Eye trematode infection in small passerines in Peru caused by Philophthalmus lucipetus, an agent with a zoonotic potential spread by an invasive freshwater snail
Graphical abstract
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
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2022, Veterinary Parasitology: Regional Studies and ReportsCitation Excerpt :In addition, it is important to mention that studies point to the maintenance of the transmission area for P. gralli by M. tuberculata, even after 2 years of the removal of definitive hosts (Rojas et al., 2013; Heneberg et al., 2014), which demonstrate that the control of avian philophthalmosis is dependent on the control of the intermediate host. Melanoides tuberculata has been implicated in the transmission of P. gralli in Africa, Asia, Middle East, as well as in North America, Central America, and South America (Nollen and Kanev, 1995; Pinto and Melo, 2010; Church et al., 2013; Literák et al., 2013; Veeravechsukij et al., 2018). This invasive mollusk, which presents highly adaptive and reproductive capacity, is widely distributed in Brazil (Fernandez et al., 2003; Coelho et al., 2018), which can favor the spread of P. gralli across the country.
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2018, Veterinary ParasitologyCitation Excerpt :Infection of birds with species of Philophthalmus is considered a direct or indirect cause of eye damage (Alicata, 1962; Meise and Garcia-Parra, 2015, Heneberg et al., 2018). Despite increasing number of reports worldwide (Verocai et al., 2009; Literák et al., 2013; Heneberg et al., 2018), information regarding the epidemiology of philophthalmosis is scant. Diagnosis and treatment of infected birds, associated with management strategies, including the identification of water bodies where there is the presence of naturally infected molluscs, can be considered important strategies for the control of the disease (Mukaratirwa et al., 2005; Literák et al., 2013; Church et al., 2013; Rojas et al., 2013).