Abstract
Being listed in the IUCN Red List of Threatened Species, knowledge on the biology, health and diseases of the scalloped hammerhead, Sphyrna lewini (Griffith & Smith) is limited; this is especially true for its parasites. In this paper, a new species, Pulchrascaris australis, is morphologically described followed by genetic characterisation based on the sequence of the ITS region. The new species can be easily differentiated from its congeners based on the morphology of the mouthpart, spicules, plectanes, eggs and vulva. Phylogenetic analyses clearly distinguish specimens in the present study from other parasitic nematodes found in the Australasian waters and elsewhere. The sequencing data also suggest that Terranova larval type I found previously in various fish from New Caledonian and Australian (Queensland) waters also belong to Pulchrascaris australis n. sp.
Similar content being viewed by others
References
Arizono N, Miura T, Yamada M, Tegoshi T, Onishi K (2011) Human infection with Pseudoterranova azarasi roundworm. Emerg Infect Dis 17(3):555–556. https://doi.org/10.3201/eid1703.101350
Bahlool QZ, Skovgaard A, Kania P, Haarder S, Buchmann K (2012) Microhabitat preference of Anisakis simplex in three salmonid species: immunological implications. Vet Parasitol 190(3–4):489–495. https://doi.org/10.1016/j.vetpar.2012.07.009
Baum J et al (2019) Sphyrna lewini. The IUCN Red List of Threatened Species 2009: e.T39385A10190088. Downloaded on 31 May. https://doi.org/10.2305/IUCN.UK.2007.RLTS.T39385A10190088.en
Bruce NL, Cannon LRG (1990) Ascaridoid nematodes from sharks from Australia and the Solomon Islands, southwestern Pacific Ocean. Invertebr Taxon 4(4):763–783
Chandler AC (1935) Parasites of fishes in Galveston Bay. Proceedings of the United States National Museum 83:123–157
Chelladurai JJ, Bader C, Snobl T, Magstadt D, Cooper V, Brewer MT (2015) Toxocara vitulorum infection in a cohort of beef calves in Iowa. Vet Parasitol 214(1–2):96–99. https://doi.org/10.1016/j.vetpar.2015.10.004
D'Amelio S, Cavallero S, Dronen NO, Barros NB, Paggi L (2012) Two new species of Contracaecum Railliet & Henry, 1912 (Nematoda: Anisakidae), C. fagerholmi n. sp. and C. rudolphii F from the brown pelican Pelecanus occidentalis in the northern Gulf of Mexico. Syst Parasitol 81(1):1–16. https://doi.org/10.1007/s11230-011-9323-x
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772–772. https://doi.org/10.1038/nmeth.2109
Fagerholm HP (1979) Nematode length and preservatives, with a method for determining the length of live specimens. J Parasitol 65(2):334–335
Fagerholm HP, Lovdahl M (1984) Induced morphometric variation in the preparation of nematode parasites for the Lm and Sem. Syst Parasitol 6(4):245–247. https://doi.org/10.1007/Bf00012196
Froese R, Pauly D, Editors (2019) FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2019)
Gibson DI, Colin JA (1982) The Terranova enigma. Parasitology 85(OCT):R36–R37
Gilbert CR (1967) A revision of the hammerhead sharks (family Sphyrnidae). Proceedings of the United States National Museum
Gonzalez-Solis D et al (2019) Parasitic nematodes of marine fishes from Palmyra Atoll, East Indo-Pacific, including a new species of Spinitectus (Nematoda, Cystidicolidae). ZooKeys 892:1–26. https://doi.org/10.3897/zookeys.892.38447
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hermosilla C, Hirzmann J, Silva LMR, Brotons JM, Cerdà M, Prenger-Berninghoff E, Ewers C, Taubert A (2018) Occurrence of anthropozoonotic parasitic infections and faecal microbes in free-ranging sperm whales (Physeter macrocephalus) from the Mediterranean Sea. Parasitol Res 117(8):2531–2541. https://doi.org/10.1007/s00436-018-5942-3
Jabbar A et al (2012) Larval anisakid nematodes in teleost fishes from Lizard Island, northern Great Barrier Reef, Australia. Mar Freshw Res 63(12):1283–1299. https://doi.org/10.1071/MF12211
Johnston TH, Mawson PM (1945) Some parasitic nematodes from south Australian marine fish. Transactions of the Royal Society of South Australia 69(1):114–117
Johnston TH, Mawson PM (1951a) Additional nematodes from Australian fish. Trans R Soc S Aust 74(1):18–24
Johnston TH, Mawson PM (1951b) Report on some parasitic nematodes from the Australian Museum. Rec Aust Mus 22(4):289–297
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166. https://doi.org/10.1093/bib/bbx108
Kijewska A, Dzido J, Shukhgalter O, Rokicki J (2009) Anisakid parasites of fishes caught on the African shelf. J Parasitol 95(3):639–645. https://doi.org/10.1645/ge-1796.1
Leiper RT, Atkinson EL (1914) Helminthes of the British Antarctic Expedition 1910–1913. Proc Zool Soc London:222–226
Lent H, Freitas JFTD (1948) Uma colecao de Nematodeos, parasitos de vertebrados, do Musea de Historia Natural de Montevideo. Mem Inst Oswaldo Cruz 46(1):1–71
Li L, Gibson DI, Liu YY, Zhang LP (2012) Morphological and molecular study of the poorly known species Pseudanisakis rajae (Yamaguti, 1941) (Nematoda: Acanthocheilidae) from elasmobranchs in the Yellow Sea and Taiwan Strait off the coast of China. Syst Parasitol 81(2):115–123. https://doi.org/10.1007/s11230-011-9331-x
Li L, Lü L, Nadler SA, Gibson DI, Zhang LP, Chen HX, Zhao WT, Guo YN (2018) Molecular phylogeny and dating reveal a terrestrial origin in the early carboniferous for ascaridoid nematodes. Syst Biol 67(5):888–900. https://doi.org/10.1093/sysbio/syy018
Mehrdana F, Bahlool QZ, Skov J, Marana MH, Sindberg D, Mundeling M, Overgaard BC, Korbut R, Strøm SB, Kania PW, Buchmann K (2014) Occurrence of zoonotic nematodes Pseudoterranova decipiens, Contracaecum osculatum and Anisakis simplex in cod (Gadus morhua) from the Baltic Sea. Vet Parasitol 205(3–4):581–587. https://doi.org/10.1016/j.vetpar.2014.08.027
Moravec F, Barton DP (2019) Description of Piscicapillaria bursata sp. nov.(Capillariidae) and redescription of Parascarophis sphyrnae Campana-Rouget, 1955 (Cystidicolidae), two nematode parasites of hammerhead sharks (Sphyrna spp.) off Australia. Acta Parasitol:1–13
Peng W-F, Liu S-F, Wang B-L, Wei M-M (2011) A checklist of parasitic nematodes from marine fishes of China. Syst Parasitol 79(1):17–40
Pron'kina NV, Spiridonov SE (2018) Morphological and molecular characterisation of anisakid juveniles from the golden grey mullet of the Black Sea. Russ J Nematol 26(1):87–92. https://doi.org/10.24411/0869-6918-2018-10008
Quiazon KM, Yoshinaga T, Santos MD, Ogawa K (2009) Identification of larval Anisakis spp. (Nematoda: Anisakidae) in Alaska pollock (Theragra chalcogramma) in northern Japan using morphological and molecular markers. J Parasitol 95(5):1227–1232. https://doi.org/10.1645/ge-1751.1
Rambaut A (2014) FigTree v1.4.2, a graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree/
Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Shamsi S, Suthar J (2016a) Occurrence of Terranova larval types (Nematoda: Anisakidae) in Australian marine fish with comments on their specific identities. PeerJ 4:e1722–e1722. https://doi.org/10.7717/peerj.1722
Shamsi S, Suthar J (2016b) A revised method of examining fish for infection with zoonotic nematode larvae. Int J Food Microbiol 227:13–16. https://doi.org/10.1016/j.ijfoodmicro.2016.03.023
Shamsi S, Chen Y, Poupa A, Ghadam M, Justine JL (2018a) Occurrence of anisakid parasites in marine fishes and whales off New Caledonia. Parasitol Res:3195–3204. https://doi.org/10.1007/s00436-018-6018-0
Shamsi S, Steller E, Chen Y (2018b) New and known zoonotic nematode larvae within selected fish species from Queensland waters in Australia. Int J Food Microbiol 272:73–82. https://doi.org/10.1016/j.ijfoodmicro.2018.03.007
Shamsi S, Barton DP, Zhu X (2019) Description and characterisation of Terranova pectinolabiata n. sp. (Nematoda: Anisakidae) in great hammerhead shark, Sphyrna mokarran (Rüppell, 1837), in Australia. Parasitol Res 118(7):2159–2168. https://doi.org/10.1007/s00436-019-06360-4
Skov J, Kania PW, Olsen MM, Lauridsen JH, Buchmann K (2009) Nematode infections of maricultured and wild fishes in Danish waters: a comparative study. Aquaculture 298(1–2):24–28
Szostakowska B, Myjak P, Kur J (2002) Identification of anisakid nematodes from the Southern Baltic Sea using PCR-based methods. Mol Cell Probes 16(2):111–118. https://doi.org/10.1006/mcpr.2001.0391
Thwaite JW (1927) On a collection of nematodes from Ceylon. Annals of Tropical Medicine and Parasitology 21:225–244
Umehara A, Kawakami Y, Ooi HK, Uchida A, Ohmae H, Sugiyama H (2010) Molecular identification of Anisakis type I larvae isolated from hairtail fish off the coasts of Taiwan and Japan. Int J Food Microbiol 143(3):161–165. https://doi.org/10.1016/j.ijfoodmicro.2010.08.011
Vicente JJ, dos Santos E (1972) Sobre um novo genero da subfamilia Filocapsulariinae Yamaguti, 1961 (Nematoda, Ascaridoidea). Atas de Sociedade de Biologia do Rio de Janerio 16:17–19
Weitzel T, Sugiyama H, Yamasaki H, Ramirez C, Rosas R, Mercado R (2015) Human infections with Pseudoterranova cattani nematodes, Chile. Emerg Infect Dis 21(10):1874–1875. https://doi.org/10.3201/eid2110.141848
Acknowledgements
Thanks are due to the various commercial fishers for the collection of shark specimens. Additionally, the authors are indebted to Ms. Brooke D’Alberto and many student helpers at James Cook University for their assistance in the processing of the shark specimens. In addition, the authors thank Dr. Michelle Heupel (JCU & AIMS, Townsville) and Prof Liang Li (Hebei Normal University, China) for their answers to queries.
Funding
Diane Barton was supported by the Marine Biodiversity Hub through funding from the Australian Government’s National Environmental Science Program. This study was partially funded by Charles Sturt University (A516-828-66770 (granted to SS)).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Una Ryan
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
Shamsi, S., Barton, D.P. & Zhu, X. Description and genetic characterisation of Pulchrascaris australis n. sp. in the scalloped hammerhead shark, Sphyrna lewini (Griffin & Smith) in Australian waters. Parasitol Res 119, 1729–1742 (2020). https://doi.org/10.1007/s00436-020-06672-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-06672-w