Abstract
Trematodes of the genus Philophthalmus are cosmopolitan parasites that infect the eyes of birds and mammals. They have the potential to affect the survival of their hosts and a few cases of human philophthalmiasis have occurred worldwide. Adults of known Philophthalmus species have never been recorded from bird hosts in New Zealand, despite their cercarial stage being a focus of various studies. Here, we describe a new species of Philophthalmus infecting New Zealand red-billed and black-backed gulls, Philophthalmus attenuatus n. sp. It is distinguished from other marine species of Philophthalmus by its long, thin body shape, consistently longer vitelline field on the left, and its body reflexed at the ventral sucker. We use molecular methods to complete the life cycle of this species, matching it with the larval stage infecting the mud whelk, Zeacumantus subcarinatus, and present a preliminary cox1 phylogeny. In addition, we comment on the validity of some taxonomic characters used to differentiate species of this genus, discuss potential colonisation routes to New Zealand and comment on the potential for zoonotic infection.
Similar content being viewed by others
References
Blasco-Costa I, Waters JM, Poulin R (2012) Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Mol Ecol 21(1):207–217
Bowles J, Hope M, Tiu WU, Xushian L, McManus DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Trop 55:217–229
Ching HL (1961) The development and morphological variation of Philophthalmus gralli Matthis and Leger, 1910, with a comparison of species of Philophthalmus Loos, 1899. P Helm Soc Wash 28:130–138
Dailey M, Ellin R, Parás (2005) First report of parasites from pinnipeds in the Galapagos Islands, Ecuador, with a description of a new species of Philophthalmus (Digenea: Philophthalmidae). J Parasitol 91(3):614–617
Dissanaike AS, Bilimoria DP (1958) On an infection of a human eye with Philophthaltmus sp. in Ceylon. J Helminthol 32(3):115–118
Dronen NO, Fried B (2008) Comparative study of the age classes of two species of Philophthalmus Loos, 1899 (Philophthalmidae: Philophthalminae). Comp Parasitol 75:12–23
Dronen NO, Penner LR (1975) Concerning Philophthalmus andersoni sp. n. (Trematoda: Philophthalmidae), another ocular helminth from birds which develops in a marine gastropod. U Connecticut Occ Pap. Biol Sci Ser 2:217–224
Given AD, Mills JA, Baker AJ (2005) Molecular evidence for recent radiation in southern hemisphere masked gulls. Auk 122(1):268–279
Gutierrez Y, Grossnikiaus HE, Annable WL (1987) Human conjunctivitis caused by the bird parasite Philophthalmus. Am J Ophthalmol 104(4):417–419
Heneberg P, Casero M, Waap H, Sitko J, Azevedo F, Těšínský M, Literák I (2018) An outbreak of philophthalmosis in Larus michahellis and Larus fuscus gulls in Iberian Peninsula. Parasitol Int 67(2):253–261
Howell MJ (1965) Notes on a potential trematode parasite of man in New Zealand. Tuatara 13(3):182–184
Howell MJ, Bearup AJ (1967) The life histories of two bird trematodes of the family Philophthalmidae. Proc Linn Soc NSW 92:182–194
Huelsenbeck JP, Ronquist F (2001) MRBAYES. Bayesian inference of phylogeny. Bioinformatics 17:754–755
Kalthoff H, Janitschke K, Mravak S, Schopp W, Werner H (1981) Ein ausgereifter saugwurm der gattung Philophthalmus unter der Bindehaut des Menschen. Klin Monatsbl Augenh 179(11):373–375
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence date. Bioinformatics 28:1647–1649
Keeney DB, King TM, Rowe DL, Poulin R (2009) Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites. Mol Ecol 18:4591–4603
Králová-Hromadová I, Špakulová M, Horáčková E, Turčeková L, Novobilský A, Beck R, Koudela B, Marinculić A, Rajský D, Pybus M (2001) Sequence analysis of ribosomal and mitochondrial genes of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae): intraspecific variation and differentiation from Fasciola hepatica. J Parasitol 94:58–67
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Lang Y, Weiss Y, Garzozi H, Gold D, Lengy J (1993) A first instance of human philophthalmosis in Israel. J Helminthol 67(2):107–111
Leung TLF, Poulin R (2011) Small worms, big appetites; ratios of different functional morphs in relation to interspecific competition in trematode parasites. Int J Parasitol 41:1063–1068
Leung TLF, Donald KM, Keeney DB, Koehler AV, Peoples RC, Poulin R (2009) Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. New Zeal J Mar Fresh Res 43:857–865
Literák I, Heneberg P, Sitko J, Wetzel EJ, Cardenas Callirgos JM, Čapek M, Valle Basto D, PapouŠek I (2013) Eye trematode infection in small passerines in Peru caused by Philophthalmus lucipetus an agent with a zoonotic potential spread by an invasive freshwater snail. Parasitol Int 62:390–396
Lloyd MM, Poulin R (2012) Fitness benefits of a division of labour in parasitic trematode colonies with and without competition. Intl J Parasitol 42:939–946
Lloyd MM, Poulin R (2014) Multi-clone infections and the impact of intraspecific competition of trematode colonies with a division of labour. Parasitology 141(2):304–310
Marković A (1939) Der erste fall von Philophthalmose beim Menschen. A Graefes Arch Ophthalmol 140(3):515–526
Martorelli SR, Fredensborg BL, Leung TLF, Poulin R (2008) Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). NZ J Zool 35:73–84
McGill AR (1943) Probable occurrence of the southern black-backed gull (Larus dominicanus) in Australia. Emu – Austral Ornithol 43(1):65–66
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments workshop (GCE). New Orleans, pp.1–8
Mimori T, Hirai H, Kifune T, Inada K (1982) Philophthalmus sp. (Trematoda) in a human eye. Am J Trop Med Hyg 31(4):859–861
Miura O, Kuris AM, Torchin ME, Hechinger RF, Dunham EJ, Chiba S (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batellaria cumingi (Crosse). Int J Parasitol 35:793–801
Mukaratirwa S, Hove T, Cindzi ZM, Maononga DB, Taruvinga M, Matenga E (2005) First report of an outbreak of the oriental eye-fluke, Philophthalmus gralli (Mathis & Leger 1910), in commercially reared ostriches (Struthio camelus) in Zimbabwe. Onderstepoort J Vet Res 72:203–206
Neal AT, Poulin R (2012) Substratum preference of Philophthalmus sp. cercariae for cyst formation under natural and experimental conditions. J Parasitol 98:293–298
Nollen PM, Kanev I (1995) The taxonomy and biology of philophthalmid eye flukes. In: Baker JR, Muller R, Rollinson D (eds) Adv Parasit. Academic Press, London, pp 205–269
O’Dwyer K, Blasco-Costa I, Poulin R, Faltynkova A (2014) Four marine digenean parasites of Austrolittorina spp. (Gastropoda: Littorinidae) in New Zealand: morphological and molecular data. Syst Parasitol 89(2):133–152
O’Dwyer K, Faltynkova A, Georgieva S, Kostadinova A (2015) An intergrative taxonomic investigation of the diversity of digenean parasites infecting the intertidal snail Austrolittorina unifasciata Gray, 1826 (Gastropoda: Littorinidae) in Australia. Parasitol Res 114(6):2381–2397
Penner LR, Fried B (1963) Philophthalmus hegeneri sp. n., an ocular trematode from birds. J Parasitol 49:974–977
Penner LR, Trimble JJ (1970) Philophthalmus larsoni sp. n., an ocular trematode from birds. U Connecticut Occ Pap Biol Sci 1:265–273
Phillips BE, Páez-Rosas D, Flowers JR, Cullen JM, Law JM, Colitz C, Dereresienski D, Lohmann KJ, Lewbart GA (2018) Evaluation of the ophthalmic disease and histopathologic effects due to the ocular trematode Philophthalmus zalophi on juvenile Galapagos sea lions (Zalophus wollebaeki). J Zoo Wildlife Med 49(3):581–590
Powell AWB (1979) New Zealand mollusca. William Collins Publishers Ltd, Auckland
Robertson CJR, Bell BD (1984) Seabird status and conservation in the New Zealand region. In: Croxall JP, Evans PGH, Schreiber RW (eds) Status and conservation of the world’s seabirds, ICBP Tech Pub No, vol 2. Princeton, Princeton University Press, pp 573–586
Woehler E, Patterson TA, Bravington MV, Hobday AJ, Chambers LE (2014) Climate and competition in abundance trends in native and invasive Tasmanian gulls. Mar Ecol Prog Ser 511:249–263
Acknowledgments
We thank Olivia McPherson for her help with the dissections.
Funding
This research was indirectly funded by a grant from the Marsden Fund (Royal Society of New Zealand) and a grant from the University of Otago’s Zoology Department PBRF Research Enhancement Fund, both to Robert Poulin.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Julia Walochnik
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bennett, J., Presswell, B. Morphology and molecules resolve the identity and life cycle of an eye trematode, Philophthalmus attenuatus n. sp. (Trematoda: Philophthalmidae) infecting gulls in New Zealand. Parasitol Res 118, 1501–1509 (2019). https://doi.org/10.1007/s00436-019-06289-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06289-8