Eye trematode infection in small passerines in Peru caused by Philophthalmus lucipetus, an agent with a zoonotic potential spread by an invasive freshwater snail

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Highlights

  • Passerine bird reported for the first time as eye trematode host in South America.

  • DNA sequence of the first South American eye trematode is provided.

  • P. lucipetus is spread by invasive water snail and found for the first time in Peru.

  • P. lucipetus was highly prevalent (48%) in its definitive host Tachuris rubrigastra.

  • P. lucipetus was highly prevalent (31%) in its intermediate host Melanoides tuberculata.

Abstract

Until now, four species of eye trematodes have been found in South America. Of them, Philophthalmus lucipetus (synonymized with Philophthalmus gralli) displays a broad host spectrum, with at least 30 bird species (prevalently large water birds), five mammal species and humans serving as definitive hosts, and with snails Fagotia (Microcolpia) acicularis, Amphimelania holandri, Melanopsis praemorsa and Melanoides tuberculata serving as intermediate hosts. When examining a total of 50 birds of ten species in the wetland of Pantanos de Villa, Lima, Peru in July 2011, eye trematodes were identified visually in the edematous conjunctival sac of 11 (48%) out of 23 resident many-colored rush tyrants Tachuris rubrigastra. Based on morphometric characteristics, the trematodes were identified as P. lucipetus. ITS2 and CO1 gene of the examined specimens combined showed a 99% similarity to an Iranian isolate of Philophthalmus sp. from the intermediate host Melanoides tuberculata, an invasive freshwater snail, suggesting that these two isolates represent the same species with a wide geographical range. Moreover, the prevalence of infection with the philophthalmid cercariae was 31% in 744 Melanoides tuberculata examined in Pantanos de Villa in 2010. It is evident that P. lucipetus occurs throughout the world as well as locally, including Eurasia and South America. Here we report this trematode for the first time in Peru, and we were the first to sequence any of the South American eye trematodes. Low host specificity of P. lucipetus and the invasive character of Melanoides tuberculata as a competent intermediate host suggest that eye trematodosis caused by P. lucipetus may emerge frequently in various parts of the world, especially in the tropics. Increase of the zoonotic potential of the P. lucipetus associated with this invasive snail spreading across the world is predictable and should be of interest for further research.

Introduction

Eye trematodes (Echinostomata: Philophthalmidae Loos, 1819) of the genus Philophthalmus Loos, 1899 (including recently proposed but already questioned genus Natterophthalmus Radev, Kanev, Nollen and Sattmann, 1996) are cosmopolitan parasites, occurring as adults mostly in conjuctival sacs in various birds and mammals [1]. Human cases of philophthalmosis have previously been reported in Europe, Asia, and North America (i.e., former Yugoslavia, Sri Lanka, Japan, Israel, Mexico, and the United States); for a review cf. J. Waikagul et al. [2].

Until now, four species of the eye trematodes have been found in South America. Philophthalmus zalophi Dailey, Ellin and Paras, 2005 has recently been described from a mammalian host, the Galapagos fur seal Arctocephalus galapagoensis at the Galapagos Islands, Ecuador [3]. Other species of eye trematodes are known from continental South America. Philophthalmus lachrymosus Braun, 1902 (also frequently spelled out as P. lacrymosus or P. lacrimosus) was described on the basis of Brazilian trematode samples recovered from eyes of brown-hooded gulls Chroicocephalus maculipennis [4]. All other findings of P. lachrymosus in birds originated also from Brazil: J. F. T. Freitas [5] revealed great egret Ardea alba, yellow-crowned night heron Nyctanassa violacea and royal tern Thalasseus maximus as final hosts for the parasite. The species was also found in the conjunctival sacs of kelp gull Larus dominicanus [6]. Moreover, adult P. lachrymosus was found in human eyes in Mexico [7], and in the eyes of capybaras Hydrochaeris hydrochaeris in Brazil [8]. Philophthalmus semipalmatus Nasir and Diaz, 1972 was synonymized with Philophthalmus lachrymosus by R. M. Pinto et al. [8], but is noted as a valid species by H. U. Pinto and A. L. de Melo [9]. P. semipalmatus was described in Venezuela based on the finding of the trematode in willet Tringa semipalmata [10]. P. lucipetus (Rudolphi, 1819) identified as P. gralli Mathis and Leger, 1910 was found in white-cheeked pintail Anas bahamensis and Brazilian teal Amazonetta braziliensis, and in an intermediate snail host red-rimmed melania Melanoides tuberculata in Brazil [9], [11]. P. gralli was synonymized with P. lucipetus from Eurasia and the Americas [1]. At least 30 different bird species (mostly large water birds of the families Anatidae, Ardeidae, Laridae or Scolopacidae), five mammal species and humans living in different parts of Europe were found as definitive hosts of P. lucipetus. Snails Fagotia (Microcolpia) acicularis, Amphimelania holandri, and Melanopsis praemorsa were revealed as intermediate hosts of P. lucipetus [12]. Recently, P. lucipetus infection was reported from captive greater rheas Rhea americana, where Melanoides tuberculata were reported as intermediate hosts [13].

Here we focus on the highly prevalent eye trematode infection of a small resident passerine bird species in the wetland of Pantanos de Villa within the agglomeration of Lima, Peru, which we observed in 2011. Here we report the first record of a passerine bird as a host of eye trematodes in South America. We identified the species of eye trematode that caused this infection using morphometric features and provide supplemental molecular data for the species. Regarding a discussion of this case, we used the results of the research which characterized the trematode community found in a population of Melanoides tuberculata in Pantanos de Villa in 2010.

Section snippets

Study area

Birds were examined in a wetland at sea level in Refugio de Vida Silvestre Los Pantanos de Villa, Lima, Peru (12°13′S, 76°59′W). This protected area was established in 1989 and since 1997 the RAMSAR Convention has recognized it as an internationally important area for aquatic birds. It spans across 396 ha and it is the only protected area which exists within the urban agglomeration of Lima. Los Pantanos de Villa is an integral part of the hydrological system of the Rimac River, whose underground

Morphology of adult eye trematodes

Eye trematodes were found in 11 (48%) out of 23 T. rubrigastra. In eight cases both eyes were affected while in three cases only one eye of a bird was affected. Lower eyelids of the infected birds were edematous and in some infected individuals we found serous eye discharge (Fig. 1). The number of trematodes varied from two to 13 (mean 5.3) in individual birds.

The brief description (Fig. 2): Body pyriform, long 1.800–2.429 (average 2.111), maximum width 0.671–1.429 (0.958) in the second third

Discussion

Only T. rubrigastra was found parasitized with P. lucipetus. Tyrants T. rubrigastra are resident birds in Peru and the prevalence of 48% of birds infected with the P. lucipetus in the Pantanos de Villa population was surprisingly high. The clinical signs observed in the infected T. rubrigastra consisted of conjunctivitis, lower eyelid edema and serous eye discharge. It is consistent with the fact that the formerly reported heavily infected birds had symptoms including an irritation of

Ethics statement

All the animal-based experiments were performed according to the USGS National Wildlife Health Center Field Manual of Wildlife Disease — General Field Procedures and Diseases of Birds (available from http://www.nwhc.usgs.gov/publications/field_manual/), and according to the Instructions for the Activity of Collaborators of the Praha Bird Ringing Centre, National Museum Praha, Czech Republic (http://www.czechringing.com/download/pokyny.pdf). The field work in the wetland reserve was approved by

Acknowledgments

We thank Martina Literaková, Zuzana Literaková and Liziie Ortiz Cam for the help in the field. We also thank Milena Malá and Marcela Znamirowská for expert technical assistance. The study was supported in part by the projects UNCE 204015 and PRVOUK P31/2012 from the Charles University in Prague, by the project P301/12/1686 from the Czech Science Foundation, project IAA601690901 of the Grant Agency of the Academy of Sciences of the Czech Republic, project NT13663-3/2012 of the Internal Grant

References (31)

  • L.J. Smith et al.

    Extraction of cellular DNA from human cells and tissues fixed in ethanol

    Analytical Biochemistry

    (1987)
  • P. Heneberg et al.

    Molecular phylogenetic characterization of Collyriclum faba with reference to its three host-specific ecotypes

    Parasitology International

    (2013)
  • P.D. Olson et al.

    Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda)

    International Journal of Parasitology

    (2003)
  • V. Radev et al.

    Comments on eye-flukes (Philophthalmidae Loos, 1819) in the genera Philophthalmus and Natterophthalmus, with a re-designation of the type-species of Natterophthalmus

    Zootaxa

    (2006)
  • J. Waikagul et al.

    Conjunctiva philophthalmosis: a case report in Thailand

    The American Journal of Tropical Medicine and Hygiene

    (2006)
  • M. Dailey et al.

    First report of parasites from pinnipeds in the Galapagos Island, Ecuador, with a description of a new species of Philophthalmus (Digenea: Philophthalmidae)

    Journal of Parasitology

    (2005)
  • M. Braun

    Fascioliden der Vögel

    Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere

    (1902)
  • J.F.T. Freitas

    Sobre dois trematodeos parasitos de aves: Philophthalmus lachrymosus Braun, 1902 e Renicola mirandaribeiroi n. sp.

    Arquivos do Museu Nacional

    (1955)
  • L. Travassos et al.

    Excursao a Cabo Frio, Estado do Rio de Janeiro

    Atas de Sociedade de Biologia do Rio de Janeiro

    (1960)
  • R. Lamothe-Argumedo et al.

    The first human case in Mexico of conjunctivitis caused by the avian parasite, Philophthalmus lacrimosus

    Journal of Parasitology

    (2003)
  • R.M. Pinto et al.

    Pathology and first report of natural infections of the eye trematode Philophthalmus lachrymosus Braun, 1902 (Digenea, Philophthalmidae) in a non-human mammalian host

    Memórias do Instituto Oswaldo Cruz

    (2005)
  • H.U. Pinto et al.

    Melanoides tuberculata as intermediate host of Philophthalmus gralli in Brazil

    Revista do Instituto de Medicina Tropical de São Paulo

    (2010)
  • P. Nasir et al.

    Avian flukes of Venezuela

    Rivista di Parassitologia

    (1972)
  • L.C. Muniz-Pereira et al.

    Philophthalmus gralli (Digenea: Philophthalmidae) parasite of Anas bahamensis and Amazonetta brasiliensis, from lagoons of Marica county, Rio de Janeiro, Brazil

    Memórias do Instituto Oswaldo Cruz

    (1993)
  • I. Kanev et al.

    Redescription of Philophthalmus lucipetus (Rudolphi, 1819) (Trematoda: Philophthalmidae) with a discussion of its identity and characteristics

    Annalen des Naturhistorischen Museums in Wien

    (1993)
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