Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-26T05:57:19.424Z Has data issue: false hasContentIssue false
  • English
  • Français

Galactosomum otepotiense n. sp. (Trematoda: Heterophyidae) infecting four different species of fish-eating birds in New Zealand: genetically identical but morphologically variable

Published online by Cambridge University Press:  10 September 2019

B. Presswell Open the ORCID record for B. Presswell [Opens in a new window]  and
J. Bennett
B. Presswell*
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
J. Bennett
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
*
Author for correspondence: B. Presswell, E-mail: bpresswell@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Trematodes of the genus Galactosomum are cosmopolitan parasites that infect the intestines of fish-eating birds and mammals. Adults of named Galactosomum species have not been recorded from bird hosts in New Zealand, despite their cercarial stage being known from various studies of the first intermediate host, Zeacumantus subcarinatus. Here we describe a new species of Galactosomum infecting four different piscivorous birds in New Zealand: Caspian terns, red-billed and black-backed gulls and little blue penguins. Specimens from each of these hosts are genetically identical in the genes sequenced, but show considerable morphological variability. Galactosomum otepotiense n. sp. is distinguished from most other members of the ‘bearupi-group’ in having a single circle of spines on the ventral sucker, and spines, as opposed to scales, over most of the body. It is most similar to G. bearupi and G. angelae, both from Caspian terns in Australia, but differs in the relative sizes of the reproductive organs and in the possession of a very long forebody. Molecular data confirm that G. otepotiense is not conspecific with G. bearupi, but 28S and ITS2 phylogenies show its close relationship to G. bearupi and other Australian species. We use the cox1 sequence to confirm identity with the larval stage infecting Z. subcarinatus, as previously described in the literature. We discuss briefly the relationships between Australian and New Zealand Galactosomum spp. and their hosts, variability between genetically identical specimens found in different hosts and their potential for harm to mariculture economy.

Keywords

Hydroprogne caspiaLarus dominicanusChroicocephalus scopulinusEudyptula novaehollandiaeNew ZealandGalactosomum new specieshost-induced variability
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e86
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bakke, TA (1976) Functional morphology and surface topography of Leucochloridium sp. (Digenea), revealed by scanning electron microscopy. Zeitschrift für Parasitenkunde 51(1), 115–128.Google Scholar
Bartoli, P and Boudouresque, CF (2007) Effect of the digenean parasites of fish on the fauna of Mediterranean lagoons. Parassitologia 49(3), 111–117.Google Scholar
Belden, LK, Peterman, WE, Smith, SA, Brooks, LR, Benfield, EF, Black, WP, Yang, Z and Wojdak, JM (2012) Metagonimoides oregonensis (Heterophyidae: Digenea) infection in Pleurocerid snails and Desmognathus quadramaculatus salamander larvae in southern Appalachian streams. Journal of Parasitology 98(4), 760–768.Google Scholar
Blankespoor, HD (1974) Host-induced variation in Plagiorchis noblei Park, 1936 (Plagiorchiidae: Trematoda). American Midland Naturalist 92(2), 415–433.Google Scholar
Blasco-Costa, I and Poulin, R (2017) Parasite life-cycle studies: a plea to resurrect an old parasitological tradition. Journal of Helminthology 91, 647–656.Google Scholar
Bowles, J, Hope, M, Tiu, WU, Liu, X and McManus, DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Tropica 55(4), 217–229.Google Scholar
Cribb, TH, Adlard, RD and Bray, RA (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology 28(11), 1791–1795.Google Scholar
Cribb, TH, Adlard, RD, Bray, RA, Sasal, P and Cutmore, SC (2014a) Biogeography of tropical Indo-West Pacific parasites: a cryptic species of Transversotrema and evidence for rarity of Transversotrematidae (Trematoda) in French Polynesia. Parasitology International 63(2), 285–294.Google Scholar
Cribb, TH, Miller, TL, Bray, RA and Cutmore, SC (2014b) The sexual adult of Cercaria praecox Walker, 1971 (Digenea: Fellodistomidae), with the proposal of Oceroma n.g. Systematic Parasitology 88(1), 1–10.Google Scholar
Cutmore, SC, Bennett, MB and Cribb, TH (2010) Staphylorchis cymatodes (Gorgoderidae: Anaporrhutinae) from carcharhiniform, orectolobiform and myliobatiform elasmobranchs of Australasia: low host specificity, wide distribution and morphological plasticity. Parasitology International 59(4), 579–586.Google Scholar
Dailey, MD, Demaree, RS and Critchfield, RL (2002) Galactosomum stelleri sp. n. (Trematoda: Heterophyidae) from the northern sea-lion, Eumetopias jubatus (Schreber, 1776) (Carnivora: Otariidae). Comparative Parasitology 69(1), 58–62.Google Scholar
Diamond, JM (1984) Distributions of New Zealand birds on real and virtual islands. New Zealand Journal of Ecology 7, 37–55.Google Scholar
El Abdou, N, Betalgy, SM, Heckmann, RA and Ashour, AA (2001) Pseudoplagioporus interruptus Durio and Manter, 1968 and Hamacreadium agyptia sp. n. (Trematoda: Opecoeliidae) from the Red Sea fish in Egypt. Journal of King Abdulaziz University Marine Sciences 12(1), 175–188.Google Scholar
Fischthal, JH and Kuntz, RE (1972) Some digenetic trematodes of birds from Palawan Island, Philippines. Journal of Helminthology 46(4), 363–380.Google Scholar
Flemming, SA, Lalas, C and van Heezik, Y (2013) Little penguin (Eudyptula minor) diet at three breeding colonies in New Zealand. New Zealand Journal of Ecology 37(2), 199–205.Google Scholar
Fraser, MM and Lalas, C (2004) Seasonal variation in the diet of blue penguins (Eudyptula minor) at Oamaru, New Zealand. Notornis 51(1), 7–15.Google Scholar
Georgieva, S, Selbach, C, Faltýnková, A, Soldánová, M, Sures, B, Skírnisson, K and Kostadinova, A (2013) New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasites & Vectors 6, 64.Google Scholar
Georgieva, S, Blasco-Costa, I and Kostadinova, A (2017) Molecular characterisation of four echinostomes (Digenea: Echinostomatidae) from birds in New Zealand, with descriptions of Echinostoma novaezealandense n. sp. and Echinoparyphium poulini n. sp. Systematic Parasitology 94(4), 477–497.Google Scholar
Given, AD, Mills, JA and Baker, AJ (2005) Molecular evidence for recent radiation in southern hemisphere masked gulls. The Auk 122(1), 268–279.Google Scholar
Grosser, S, Burridge, CP, Peucker, AJ and Waters, JM (2015) Coalescent modelling suggests recent secondary-contact of cryptic penguin species. PLoS One 10(12).Google Scholar
Grosser, S, Scofield, RP and Waters, JM (2017) Multivariate skeletal analyses support a taxonomic distinction between New Zealand and Australian Eudyptula penguins (Sphenisciformes: Spheniscidae). Emu – Austral Ornithology 117(3), 276–283.Google Scholar
Guilloteau, P, Poulin, R and MacLeod, CD (2016) Impacts of ocean acidification on multiplication and caste organisation of parasitic trematodes in their gastropod host. Marine Biology 163, 96.Google Scholar
Harper, JT and Saunders, GW (2001) The application of sequences of the ribosomal cistron to the systematics and classification of the florideophyte red algae (Florideophyceae, Rhodophyta). Cahiers de Biologie Marine 42(1/2), 25–38.Google Scholar
Heneberg, P, Faltynkova, A, Bizos, J, Mala, M, Ziak, J and Literak, I (2015) Intermediate hosts of the trematode Collyriclum faba (Plagiochiida: Collyriclidae) identified by an integrated morphological and genetic approach. Parasites and Vectors 8(85). doi: 10.1186/s13071-015-0646-3.Google Scholar
Hernández-Orts, JS, Georgieva, S, Landete, DN and Scholz, T (2019) Heterophyid trematodes (Digenea) from penguins: a new species of Ascocotyle Looss, 1899, first description of metacercaria of Ascocotyle (A.) patagoniensis Hernández-Orts et al. (2012), and first molecular data. International Journal for Parasitology: Parasites and Wildlife 8, 94–105.Google Scholar
Hildebrand, J, Adamczyk, M, Laskowski, Z and Zaleśny, G (2015) Host-dependent morphology of Isthmiophora melis (Schrank, 1788) Lühe, 1909 (Digenea, Echinostomatinae) – morphological variation vs. molecular stability. Parasites & Vectors 8(1), 481.Google Scholar
Hostettler, R, Cutmore, SC and Cribb, TH (2018) Two new species of Haplorchoides Chen, 1949 (Digenea: Heterophyidae) infecting an Australian siluriform fish, Neoarius graeffei Kner & Steindachner. Systematic Parasitology 95(2–3), 201–211.Google Scholar
Huelsenbeck, J and Ronquist, F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.Google Scholar
Huston, DC, Cutmore, SC and Cribb, TH (2018) Molecular systematics of the digenean community parasitising the cerithiid gastropod Clypeomorus batillariaeformis Habe & Kusage on the Great Barrier Reef. Parasitology International 67(6), 722–735.Google Scholar
Kearn, GC (1998) Parasitism and the platyhelminths. London, Chapman & Hall.Google Scholar
Kearse, M, Moir, R, Wilson, A, et al. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12), 1647–1649.Google Scholar
Kimura, M and Endo, M (1979) Whirling disease caused by metacercaria of a fluke. Fish Pathology 13(4), 211–213 [in Japanese].Google Scholar
Králová-Hromadová, I, Špakulová, M, Horáčková, E, et al. (2008) Sequence analysis of ribosomal and mitochondrial genes of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae): intraspecific variation and differentiation from Fasciola hepatica. Journal of Parasitology 94(1), 58–68.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7), 1870–1874.Google Scholar
Kuzmina, TA, Tkach, VV, Spraker, TR, Lyons, ET and Kudlai, O (2018) Digeneans of northern fur seals Callorhinus ursinus (Pinnipedia: Otariidae) from five subpopulations on St. Paul Island, Alaska. Parasitology Research 117(4), 1079–1086.Google Scholar
Lawrence, SA and Poulin, R (2016) Detection of the bacterial endosymbiont Neorickettsia in a New Zealand digenean. Parasitology Research 115(11), 4275–4279.Google Scholar
Le, TH, Nguyen, KT, Nguyen, NTB, Doan, HTT and Blair, D (2017) The ribosomal transcription units of Haplorchis pumilio and H. taichui and the use of 28S rDNA sequences for phylogenetic identification of common heterophyids in Vietnam. Parasites & Vectors 10(1), 17.Google Scholar
León-Régagnon, V, Brooks, DR and Pérez-Ponce de León, G (1999) Differentiation of Mexican species of Haematoloechus Loos, 1899 (Digenea: Plagiorchiformes): molecular and morphological evidence. Journal of Parasitology 85, 935–946.Google Scholar
Leung, TLF, Donald, KM, Keeney, DB, Koehler, AV, Peoples, RC and Poulin, R (2009) Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. New Zealand Journal of Marine and Freshwater Research 43(4), 857–865.Google Scholar
Liu, OR, Molina, R, Wilson, M and Halpern, BS (2018) Global opportunities for mariculture development to promote human nutrition. PeerJ 6, e4733.Google Scholar
Lloyd, MM and Poulin, R (2011) In vitro culture of marine trematodes from their snail first intermediate host. Experimental Parasitology 129(2), 101–106.Google Scholar
MacLeod, CD and Poulin, R (2015) Differential tolerances to ocean acidification by parasites that share the same host. International Journal for Parasitology 45(7), 485–493.Google Scholar
Martorelli, SR, Fredensborg, BL, Leung, TLF and Poulin, R (2008) Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). New Zealand Journal of Zoology 35(1), 73–84.Google Scholar
Masala, S, Piras, MC, Sanna, D, Chai, JY, Jung, BK, Sohn, WM, Garippa, G and Merella, P (2016) Epidemiological and molecular data on heterophyid trematode metacercariae found in the muscle of grey mullets (Osteichthyes: Mugilidae) from Sardinia (western Mediterranean Sea). Parasitology Research 115(9), 3409–3417.Google Scholar
McKenna, PB (2009) Register of new host-parasite records. Surveillance 36, 14–15.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. in 2010 Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, pp. 1–8.Google Scholar
Nolan, MJ and Cribb, TH (2005) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 101–163.Google Scholar
Ogawa, K (2015) Diseases of cultured marine fishes caused by Platyhelminthes (Monogenea, Digenea Cestoda). Parasitology 142(1), 178–195.Google Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DT (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33(7), 733–755.Google Scholar
Otubanjo, OA (1985) Scanning electron microscopic studies of the body surface and external genitalia of a dicrocoeliid trematode, Concinnum epomopis Sandground 1973. Zeitschrift für Parasitenkunde 71(4), 495–504.Google Scholar
Pearson, J (1964) A revision of the subfamily Haplorchinae Looss, 1899 (Trematoda: Heterophyidae). I. The Haplorchis group. Parasitology 54, 601–676.Google Scholar
Pearson, J (1973) A revision of the subfamily Haplorchinae Looss, 1899 (Trematoda: Heterophyidae). II. Genus Galactosomum. Philosophical Transactions of the Royal Society of London B 266(879), 341–447.Google Scholar
Pearson, J (2008) Heterophyidae. pp. 113–142, Vol. 3 in Bray, RA, Gibson, DI and Jones, A (Eds) Keys to the Trematoda. Wallingford, UK, CABI.Google Scholar
Pérez Ponce de León, G (1995) Host-induced morphological variability in adult Posthodiplostomum minimum (Digenea: Neodiplostomidae). Journal of Parasitology 81(5), 818–820.Google Scholar
Pornruseetairatn, S, Kino, H, Shimazu, T, Nawa, Y, Scholz, T, Ruangsittichai, J, Saralamba, NT and Thaenkham, U (2016) A molecular phylogeny of Asian species of the genus Metagonimus (Digenea) – small intestinal flukes – based on representative Japanese populations. Parasitology Research 115(3), 1123–1130.Google Scholar
Presswell, B, Poulin, R and Randhawa, HS (2012) First report of a gryporhynchid tapeworm (Cestoda: Cyclophyllidea) from New Zealand and from an eleotrid fish, described from metacestodes and in vitro-grown worms. Journal of Helminthology 86(4), 453–464.Google Scholar
Sándor, D, Molnár, K, Gibson, DI, Székely, C, Majoros, G and Cech, G (2017) An investigation of the host-specificity of metacercariae of species of Apophallus (Digenea: Heterophyidae) in freshwater fishes using morphological, experimental and molecular methods. Parasitology Research 116(11), 3065–3076.Google Scholar
Sato, H, Ihara, S, Inaba, O and Une, Y (2010) Identification of Euryhelmis costaricensis metacercariae in the skin of Tohoku hynobiid salamanders (Hynobius lichenatus), northeastern Honshu, Japan. Journal of Wildlife Diseases 46(3), 832–842.Google Scholar
Shumenko, PG, Tatonova, YV and Besprozvannykh, VV (2017) Metagonimus suifunensis sp. n. (Trematoda: Heterophyidae) from the Russian Southern Far East: Morphology, life cycle, and molecular data. Parasitology International 66(1), 982–991.Google Scholar
Smales, LR and Blankespoor, HD (1984) Echinostoma revolutum (Froelich, 1802) Looss, 1899 and Isthmiophora melis (Schrank, 1788) Lühe, 1909 (Echinostomatinae, Digenea): scanning electron microscopy of the tegumental surfaces. Journal of Helminthology 58(3), 187–195.Google Scholar
Snyder, SD and Tkach, VV (2009) Haplorchis popelkae n. sp. (Digenea: Heterophyidae) from short-necked turtles (Chelidae) in Northern Australia. Journal of Parasitology 95, 204–207.Google Scholar
Studer, A and Poulin, R (2012) Seasonal dynamics in an intertidal mudflat: the case of a complex trematode life cycle. Marine Ecology Progress Series 455, 79–93.Google Scholar
Stunkard, HW (1957) Intraspecific variation in parasitic flatworms. Systematic Zoology 6(1), 7–18.Google Scholar
Tatonova, YV, Shumenko, PG and Besprozvannykh, VV (2018) Description of Metagonimus pusillus sp. nov. (Trematoda: Heterophyidae): phylogenetic relationships within the genus. Journal of Helminthology 92(6), 703–712.Google Scholar
Thaenkham, U, Nawa, Y, Blair, D and Pakdee, W (2011) Confirmation of the paraphyletic relationship between families Opisthorchiidae and Heterophyidae using small and large subunit ribosomal DNA sequences. Parasitology International 60(4), 521–523.Google Scholar
Thaenkham, U, Blair, D, Nawa, Y and Waikagul, J (2012) Families Opisthorchiidae and Heterophyidae: are they distinct? Parasitology International 61, 90–93.Google Scholar
Yasunaga, N (1981) On the marine-fish disease caused by Galactosomum sp. with special reference to its species and life cycle. Bulletin of the Nagasaki Prefecture Institute of Fisheries 7, 65–76.Google Scholar