Despite the ubiquity of Cucullanus spp. in aquatic ecosystems around the world, their embryonic and

post-embryonic development, as well as transmission patterns, remain little known and in some cases

controversial. In the present study, comparative and embryological data of Cucullanus pinnai pinnai

(Travassos, Artigas & Pereira, 1928) are provided. Adults from Rhamdia quelen (Quoy & Gaimard, 1824)

(Heptapteridae) are described and illustrated by scanning electron microphotography. Eggs were

obtained from gravid females and embryonic and larval development was followed in vitro. The L and L

2 3

stages are described and illustrated for the first time. The embryonic development of C. pinnai pinnai goes

very fast at 20-22ºC. In five days, hatching takes place and the free L remain alive for less than two weeks.

A heteroxenic pattern of transmission is hypothesized involving R. quelen as definitive host and

Bryconamericus iheringii (Boulenger, 1887) (Characidae) as the intermediate host.

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

Neotropical Helminthology, 2020, 14(2), jul-dic:217-225.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

ON THE LIFE CYCLE OF CUCULLANUS PINNAI PINNAI (TRAVASSOS, ARTIGAS &

PEREIRA, 1928) (NEMATODA: CUCULLANIDAE) PARASITE OF RHAMDIA QUELEN (QUOY

& GAIMARD, 1824) (SILURIFORMES) FROM ITS SOUTHERN LOCALITIES

ACERCA DEL CICLO DE VIDA DE CUCULLANUS PINNAI PINNAI (TRAVASSOS, ARTIGAS &

PEREIRA, 1928) (NEMATODA: CUCULLANIDAE) PARÁSITO DE RHAMDIA QUELEN (QUOY

& GAIMARD, 1824) (SILURIFORMES) EN SU DISTRIBUCIÓN MÁS MERIDIONAL

1Universidad Nacional del Sur, Departamento de Biología, Bioquímica y Farmacia, calle San Juan nº 670 (8000) Bahía

Blanca, Buenos Aires, Argentina.

2Instituto de Ciencias Biológicas y Biomédicas del Sur (INBIOSUR/CONICET) calle San Juan n°671 (8000) Bahía Blanca,

Buenos Aires, Argentina

*Corresponding author: rtanzola@uns.edu.ar

1,2,* 1,2 1 1

Ruben Daniel Tanzola ; Silvia Elizabeth Guagliardo ; Cintia Poggi ; Bárbara Angeletti & Carla Belén

1,2

Schwerdt

Neotropical Helminthology

217

doi:10.24039/rnh2020142808

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

Lima-Perú

VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

Volume14,Number2(jul-dec)2020

ABSTRACT

Keywords: Cucullanus pinnai – freshwater ﬁshes – life cycle – Nematoda – Rhamdia quelen

INTRODUCTION

218

RESUMEN

Palabras clave: Cucullanus pinnai – peces de agua dulce – ciclo de vida – Nematoda – Rhamdia quelen

A pesar de la ubicuidad de Cucullanus spp. en los ecosistemas acuáticos de todo el mundo, su desarrollo

embionario y post-embrionario, así como los patrones de transmisión, siguen siendo poco conocidos y, en

algunos casos, controvertidos. En el presente estudio se proporcionan datos comparativos y

embriológicos de Cucullanus pinnai pinnai (Travassos, Artigas & Pereira, 1928). Los nematodes adultos

provenientes de Rhamdia quelen (Quoy & Gaimard, 1824) (Heptapteridae) se describen e ilustran

mediante microfotografía electrónica de barrido. Se obtuvieron huevos de hembras grávidas y se siguió el

desarrollo embrionario y larvario in vitro. Las etapas L y L se describen e ilustran por primera vez. El

2 3

desarrollo embrionario de C. pinnai pinnai es muy rápido a 20-22°C. En cinco días tiene lugar la eclosión

y las L libres permanecen vivas menos de dos semanas. Se plantea la hipótesis de un patrón de transmisión

heteroxeno que involucra a R. quelen como hospedador definitivo y Bryconamericus iheringii

(Boulenger, 1887) (Characidae) como hospedador intermediario.

Neotropical Helminthology, 2020, 14(2), jul-dic

s u r i n a m e n s i s Géry, 1 9 6 2 ( Teleostei:

Characidae)(Hoshino et al., 2014) and the body

cavity of Bryconamericus iheringii (Boulenger,

1887) (Teleostei: Characidae)(Tanzola et al.,

2019).

Cucullanus pinnai pinnai (Travassos, Artigas &

Pereira, 1928) was described by Travassos et al.

(1928) from Synodontis clarias (Linnaeus,

1758)(= Pimelodus clarias) on the Mogi-Guazú

river, Sao Paulo state, Brazil. To date it is the taxon

with the highest number of records in neotropical

freshwater fishes, having been cited in 20 host

species, mostly siluriforms of the family

Pimelodidae (Moravec, 1998; Soares de Oliveira et

al., 2015, Vieira et al., 2015, Chemes & Takemoto,

2020). The southernmost record of this cucullanid

is the Napostá Grande stream, southwest of Buenos

Aires province, parasitizing Rhamdia quelen

(Quoy & Gaimard, 1824) (Heptapteridae) (Tanzola

et al., 2009). Given the lack of morphological

information of the adults from R. quelen as well as

details of their embryonic development and

possible patterns of transmission, the aim of this

study was to provide comparative and

development data of C. pinnai pinnai in the

southernmost dispersion area. Also a description of

a third stage larvae of Cucullanus sp. in the body

cavity of B. iheringii (Characidae), a fish prey of R.

quelen from the same habitat, is given and

compared to the L experimentally obtained.

The family Cucullanidae Cobbold, 1864

(Ascaridida: Seuratoidea) includes parasitic

nematodes from the digestive tract of marine,

estuarine and freshwater teleosts, with some

representatives in cyclostomes, elasmobranchs and

occasionally in aquatic turtles (Anderson et al.,

2009; Moravec & Justine, 2011). Cucullanus

Müller, 1777, the type-genus, is the richest and

most diverse in the family, with more than 100

species described worldwide, of which at least 32

parasitize marine and freshwater fish in the

Neotropical region (Luque et al., 2011; Vieira et

al., 2015). Despite their ubiquity in aquatic

ecosystems around the world, their embryonic and

post-embryonic development, as well as

transmission patterns, remain little known and in

some cases controversial (Moravec, 1979;

Anderson, 2000). Valovaya (1978) conducted a

detailed study of the embryonic development of

Cucullanus cirratus Müller, 1777. Since then

heteroxenous patterns have been experimentally

demonstrated, involving an intermediate or

paratenic host, or monoxenic mechanisms, in

which the larvae undergo histotropic phase, in a

single host (Moravec, 1979; Baker, 1984;

Anderson, 2000; Choudhury & Cole, 2019). To

date two records of Cucullanus sp. larvae, without

descriptions, were recorded from the Neotropical

region, parasitizing the gut of Hemibrycon

Tanzola et al.

molecular studies.

Collection of L from Bryconamericus iheringii

Third stage larvae of a Cucullanus sp. were

collected alive in the body cavity of “tetras” B.

iheringii. They were extracted from the peritoneal

tissue by mean of dissection needles, washed in

saline solution and fixed in 70% ethanol. L were

measured and photographied using a Motic BA

microscope.

Quantitative data

Parasitic indicators (prevalence, intensity and

abundance) were calculated following Bush et al.

(1997). Parasitic prevalences between sites were

compared using the Z statistic for samples ≤ 100

hosts (Morales & Pino, 1987). Parasitic

abundances between sites were tested using the U-

Mann Whitney test (IBM SPSS Statistic 23).

Ethic aspects: The authors declare that they have no

conflict of interest, that no experimental animals

have been used and that the research did not

produce negative impacts on people or the

environment.

Description of adults Cucullanus pinnai pinnai

Travassos, Artigas & Pereira, 1928

Male (n=5): Total length 7,254 (6,650-7,750) mm.

Maximum width 240 (200-270). Oral opening

dorso-ventral elongated with a cuticular collarete

surrounding a border of about 80 denticules (Fig.

1a). Two submedian pairs of cephalic papillae.

Small pair of lateral amphids between them.

Oesophagus length 774 (730-850). Distance of the

nervous ring to cephalic end 300 (300-300).

Distance of deirids to the cephalic end 442 (390-

510). Excretory pore was not observed. Tail 170

(150-190), curved ventrally. Precloacal sucker well

developed, notorious in translucent specimens but

inapparent under SEM images. Spicules equal

687,5 (570-800) semicircular in cross section, with

distal end pointed and bent (Fig. 1b).

Gubernaculum present, about 60 in length. Ten pair

of caudal papillae arranged as follows: Precloacal

five pairs, first one (sv1) in the frontal border of

precloacal sucker (Su), second (sv2) in the

Study area, hosts sampling and dates

Three adults R . qu ele n (Siluriformes:

Heptapteridae), 45 B. iheringii (Characiformes:

Characidae) from Napostá Grande stream

(38°42'39.37”S 62°15'16.80” W) and 45 B.

iheringii from Sauce Chico river (38°42'06.06”S

62°27'28.11 W), were caught with line and hook

(R. quelen) and trawl net (B. iheringii). They were

caught during late summer 2018 and late spring

2019. The hosts were transported alive to the

laboratory and euthanized by overdose of an

-1

ethanolic benzocaine solution (1g·30mL )

(Gilderhus, 1990). The taxonomic status of the

fishes follows Froese & Pauly (2019).

Collection of adult nematodes

The fish were dissected and the visceral mass

extracted in NaCl saline solution. The intestine

were dissected and the worms collected alive under

stereoscopic microscope. They were washed in

distilled water and fixed in 10% formaldehyde (at

room temperature 20°C) or in hot 70% ethanol.

Two males and two females were examined

ultrastructurally by scanning electron microscopy

(SEM). They were dehydrated in acetone, dried in a

CO critical point, metallized in gold, observed and

photographied in a JEOL JSM T-100 scanning

microscope at 15kv, at Museo de La Plata

(Argentina). The measurements are given in µm,

unless otherwise is stated, as a mean and range

between parentheses. The nomenclature for the

male caudal papillae follows Vieira et al. (2015).

Voucher specimens (3 males, 3 females) of C.

p i n n a i p i n n a i w e r e d e p o s i t e d a t t h e

Helminthological Collection of the División

Zoología Invertebrados del Museo de La Plata,

accesion number MLP-He 7691.

Collection of eggs and monitoring of embryonic

devolpment

Two gravid females were maintained at room

temperature (20ºC) in a Petri dish containing

distilled water to allow their spontaneous

oviposition (Moravec, 1979). Once the eggs were

laid, they were monitored every 8-10 h under light

microscope and photographied during the process,

until the hatching of larvae. Larvae were fixed in

70% ethanol, measured and photographied. Ten

larvae were collected in 96% ethanol to future

MATERIALS AND METHODS

219

RESULTS

Neotropical Helminthology, 2020, 14(2), jul-dic Life cycle of Cucullanus pinnai pinnai

Female (n=4): Total length 7,53 (6,35-8,82) mm.

Maximum width 257,5 (220-280). Oesophagus

length 827,5 (810-870). Distance of the nervous

ring to cephalic end 302,5 (280-320). Distance of

deirids to the cephalic end 550-550. Excretory pore

not observed. Vulva postequatorial, distance to the

anterior end 4,522 (3,400-5,770) mm, in the mid-

ventral line, slightly elevated (Fig. 1c). Tail 225,6

(212-230). Eggs in uterus 30 x 37,5-45, eggs, 32 x

55 once laid.

posterior limit of the sucker, third (sv3) in mid-

point between sv2 and cloacal opening, fourth

(sv4) and fifth (sv5) close to cloaca. A little

adcloacal subventral pair (ad). Four postcloacal

pairs, two subventral (sv6, sv7) and two lateral (l1,

l2). A little pair of phasmids (f) between to the last

postcloacal papillae (l2 and sv7) slightly behind

them.

220

Figure 1. Cucullanus pinnai pinnai Travassos, Artigas & Pereira, 1928 adults from Rhamdia quelen (SEM). a- Oral end in frontal

view (female), a= amphids, p= cephalic papillae; b= caudal end (male), f= phasmid, Su= precloacal sucker, svd= subventral right

papillae, svi= subventral left papillae, ld= lateral right papillae, li= lateral left papillae; c= posterior region (female), vulva (white

arrow), anus (black arrow), inbox: detail of vulva. Scale bars: 1a= 0,05mm, 1b= 0,10mm, 1c= 0,20mm.

Neotropical Helminthology, 2020, 14(2), jul-dic Tanzola et al.

Figure 2. Cucullanus pinnai pinnai, embryonic and postembryonic development. a- unsegmented egg at oviposition; b= two-

cells embryo (Day 1); c= 16-cells morula (Day 2); d= L1 in egg (*: micropyle)(Day 4); e= newly hatched L (inbox: detail of M1

(arrow))(Day 5); f: Cucullanus sp. L from the body cavity of Bryconamericus iheringii (inbox: detail of the caudal end). Scale-

bars: Figs. 2a-e= 0,05mm; 2f=0,10mm (inbox= 0,05).

221

Neotropical Helminthology, 2020, 14(2), jul-dic Life cycle of Cucullanus pinnai pinnai

1,100-1,259 mm and 40-45 in maximum width. At

the cephalic end they showed a mouth opening as a

dorso-ventral groove surrounded by a cuticular

collarete in formation. Oesophagus about 330 in

length, sligthly club-shaped, with a dense

esophageal gland near the oral opening. Nervous

ring approximately 130 to the anterior end.

Excretory pore immediately behind the nervous

ring level. Tail conical elongated, 130-140 in

length. They were found moving freely between

the perivisceral peritoneum with no reactive

capsule from the host.

Quantitative data of Cucullanus sp. L from

Bryconamericus iheringii

Prevalence 48,7% (Naposta Grande stream, n=45)

and 35,5% (Sauce Chico river, n=45)(Z= 1,023

p>0,05). Mean abundance 2,24 (Naposta Grande

stream, n=45) and 1,40 (Sauce Chico river,

n=45)(U Mann Whitney= 7,00 p>0,05). This L

was a component species of the helminth

assemblages of B . ih er i ng ii from both

environments.

Moreira et al. (2014) highlighted the low host

specificity of C. pinnai pinnai having been

recorded from 20 host species. Previous findings in

R. quelen, without descriptions, are those of

Tanzola et al. (2009), Venancio et al. (2010) and

Moreira et al. (2014). Values of prevalence and

abundance were similar in the first two references

and higher in Moreira et al. (op.cit.). Albuquerque

et al. (2008) collected C. pinnai as adults in the

stomach, intestine and larvae in the body cavity of

P i m e l o d u s m a c u l a t u s Lacépè d e , 1803

(Pimelodidae) from Rio Guandu basin, Rio de

Janeiro, Brazil, suggesting that under certain

environmental conditions, it could experiment a

histotropic phase as observed in other Cucullanus

spp. (Anderson, 2000). No descriptions of C.pinnai

larvae are available to date.

The final host, R. quelen was considered as an

omnivorous fish with tendency to carnivorism

(Ringuelet, 1975; Brazil-Souza et al., 2009).

López-Cazorla et al. (2003) categorized this catfish

as euriphagous because 24 food items were

Remarks: The three hosts were parasitized by C.

pinnai pinnai (with 20, 37 and 131 worms,

respectively). This fact allowed us to hypothesize

that it is a common parasite of R. quelen in the area.

Observations on the embryonic development

and free larvae

Gravid females spontaneously began to lay eggs

immediately placed in distilled water. The eggs

were laid in the one- or two-cell stage, mostly in

small groups of 4-6 or individually (Figs. 2a, 2b).

They were oval, 45-55 x 30-32,5, thin shelled with

a visible mycropile at one of the poles. Apparently,

a thin vitelline cover is present and holds the eggs

together or allows them to adhere to solid

substrates (i.e. the glass of a Petri dish or perhaps

the leaves of submerged vegetation in the natural

environment). The observation of two cellular size

in the 2-cell stage (S1 and P1) leads us to think that

the cleavage model responds to that typical of

Secernentea, that is, of the determinated type.

Cleavage splits happen quickly and about 24 h a

16-blastomers morula is formed (Fig. 2c). The

gastrula was not observed but in 72-96 h the L

stage is visible inside the egg and showed slow

movements (Fig. 2d). A molt could not be observed

in this stage but at day 5 the larvae began to hatch

and move actively and twisted. These larvae are

covered by a thin envelope considered as a moult

M1 (Fig. 2e). So, the larvae are in the L2 stage

when hatch. They measured 211-275 in total length

and 10-12,5 in maximum width. The oesophagus

occupies about 40% of the total length and the

intestinal joining is visible. They could not be

observed neither the nervous ring nor the excretory

pore. The intestine is loaded with a granular content

and the anus is a conspicuous knob that marks the

origin of the pointed tail, about 26-33 in length.

Second stage larvae remained active till day 12-14

and then all died. No growth in body mass was

detected during the free stage. It seems that L

doesn't feed in free stage and depends on the

embryonic nutritional reserves.

Description of Cucullanus sp. L from

Bryconamericus iheringii

A sample of B. iheringii from Napostá Grande

stream and Sauce Chico river presented in the body

cavity early third-stage larvae completely enclosed

in a sheat, the moult of the L (Fig. 2f). From the

following combination of characters, they were

considered to belong to Cucullanus sp. Total length

222

DISCUSSION

Neotropical Helminthology, 2020, 14(2), jul-dic Tanzola et al.

Albuquerque, MC, Santos, MD, Monteiro, CM,

Martins, AN, Ederli, NB & Brasil-Sato,

MB. 2008. Helmintos endoparasitos de

Pimelodus maculatus Lacépède, 1803

(Actinopterygii, Pimelodidae) de duas

localidades (Lagoa e Calha do Rio) do Rio

Guandu, Estado do Rio de Janeiro, Brasil.

Revista Brasileira de Parasitologia

Veterinária, vol. 17, Supl. 1, pp. 113-119.

Anderson, RC. 2000. Nematode parasites of

vertebrates: their development and

transmission. 2 ed. Wallingford (UK):

CAB International.

Anderson, RC, Chabaud, AG & Willmott, S (Eds.).

2009. Keys to the nematode parasites of

vertebrates. [Archival volume] Wallingford

(UK): CAB International.

Baker, MR, 1984. On the biology of Dichelyne

(Cucullanellus) cotylophora (Ward and

Magath, 1917) (Nematoda, Cucullanidae)

in perch (Perca flavescens) from Lake Erie,

Ontario. Canadian Journal of Zoology, vol.

62, pp. 2062–2073.

Brazil-Sousa, C, Marques, RM & Albrecht, MP.

2009. Food partitioning between two

heptapterid fish species in Macaé River, RJ

(Southeastern Brazil). Biota Neotropica,

v o l . 9 ,

http://www.biotaneotropica.org.br/v9n3/en

/abstract?article+bn00309032009.

Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW.

1997. Parasitology meets ecology on its

own terms: Margolis et al. revisited. Journal

of Parasitology, vol. 83, pp. 575-583.

Chemes, SB & Takemoto, RM. 2020. New records

of parasitic helminths of Pimelodidae fishes

in the Middle Paraná system (Argentina).

Neotropical Helminthology, vol. 14, pp. 19-

34.

Choudhury, A & Cole, RA. 2019. Life Cycle of the

Trout Cecal Nematode, Truttaedacnitis

truttae (Nematoda: Cucullanidae):

Museo de La Plata. This study was carried out with

the aid of grants UNS-PGI 24/B293 and PIO-

UNS/CONICET (2016-2017) “Evaluación de la

calidad del agua para consumo rural y otras fuentes

alternativas de abastecimiento urbano”.

registered in Sauce Grande river, from that basin of

Napostá Grande and Sauce Chico river belong. A

gastropod was the dominat food item in that study

and may be due to the abundance of this mollusk in

the Sauce Grande river. There R. quelen actually

behaves like an opportunistic predator. On the

other hand, B. iheringii inhabits calm and

vegetated waters as the streams of Southwest

Buenos Aires province. It is considered as

omnivorous or invertebrate-predator which feeds

mostly on aquatic insects (Escalante, 1987; López-

Cazorla et al., 2003). Grossman et al. (1996)

concluded that B. iheringii is a species related to the

phytoplancton-periphyton in a pond from centre of

Buenos Aires province. The possibility that R.

quelen predates on B. iheringii is not ruled out, and

more data are needed to confirm this hypothesis.

The L experimentally obtained from gravid

females of C. pinnai pinnai have a significant

similarity with L collected in B. iheringii. Future

molecular approaches will demonstrate their

taxonomic correspondence and the consequent

heteroxenous pattern of transmission.

The embryonic development of C. pinnai pinnai

goes very fast. In less than five days from laid, the

L hatches and must find the right host in less than

two weeks or die. This shortened transmission

model matches that of C. chabaudi which hatches

in 5-6 days post-oviposition, but follows a

histotropic phase of development in the liver of

Pangasius pangasius (Hamilton, 1822), a

freshwater fish from Southeastern Asia (Anderson,

2000). Janiszewska (1938) failed to try to infect

several crustacean with eggs and larvae of C.

minutus. Most attempts to infect invertebrates with

eggs or larvae of another cucullanid genera

(Truttaedacnitis Petter, 1974, Dichelyne

Jägerskiöld, 1902) gave negative results (Gibson,

1972, Kuzia, 1978- in Anderson, 2000). It seems to

be that life cycle of C. pinnai pinnai requires at

least the presence of a fish as intermediate or

paratenic host.This constitutes the first description

of the embryonic and post-embryonic development

of C. pinnai pinnai.

The authors are grateful to Prof. Patricia Sarmiento

for her assistance with the SEM studies at the

223

ACKNOWLEDGMENTS

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