) 76 (75-90) 11 (12-15) 33 (32-40) 41 (39-41) 40 (39-42) 21 (20-24) 18 (15-19) - -

Nothotecium

mizellei

249 (180-

255)

79 (70-85) 58 (50-60) 85 (80-92) 15 (11-16) 58 (57-60) 43 (41-45) 33 (31-35) 25 (23-26) 22 (21-23) - -

Nothozotheciu

m penetrarum

1350 (1001-

1400)

390 (310-

420)

160 (145-

172)

145 (140-

156)

75 (67-82) 36 (33-39) 42 (39-44) 37 (34-41) 211 (209-

213)

65 (54-68) - -

Rhinoxenus

piranhus

702 (680-

730)

170 (165-

199)

109 (107-

113)

110 (76-

115)

33 (32-36) 125 (122-

132)

55 (49-57) - 179 (173-

182)

49 (45-56) 119 (115-

125)

Gyrodactylus

sp.

700 (388-

750)

240 (185-

295)

192 (165-

213)

154 (130-

170)

81 (70-98) 101 (100-

105)

- - *29 (22-

36)

- 55(45-39)

270

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Morais & Malta

Table 1. Morphometric characters measuring matrix of Monogenoidea species parasitizing Pygocentrus nattereri. (measures in mµ).

*Masculine Copulatory Organ diameter (MCO).

271

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Biodiversity of monogenoideans from Pygocentrus nattereri

Amphithecium microphalum Amphithecium thatcheri Anacanthorus reginae Anacanthorus stachophallus Anacanthorus sp. Enallotecium aegidatum

Amphithecium falcatusAmphithecium brachycirrum Amphithecium calycinum Amphithecium camelum Amphithecium cataloensis Amphithecium junki

Figure 2. Anchors, ventral and dorsal bars complex, and copulatory complex of the species of monogenoideans described on

Pygocentrus nattereri.

Figure 3. continuation. Anchors, ventral and dorsal bars complex, and copulatory complex of the species of monogenoideans

described on Pygocentrus nattereri.

272

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Morais & Malta

simple base while that of A. stacophallus is C-

shaped. These observations agree with what

was observed initially by Boeger & Kritsky

(1988) and later by Kritsky et al. (1992) on P.

nattereri collected at Ilha da Marchantaria

lakes, Solimões River, State of Amazonas.

Enallotecium aegidatum was originally

described as N. aegidatum by Boeger &

Kritsky (1988) parasitizing the gills of P.

nattereri, and placed in Enallothecium genus

by Kritsky et al. (1998).

This species apparently possessing low

specificity was found on nine hosts of genera

Prystobrycon Eigenmann, 1915, Pygocentrus

(Müller & Troschel, 1844) and Serrasalmus

Cuvier, 1819, though they were not reported in

the original description. Notothecium

aegidatum described in this study, possesses a

small, weakly sclerotized drop or umbrella-

like protuberance on the accessory piece

similar to what was described by Kritsky et al.,

(1998).

Notothecium mizellei was designated as type

species for this genus. Specimens found in this

study do not differ from those utilized in the

studies of Boeger & Kritsky (1988) and

Kritsky et al. (1997b). In does not have a

ventral aperture similar to what was found by

Kritsky et al. (1997b). In this study N. mizzelei

differed from the other species by being the

only one possessing two protruding branches

on its copulatory organ.

Notozothecium penetrarum is type species of

the genus; the specific name is due to the

peculiar way the adults penetrate through the

haptor into the gill filament tissues. This

results into a relatively permanent fixation on

the gills, causing a major damage on the

penetrating site. It also stands out by

presenting larger body length and width than

other species.

It is considered to be the largest species of the

DISCUSSION

Amazonian fish parasite biodiversity has been

increasing with new descriptions being

reported from year to year. Nearly 472

parasitic species, distributed into protozoans

and metazoans, have been described so far,

they represent 4% of the parasite fauna

estimated for the fishes in the region, and P.

nattereri as the major host harboring the largest

number of metazoan parasite species (Morais

et al., 2011).

Differences in Amphithecium genus species

are based on the anchors, hook and bars

morphology (Boeger & Kritsky, 1988; Kritsky

et al. 1997a). The same authors described the

seven species found in this study, including A.

calcynum, the type species of this genus.

All species of Amphithecium genus possess a

hook-shaped termination on the cirrus

accessory piece, but for A. brachycirrum, as

observed by Boeger & Kritsky (1988). Other

specific differences on the species found in the

present study corroborate the ones determined

by Boeger & Kritsky (1988) and Kritsky et al.

(1997a).

Anacanthorus stacophallus, first recognized

by Boeger & Kritsky (1988) as Anacanthorus

sp. and later described by Kritsky et al. (1992)

as A. stacophallus is easily distinguished by

the copulatory complex morphology. Hence,

A. stacophallus is considered A. thatcheri

sister species, but differing in the accessory

piece morphology. Anacanthorus stacophallus

presents diagonal, basal aperture on the cirrus

proximal extremity, while in A. thatcheri it

shows to be lateral (Kritsky et al., 1992).

The differences observed between A.

thatcheri, A. reginae and A. stacophalus in this

study are found in the cirrus morphology.

Anacanthorus thatcheri possesses hook-like

cirrus; A. reginae presents cirrus with J-shaped

similar to that of Gyrodactylus sp.n.4., found

by Viana (2007). Nevertheless, since the

specimens in this study were not stained with

Gomori trichrome, we were unable to assert

them to belong to the same species, since the

staining can give a false appearance to their

superficial shield. This is the first record of a

species of the family Gyrodactylidae

parasitizing P. nattereri.

Therefore, in spite of all morphological and

morphometric characters found in

Gyrodactylus sp., being in conformity with

Gyrodactylus sp.n.4, the absence of the shield

on Gyrodactylus sp. may be an effect from the

mounting of the specimens on the slide which

occurred in Hoyer's solution, not allowing us to

assert them to be the same species. Thus, new

collections and ways of preparing slides with

Gomori trichrome as a staining technique must

be considered in the identification of that

species so as to be able to confirm the absence

of the shield, or not.

Works as those of Vital et al. (2011) and

Boeger & Kritsky (1988) recorded the high

parasite diversity of Monogenoidea for P.

nattereri. Of the 308 species of Monogenoidea

recorded in 144 freshwater fish species

described for the Neotropical region (Boeger

et al., 2006), 28 of them, that is, 9.1%

parasitize P. nattereri.

Since the monogenoideans possess a high

degree of parasite specificity, occurring on one

host or on very phylogenetic close hosts (Cone

& Kurt, 1982). Pygocentrus nattereri

represents a major host for this group of

parasites since these possess a direct life cycle

depending only on that host to complete their

life cycle.

Of the 28 species of Monogenoidea parasites

described for P. nattereri, 15 of them were

determined in the present work. The species

were similar to those described in the works of

Boeger & Kritsky (1988) and Vital et al.

genus (Boeger & Kritsky, 1988). The

morphometric measures corroborate those

reported by Boeger & Kritsky (1988) and

Kritsky et al. (1996). There are small

differences on the amplitudes; the specimens

in this study presented the highest values.

Rhinoxenus piranhus is specific to the nostrils

and the morphological and structural

characteristics are in accordance with those of

the species determined by Kritsky et al. (1988).

According to these authors the modifications

of the haptor in R. piranhus as well as in the

other species of the genus are apparently

related with the needs required to get fixed on

the surface of the nostrils.

Our viviparous species of Monogenoidea of

the family Gyrodactylidae of the genus

Gyrodactylus were described as collected on

the body surface of Characiformes of Brazil.

One of them was Gyrodactylus sp.n.4 parasite

of S. rhombeus Linnaeus, 1766) which is a (

species whose phylogeny is very close to P.

nattereri (Viana, 2007).

The species Gyrodactylus sp. found in this

study presented a pair of anchors with the

superficial root and point overpassing the

haptor border boundaries. This characteristic

was also observed in G. traira and Kritsky et

al. (1995) parasite of Hoplias malabaricus

(Bloch, 1794).

The absence of the shield of the superficial bar

of Gyrodactylus sp. was also observed in

Gyrodactylus sp.n.3, a species also described

by Viana (2007). However, Gyrodactylus

sp.n.3 possesses small anterolateral

protuberances on the superficial bar and the

platform of the head of the hook is convex,

characteristics absent from Gyrodactylus sp.

and Gyrodactylus sp.n.4.

In this study were collected specimens of

Gyrodactylus sp. which characterizes itself by

presenting a superficial bar shield not very

273

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Biodiversity of monogenoideans from Pygocentrus nattereri

274

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Morais & Malta

(2011). These figures confirm P. nattereri as

the freshwater fish species harboring the

largest number of parasite species in Brazil.

The high parasitic diversity comprised by

different taxonomic groups in distinct and

complex life cycle stages, demonstrates the

importance of P. nattereri as a direct sustainer

of 55 invertebrate parasite species. This fact

reveals the determining role this fish species

plays in contributing to increase and maintain

the biodiversity in Amazonian floodplain lakes

as well as any other environment this species

may occur.

Funding this research was financially

supported by the PIATAM project And

INPA/MCTI.

the Central Amazon. Proceedings of the

H e l m i n t h o l o g i c a l S o c i e t y o f

Washington, vol. 55, pp. 87-90.

Boeger, WA, Vianna, RT & Thatcher, VE.

2006. Monogenoidea. p. 43-116. In:.

Adis, J.; Arias, J.R.; Rueda-Delgado, G.

& Wantzen, K.M. (Eds.). Aquatic

Biodiversity in Latin America, Pensoft,

Second edition Sofia, Bulgaria.

Brooks, DR. 2000. Parasite systematics in the

s t

21 century: opportunities and

obstacles. Memórias do Instituto

Oswaldo Cruz, vol.95, pp. 99-107.

Cone, DK & Kurt, MDB. 1982. The host

especifity of Urocleidus adspectus

( M u l l e r, 1 9 3 8 ) ( M o n o g e n e a :

An c yrocep h al i n a e) . Journal of

Parasitology, vol. 75, pp. 702-706.

Eiras, JC, Takemoto, RM & Pavanelli, GC.

2010. Diversidade dos parasitas de

peixes de água doce do Brasil. Maringá,

PR: Clichetec, NUPELIA, Maringá,

Brasil. pp. 333.

Kritsky, DC, Boeger, WA & Thatcher, VE.

1988. Neotropical Monogenea. 11.

Rhinoxenus gen. n. (Dactylogyridae:

Ancyrocephalinae) with descriptions of

three new species from the nasal cavities

o f A m a z o n i a n C h a r a c o i d e a .

Proceedings of the Biological Society of

Washington, vol. 101, pp. 87-94.

Kritsky, DC, Boeger, WA & Van Every, LR.

1992. Neotropical Monogenoidea. 17.

Anacanthorus Mizelle & Price, 1965

(Dactylogyridae, Anacanthorinae) from

Characoid fishes of the Central Amazon.

Journal of the Helminthological Society

of Washington, vol. 59, pp. 25-51.

Kritsky, DC, Boeger, WA & Popazoglo, F.

1995. Neotropical Monogenoidea. 22.

Variation in Scleroductus species

(Gyrodactylidea, Gyrodactylidae) from

Siluriformes fishes of Southeastern

Brazil. Journal of Helminthology

Society of Washington, vol. 62, pp. 53-

56.

Kritsky, DC, Boeger, WA & Jégu, M. 1996.

ACKNOWLEDGEMENTS

Amato, JFR, Boeger, WA & Amato, SB. 1991.

Protocolos para laboratório coleta e

processamento de parasitas do pescado.

Imprensa Universitária, Universidade

Federal do Rio de Janeiro, Rio de

Janeiro, Brasil. pp. 81.

Boeger, WA & Kritsky, DC. 1988. Neotropical

Monogenea. 12. Dactylogyridae from

S e r r a s a l m u s n a t t e r e r i ( K n e r )

(Cypriniformes, Serrasalmidae) and

aspects of their morphologic and

distribution variation in the Brazilian

A m a z o n . P r o c e e d i n g s o f t h e

H e l m i n t h o l o g i c a l S o c i e t y o f

Washington, vol. 55, pp. 188-213.

Boeger, WA & Thatcher, VE. 1988.

Rhinergasilus piranhus gen. et sp. n.

(Copepoda, Poecilostomatoida ,

Ergasilidae) from the nasal cavities of

piranha caju, Serrasalmus nattereri, in

BIBLIOGRAPHIC REFERENCES

fishes: hotspots and the geography of

biodiversity. Parasitology, vol. 134, pp.

865-878.

Malta, JCO & Varella, AMB. 2006. Os

crustáceos branquiúros parasitas de

peixes (Argulidae: Maxillopoda). pp.

17-29. In: Fonseca, C.R.V.; Magalhães,

C.; Rafael, J.A.; Franklin, E. (Eds.). A

fauna de artrópodos da Reserva

Florestal Adolpho Ducke. Estado Atual

do Conhecimento Taxonômico e

Biológico. Instituto Nacional de

Pesquisas da Amazônia, Manaus,

Amazonas.

Morais, AM, Varella, AMB, Villacorta-Correa,

MA & Malta, JCO. 2010. A fauna de

parasitos em juvenis de tambaqui

Colossoma macropomum (Cuvier,

1818) (Characidae: Serrasalminae)

criados em tanques-rede em lago de

várzea da Amazônia Central. Biologia

Geral e Experimental, vol.9, pp. 14-23.

Morais, AM, Varella, AMB, Fernandes, BMM,

Malta, JCO. 2011. Clinostomum

marginatum (Braun, 1899) and

Austrodiplostomum compactum (Lutz,

1928) metacercariae with zoonotic

potential on Pygocentrus nattereri

( K n e r, 1 8 5 8 ) ( C h a r a c i f o r m e s :

Serrasalmidae) from Central Amazon,

Brazil. Neotropical Helminthology, vol.

5,pp. 08-15.

Morais, AM & Malta JCO. 2014. Chemical

analysis trough “Energy-Dispersive

Spectroscopy (EDS)” of digenea

m e t a c e rca r i a e f o u n d i n f e s t i n g

specimens of Hoplosternum litoralle

(Hancock, 1828) (Siluriformes:

Callichthydae), captured in Manaus

polluted Igarap es. Neotropical

Helminthology, vol.8, pp. 217-225.

Overstreet, RM. 1997. Parasitological data as

monitors of environmental health.

Parassitologia, vol. 39, pp. 169-175.

Poulin, R. 2004. Parasite species richness in

New Zealand fishes: a grossly

u n d e re s t i m a t e d c o m p o n e n t o f

Neotropical Monogenoidea. 28.

Ancyrocephalinae (Dactylogyridae) of

piranha and their relatives (Teleostei,

Serrasalmidae) from Brazil and French

Guiana: species of Notozothecium

Bo e g e r & K ri ts k y, 1 9 8 8 , a n d

Mymarothecium gen. n. Journal of the

H e l m i n t h o l o g i c a l S o c i e t y o f

Washington, vol. 63, pp. 153-175.

Kritsky, DC, Boeger, WA & Jegú, M. 1997a.

Neotropical Monogenoidea. 29.

Ancyrocephalinae (Dactylogyridae) of

piranha and their relatives (Teleostei,

Serrasalmidae) from Brazil: species of

Amphithecium Boeger & Kritsky, 1988,

H e t e r o t h e c i u m g e n . n . a n d

Pithanothecium gen. n. Journal of the

H e l m i n t h o l o g i c a l S o c i e t y o f

Washington, vol. 64,pp. 25-54.

Kritsky, DC, Boeger, WA & Jegú, M. 1997b.

Neotropical Monogenoidea. 30.

Ancyrocephalinae (Dactylogyridae) of

piranha and their relatives (Teleostei,

Serrasalmidae) from Brazil: species of

C a l p i d o t h e c i u m g e n . n . ,

Calpidothecioides gen. n., Odothecium

gen. and Notothecioides gen. n. Journal

of the Helminthological Society of

Washington, vol. 64,pp. 208-218.

Kritsky, DC, Boeger, WA & Jegú, M. 1998.

Neotropical Monogenoidea. 31.

Ancyrocephalinae (Dactylogyridae) of

piranha and their relatives (Teleostei,

Serrasalmidae) from Brazil: species of

Notozothecium Boeger & Kritsky, 1988,

and Enallothecium gen. n. Journal of the

H e l m i n t h o l o g i c a l S o c i e t y o f

Washington, vol. 65, pp. 31-49.

Kritsky, DC & Stockwell, CA. 2005. New

s p e c i e s o f G y r o d a c t y l u s

(Monogenoidea, Gyrodactylidae) from

the white sands pupfish, Cyprinodon

tularosa, in New Mexico. The

Southwestern Naturalist, vol. 50, pp.

312-317.

Luque, JL & Poulin, R. 2007. Metazoan

parasite species richness in Neotropical

275

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Biodiversity of monogenoideans from Pygocentrus nattereri

276

Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015 Morais & Malta

doutorado, Curitiba, Universidade

Federal do Paraná, Paraná, Brasil. pp.

271.

Vital, JF, Varella, AMB, Porto, DB & Malta,

JCO. 2011. Sazonalidade da fauna de

metazoários de Pygocentrus nattereri

(Kner, 1858) no lago Piranha

(Amazonas, Brasil), e a avaliação de seu

potencial como indicadora da saúde do

ambiente. Biota Neotropica, vol.11, pp.

1-6.

Wood, CL, Byers, JE, Cottingham, KL,

Altman, I, Donahue, M & Blakeslee,

AMH. 2007. Parasites alter community

structure. Proceedings of National

Academy of Sciences of the United States

of America, vol. 104, pp. 9335-9339.

b i o d i v e r s i t y . D i v e r s i t y a n d

Distributions, vol. 10, pp. 31-37.

Poulin, R & Morand, S. 2004. Parasite

Biodiversity. Smithsonian Books,

Washington DC. USA. pp. 216.

Silva-Souza, AT, Shibatta, OA, Matsumura-

Tundisi, T, Tundisi, JG & Dupas, FA.

2006. Parasitas de peixes como

indicadores de estresse ambiental e

eutrofização. pp.373-386. In: Tundisi,

J.G.; Matsumura-Tundisi, T.; Galli, C.S.

(Eds.). Eutrofização na América do Sul:

causas, consequências e tecnologias

para gerenciamento e controle.. São

Carlos: Instituto Internacional de

Ecologia.

Thatcher, VE. 2006. a

Amazon fish parasites. 2

ed., Pensoft, Sofia, Bulgaria. pp. 508.

Viana, RT. 2007. Filogenia e biogeografia

h i s t ó r i c a d o s G y ro d a c t y l i d a e

( M o n o g e n o i d e a ) : m o r f o l o g i a ,

moléculas e evidência total. Tese de

Received July 30, 2015.

Accepted September 24, 2015.