ORIGINAL ARTICLE /ARTÍCULO ORIGINAL

HELMINTH PARASITES OF THE WHITE-RUMPED SANDPIPER, CALIDRIS

FUSCICOLLIS (AVES: SCOLOPACIDAE), FROM BRAZIL

HELMINTOS PARÁSITOS DEL PILRITO-DE-UROPÍGIO-BRANCO, CALIDRIS

FUSCICOLLIS (AVES: SCOLOPACIDAE), DE BRASIL

1* 1 1

Sâmara Nunes Gomes , Tatiana Cheuiche Pesenti & Gertrud Müller

1Universidade Federal de Pelotas, Departamento de Microbiologia e Parasitologia, Laboratório de Parasitologia de Animais

Silvestres, Pelotas, Rio Grande do Sul, Brasil, *sng.bio@hotmail.com, (55-51-91350993)

Neotropical Helminthology, 2016, 10(2), jul-dic: 163-168.

ABSTRACT

Keywords: Acanthocephala – Brazil – Calidris fuscicollis – Cestoda – Trematoda

Eighty white-rumped sandpipers (Calidris fuscicollis) from the State of Rio Grande do Sul,

Brazil, were collected and examined for helminth parasites during the period 2010-2012.

Helminthes consisting of two trematodes (Selfcoelum brasilianum, Maritrema sp.), two cestodes

(Nadejdolepis smithi, Nadejdolepis sp.) and one acanthocephalan species (Polymorphus

cucullatus) were identified. Selfcoelum brasilianum, Maritrema sp., N. smithi, Nadejdolepis sp.

and P. cucullatus were reported, for the first time, in C. fuscicollis.

163

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

RESUMO

Palavras chave: Acanthocephala – Brasil – Calidris fuscicollis – Cestoda – Trematoda

Oitenta maçariços da espécie Calidris fuscicollis foram coletados no Estado do Rio Grande do

Sul, para análise de helmintos, no período de 2010-2012. Foram identificadas dois trematódeos

(Selfcoelum brasilianum, Maritrema sp.), dois cestoides (Nadejdolepis smithi, Nadejdolepis sp.)

e um acantocéfalo (Polymorphus cucullatus). Selfcoelum brasilianum, Maritrema sp., N. smithi,

Nadejdolepis sp. e P. cucullatus são reportados, pela primeira vez, em C. fuscicollis.

INTRODUCTION

The coastal region of Rio Grande do Sul,

where birds find an extensive coastal area for

feeding and resting, is of utmost importance

for bird species that migrate annually and use

different food resources (Belton, 1994).

Calidris fuscicollis (Vieillot, 1819), a nearctic

migrant, nests in the arctic tundra of Alaska

and northern Canada and migrates to the

southern hemisphere during the non-breeding

season, when it can be found in lagoons and

other coastal regions of South America

(Piersma et al., 1996). According to Antas

(1989), the spring migration of the white-

rumped sandpiper follows the Amazon and

Central Brazil route, where these birds

frequently stop on sandbars and riverbanks.

They feed on small crustaceans, molluscs and

marine worms, and also eat insects and plants

on lagoon shores (Novelli, 1997).

CHLAPASIL 641; N a d e j d o l e p i s sp.

CHLAPASIL 642; Polymorphus cucullatus

CHLAPASIL 643. Prevalence, mean

abundance and mean intensity of parasitism

parameters were calculated according to Bush

et al. (1997), and statistical analyzes were

performed by means of the Chi-square test

using the Statistix 9.0 software.

Of the 80 birds collected, 29 were males and 51

females; 98% of the birds were parasitized by

at least one species of helminth belonging to

the Phylum Acanthocephala and Classes

Cestoda and Trematoda. The highest

prevalence was found in the small intestine.

The following parasites were identified:

Selfcoelum brasilianum (Stossich, 1902) and

Maritrema sp. of the Class Trematoda;

Polymorphus cucullatus (Van Cleave &

Starrett, 1940) of Phylum Acanthocephala;

Nadejdolepis smithi (Deblock & Canaris,

2001) and Nadejdolepis sp. of Class Cestoda.

Table 1 shows the list of helminths, infection

site and their respective parameters

(prevalence, mean abundance and mean

intensity).

Maritrema sp. showed the highest prevalence

(57.5%), followed by the acanthocephalan

Polymorphus cucullatus (33.75%). The

trematode Selfcoelum brasilianum showed

low prevalence, as only two hosts were

parasitized by one specimen each. It was not

possible to calculate cestode parameters

because only a few specimens were

sufficiently stained for correct identification.

According to Gibson et al., (2002), the

Cyclocoelidae family (Stossich, 1902) is

divided into three subfamilies, which are

classified according to the position of the

ovary: Cyclocoelinae (Stossich, 1902) is

l o c a t e d b e t w e e n t h e t e s t i c l e s ;

There are few publications on Calidris

fuscicollis helminths. Deblock & Canaris

(2000) made some taxonomic considerations

upon describing the cestode Nadejdolepis

litoralis (Webster, 1947) in Belize; Canaris &

Kinsella (2001) identified the cestodes N.

litoralis and N. paranitidulans (Golikova,

1959), as well as the acantocephalan

Arhythmorhynchus longicolle (Villot, 1875) in

only one specimen, also from the Belizean

coast. The aim of this study was to report

Calidris fuscicollis helminth parasites in

Brazil.

Between April 2010 and September 2012, 80

specimens of Calidris fuscicollis (ICMBIO

License N. 26234-1) were collected on the

southern coast of Rio Grande do Sul State,

Brazil (-32º15'32.57"S; -52º14'00.04" W) by

means of a mist net (Mistnets). The birds were

sedated and euthanized following Federal

Council of Veterinary Medicine procedures

(2012), placed in individual plastic bags and

referred to the Wildlife Parasitology

Laboratory of the Federal University of

Pelotas, where they were necropsied and had

their organs analyzed individually on a

stereomicroscope. Females were identified

during necropsy by the presence of the ovaries.

The parasites found were preserved in 70° GL

alcohol for further processing. The trematodes,

cestodes and acanthocephalans were

compressed, fixed in AFA, stained with

Langeron's carmine and mounted in Canada

balsam.

Helminths were identified by specialized

bibliography references for each group, and

representative specimens were deposited in the

collection of the Laboratory of Wild Animals

Parasites of the University: Selfcoelum

brasilianum CHLAPASIL 639; Maritrema sp.

CHLAPASIL 640; Nadejdolepis smithi

MATERIAL AND METHODS

RESULTS AND DISCUSSION

Neotropical Helminthology. Vol. 10, Nº2, jul-dic 2016 Nunes Gomes et al.

164

(Luhe, 1911): According to Amin (1992), a

number of species had been formerly

attributed to the genera Profilicollis (Meyer,

1931), Falsifilicollis (Webster, 1948),

P a r a f i l i c o l l i s (Pe trochenko, 1956),

S u b f i l i c o l l i s ( H o k l o v a , 1 9 6 7 ) ,

Arhythmorhynchus (Luhe, 1911), Filicollis

(Luhe, 1911) and Plagiorhynchus (Luhe,

1911) (= Prosthorhynchus Kostylev, 1915);

according to Petrochenko (1971), the genus

Polymorphus (Lühe, 1911) has a fusiform

body, its anterior section is separated from the

rest by a constriction, and it has a cylindrical or

oval proboscis, four tubular cement glands,

fusiform eggs and wavy protrusions at the

ends; according to Hoklova (1971) and Amin

(1992), the differentiation between genera of

the family Polymorphidae is given the number

and shape of cement glands, which are tubular

and four in number in Polymorphus; to Amin

(1992), the genus includes 36 species, all

parasites of waterfowl P. cucullatus (Van

Cleave et Starrett, 1940) and has a slightly

larger body in the proboscis section, which is

divided by a constriction, proboscis hooks in

22 longitudinal rows ordered with 12 hooks

each, lemnisci about twice as long as the sheath

and four long, tubular cement glands

(Petrochenko, 1971).

Nadejdolepis, a cestode of the family

Hymenolepididae (Spasskii & Spaskaya,

1954), is common in wader birds. However,

little is known about cestodes of the genus

Nadejdolepis - the few studies on these

helminths were performed by Deblock &

Ca n a r is (2 0 0 0 ), wh o i d en ti f i e d N .

p a r a n i t i d u l a n s (Golikova, 1959) in

Charadrius alexandrinus (Linnaeus, 1758), N.

arenarie (Cabot, 1969) in Arenaria interpres

(Linnaeus, 1758), and N. litoralis (Webster,

1947) in Calidris fuscicollis on the coast of

Belize; Canaris & Kinsella (1998) found N.

paranitidulans in Calidris ferruginea in King

Island, Tasmania; Deblock & Canaris (2001b),

who identified N. bealli and Nadejdolepis sp.

in Arenaria interpres and Calidris alpina

Ophthalmophaginae (Harrah, 1922) is post-

testicular, and Haematotrephinae (Dollfus,

1948) is pre-testicular. The genus Selfcoelum

(Stossich, 1902) (Sin. Corpopyrum Witenberg,

1923; Haematoprimum Witenberg, 1923;

Harrahium Witenberg, 1923; Haematotrephus

Stossich, 1902) belongs to the subfamily

Cyclocoelinae (Dollfus, 1948) (Blend &

Dronen, 2008) for having a genital pore

posterior to the pharynx, with no vitelline

glands in the posterior end, and diagonal testis

forming a triangle with the ovary, which is pre-

testicular and opposite to the anterior testis

(Blend & Dronen, 2008). Parasites of this

genus are commonly found parasitizing the

abdominal cavity and air sacs of birds (Gibson

et al., 2002). According to Skrjabin et al.,

(1964), species are differentiated by the

disposition of the vitelline glands, which in S.

brasilianum reach the pharynx level.

The Family Microphallidae (Ward, 1901) is

made up of very small trematodes (500±

300μm). They have a ventrally flattened back

and are thin, generally linguiform, piriform or

fusiform in shape and adults are mostly found

in the intestine of vertebrates (Bray et al.,

2008). The genus Maritrema (Nicoll, 1907)

includes a series of small distomata that occur

in different parts of the world, most of which

are parasites of shorebirds (Hadley & Castle,

1940). Adult forms are found parasitizing the

intestine of birds, causing enteritis and

ulceration (Swales, 1933). Their life cycle

involves gastropods as intermediate hosts and

crustaceans as second intermediate hosts

(DeBlock, 1971). The arrangement of the

vitelline glands, which are almost at the rear

end and the similar size of suckers, are marked

morphological features of this group (Hadley

& Castle, 1940).

The family Polymorphidae (Meyer, 1931)

includes three subfamilies, 10 genera, 88

species and two ambiguous species. There is

t a x o n o m i c c o n f u s i o n i n v o l v i n g

acanthocephala of the genus Polymorphus

Neotropical Helminthology. Vol. 10, Nº2, jul-dic 2016 Helminth parasites of Calidris

165

gastropods, intermediate hosts of trematodes,

thus justifying their higher prevalence in the

host bird. The same role may be attributed to

acanthocephalans and cestodes found in C.

f u s c i c o l l i s , w h i c h h a v e w a t e r

microcrustaceans as intermediary hosts.

The number of species found in this study was

higher than that found by Canaris & Kinsella

(2001); these authors reported two cestode and

one acanthocephalan species in only one

specimen captured in Belize, contrasting with

the 80 specimens analyzed in this work.

By feeding in aquatic environments that allow

the presence of intermediate hosts of

helmin t h s , such a s g a stropo d s a nd

microcrustaceans, Calidris fuscicollis showed

a greater number of trematode and cestode

species.

The trematodes Selfcoelum brasilianum and

Maritrema sp., the cestodes Nadejdolepis

smithi and Nadejdolepis sp., and the

acanthocephalan Polymorphus cucullatus

have been first reported in Calidris fuscicollis.

We thank to Coordenação de Aperfeiçoamento

de Pessoal de Nível Superior (CAPES), a

(Linnaeus, 1758) in Alaska, N. smithi (Deblock

& Canaris, 2001a) in Charadrius ruficapillus

(Temminck, 1822), and Arenaria interpres and

N. kinsellai in C. ruficapillus in Australia.

Nadejdolepis smithi was found to parasitize

the large intestine of C. ruficapillus in

Australia, and was described by Canaris and

Kinsella in 1998 as N. lauriei (Davies, 1939).

There were no significant differences between

infected and uninfected birds as to different

helminth species and as to male and female

bird infection were found by data analysis and

the chi-square test (P> 0 05).

Many seabirds feed on invertebrates, such as

arthropods and aquatic mollusks, which are

infected with helminth eggs (Mouritsen et al.,

1997). According to Bush et al. (1990), the

variety of helminth species is on average lower

in terrestrial hosts than that in water and

migratory birds which, as opposed to resident

birds, are exposed to more than a single

environment and, consequently, their parasites

(Moller & Erritzøe, 1999).

By feeding in aquatic environments, C.

fuscicollis is subject to helminth infections,

inasmuch as the habitat plays an important role

in the host-parasite relationship. The migratory

habits and varied diet of this host facilitate its

infection by various helminth genera, once

these birds have greater exposure to

Table 1. Helminths in Calidris fuscicollis (Aves: Scolopacidae) in southern Brazil, (2010-2012).

Helminths Habitat P% MI MA

Acanthocephala

Polymorphus cucullatus

33,75 3,74 1,26

Cestoda

Nadejdelipis burgessi

- -

Nadejdolepis sp. SI - - -

Trematoda

Maritrema sp.

57,5

13,32 7,66

Haematotrephus brasilianum AC 1,25 2 0,025

P = Prevalence; MI = Mean Intensity; MA = Mean Abundance; SI = Small Intestine; AC = Abdominal Cavity.

ACKNOWLEDGEMENTS

Neotropical Helminthology. Vol. 10, Nº2, jul-dic 2016 Nunes Gomes et al.

166

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

583.

Canaris, AG & Kinsella, JM. 1998. Helminth

parasite communities in four species of

shorebirds (Charadriidae) on King

I s l a n d , Ta s m a n i a . P a p e r s a n d

Procedings of the Royal Society of

Tasmania, vol. 132, pp. 49-52.

Canaris, AG & Kinsella, JM. 2001. Helminth

Parasites in Six Species of Shorebirds

(Charadrii) from the Coast of Belize.

Memórias do Instituto Oswaldo Cruz,

vol. 96, pp. 01-04.

Conselho Federal de Medicina Veterinária.

2012. Resolução nº 714 de 20 de junho

d e 2 0 1 2 . D i s p o n í v e l e m :

www.cfmb.org.br/portallegislacao/resol

ucoes/resulocao_714.pdf. Accessed on

19 January 2013.

Deblock, S. 1971. Contribution a étude des

Microphallidae Travassos,1920 XXIV.

Tentative de phylogénie et de taxonomie

Bulletin of the Natural History Museum,

vol. 7, pp. 359-468.

Deblock, S & Canaris, A. 2000. Trois

nouveaux Nadejdolepis Spasskii &

S a s s k a y a , 1 9 5 4 ( C e s t o d a :

Hy m e n ol e p i di d a e ) p a r a s i te s d e

Charadrii (Aves) du Bélize. Systematic

Parasitology, vol. 47, pp.193-201.

Deblock, S & Canaris, A. 2001a. Trois

nouveaux Nadejdolepis Spasskii &

S a s s k a y a , 1 9 5 4 ( C e s t o d a :

Hy m e n ol e p i di d a e ) p a r a s i te s d e

C h a r a d r i i ( Av e s ) d e Ta s m a n i e .

Systematic Parasitology, vol. 48, pp.

185-202.

Deblock, S & Canaris, A. 2001b. De quelques

Hymenolepididae (Cestode) d'oiseaux

Charadrii d'Alaska dont Nadejdolepis

bealli n. sp., parasite de Calidris alpina.

Systematic Parasitology, vol. 48, pp.

151-157.

Gibson, DI, Jones, A & Bray, RA. 2002. Keys

to the Trematoda, Vol. 1. CABI

Publishing, Wallingford, UK.

Hadley, CE & Castle, RM. 1940. Description

Amin, OM. 1992. Review of the genus

P o l y m o r p h u s L ü h e , 1 9 1 1

(Acanthocephala: Polymorphidae), with

the synonymization of Hexaglandula

Petrochenko, 1950, and Subcorynosoma

Hoklova, 1967, and a key to the species.

Qatar University Science Journal, vol.

12, pp. 115-123.

Antas, PTZ. 1989. Aves limícolas do Brasil. In:

Seminário Internacional sobre manejo e

conservação de maçaricos e ambientes

aquáticos nas Américas. Recife,

IBAMA, pp. 181-187.

Belton, W. 1994. Aves do Rio grande do Sul:

Distribuição e Biologia. Unisinos, São

Leopoldo, RS.

Blend, CK & Dronen, NO. 2008. Selfcoelum

lamothei n. sp. (Digenea: Cyclocoelidae:

Cyclocoelinae) from the air sacs of the

l o n g – b i l l e d c u r l e w, Nu me n iu s

americanus (Scolopacidae), from the

Galveston, Texas area, USA. Revista

Mexicana de Biodiversidad, vol. 79, pp.

41-48.

Bray, R, Gibson, D & Jones, A. 2008. Keys to

the Trematoda. Vol. 3. London: CAB

International. 824p.

Bush, AO, Aho, JM & Kennedy, CR. 1990.

Eco l ogi c a l v e r su s p hyl o gen e t ic

determinants of helminth parasite

community richness. Evolutionary

Ecology, vol. 4, pp. 1-20.

Bush, AO, Lafferty, KD, Lotz, LL & Shostak,

AW. 1997. Parasitology meets ecology

on terms: Margolis et al. Revisited.

BIBLIOGRAPHIC REFERENCES

Brazilian Federal Agency for Support and

Evaluation of Graduate Education, for the

Doctoral and to Conselho Nacional de

Desenvolvimento Científico e Tecnológico

(CNPq/Brasil), The National Council for

Scientific and Technological Development for

having supported this study in part.

Neotropical Helminthology. Vol. 10, Nº2, jul-dic 2016 Helminth parasites of Calidris

167

Novelli, R. 1997. Aves marinhas costeiras do

Brasil: identificação e biologia. Porto

Alegre. Cinco Continentes, 96p.: Il. 52.

Petrochenko, V. I. 1971. Acanthocephala of

domestic and wild animals. Academy os

Sciences of the USSR. Israel Program for

Scientific Translations Ltd, v 1 e 2, 940p.

Piersma, T, Van Gils, J & Wiersma, P. 1996.

Family Scolopacidae (sandpipers and

allies). pp. 444-533. In: Del Hoyo, J,

Elliott, A & Sargatal, J. (ed.). Handbook

of birds of the world, vol. 3. Barcelona:

Lynx Ed.

Swales, WE. 1933. Streptovilla acadiae gen. et

spc. Nov. a trematode of the family

Heterophydae from the black duck (Anas

rubripes), Journal of Helminthology,

vol. 11, pp.115.

of a new species of Maritrema Nicoll

1907, Maritrema arenaria, with studies

of the life history, Biological Bulletin,

vol. 78, pp. 338-348.

Hoklova, IG. 1971. Revision of the genus

P o l y m o r p h u s L u h e , 1 9 1 1

(Acanthocephala: Polymorphidae).

Trudi Gelmintol. Lab. Akad. Nauk

SSSR, vol. 21, pp. 130-126. (In

Russian).

Møller, AVP & Erritzøe, J. 1999. Host immune

defence and migration in birds.

Evolutionary. Ecology, vol. 12, pp. 945-

953.

Mouritsen, KVN, Jensen, T & Jensen, T. 1997.

Parasites on an intertidal Corophium-

bed: factors determining the phenology

of microphallid trematodes in the

intermediate host populations of the

mud-snail Hydrobia ulvae and the

amphipod Corophium volutator.

Hydrobiologia, vol. 355, pp. 61-70.

Received May 30, 2016.

Accepted August 25, 2016.

Neotropical Helminthology. Vol. 10, Nº2, jul-dic 2016 Nunes Gomes et al.

168