Digenean trematode cysts within the heads of threatened Galaxiella species (Teleostei : Galaxiidae) from south-eastern Australia
R. A. Coleman A B C and A. A. Hoffmann A
+ Author Affiliations
- Author Affiliations
A Victorian Centre for Aquatic Pollution Identification and Management, Bio21 Institute, School of BioSciences, The University of Melbourne, Melbourne, Vic. 3010, Australia.
B Melbourne Water Corporation, Docklands, Melbourne, Vic. 3008, Australia.
C Corresponding author. Email: rhys.coleman@melbournewater.com.au
Australian Journal of Zoology 64(4) 285-291 https://doi.org/10.1071/ZO16004
Submitted: 18 January 2016 Accepted: 31 October 2016 Published: 24 November 2016
Abstract
The dwarf galaxias (Galaxiella pusilla) and little galaxias (Galaxiella toourtkoourt) are both threatened freshwater fish from south-eastern Australia. Occasionally populations have been found with enlarged heads associated with the accumulation of ‘white balls’, but the cause of these deformities has not previously been investigated. In this study, histopathology and molecular techniques were employed to identify cysts extracted from the heads of Galaxiella species across six populations. Histopathology and DNA sequences from both mitochondrial (cytochrome c oxidase subunit I) and nuclear (ribosomal internal transcribed spacer 1) regions identified the cysts as metacercariae of Apatemon gracilis (Rudolphi, 1819), a cosmopolitan digenean trematode species. Heavy infestations of trematode metacercariae within Galaxiella populations are of concern due to the potential to cause increased mortality associated with altered behaviour of the fish host that increases the likelihood of predation. Direct mortality from infestations is also possible, but not quantified in this study.
Additional keywords: Apatemon gracilis, COI, Galaxiella pusilla, Galaxiella toourtkoourt, ITS1.
References
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.| Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFyhu7w%3D&md5=74de219b2f2ebbab1a4f946fa3c5a7d0CAS |
Bell, A. S., and Sommerville, C. (2002). Molecular evidence for the synonymy of two species of Apatemon Szidat, 1928, A. gracilis (Rudolphi, 1819) and A. annuligerum (von Nordmann, 1832) (Digenea: Strigeidae) parasitic as metacercariae in British fishes. Journal of Helminthology 76, 193–198.
| Molecular evidence for the synonymy of two species of Apatemon Szidat, 1928, A. gracilis (Rudolphi, 1819) and A. annuligerum (von Nordmann, 1832) (Digenea: Strigeidae) parasitic as metacercariae in British fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xnsl2htbo%3D&md5=cbaf3d55a00369c518986c47eeaaa571CAS |
Bell, A. S., Sommerville, C., and Tellervo Valtonen, E. (2001). A molecular phylogeny of the genus Ichthyocotylurus (Digenea, Strigeidae). International Journal for Parasitology 31, 833–842.
| A molecular phylogeny of the genus Ichthyocotylurus (Digenea, Strigeidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Kit7Y%3D&md5=458ced75d74cbdc188a3f8861a26be73CAS |
Blair, D. (1976). Observations on the life-cycle of the strigeoid trematode Apatemon (Apatemon) gracilis (Rudolphi, 1819) Szidat, 1928. Journal of Helminthology 50, 125–131.
| Observations on the life-cycle of the strigeoid trematode Apatemon (Apatemon) gracilis (Rudolphi, 1819) Szidat, 1928.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s%2Fgs12qtw%3D%3D&md5=34b8d482963d2fd5e0ccd291f7b22a40CAS |
Blasco-Costa, I., Poulin, R., and Presswell, B. (2016). Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: linking and characterising life cycle stages with morphology and molecules. Parasitology Research 115, 271–289.
| Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: linking and characterising life cycle stages with morphology and molecules.Crossref | GoogleScholarGoogle Scholar |
Bowles, J., and McManus, D. P. (1993). Rapid discrimination of Echinococcus species and strains using a PCR-based method. Molecular and Biochemical Parasitology 57, 231–239.
| Rapid discrimination of Echinococcus species and strains using a PCR-based method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Kksr8%3D&md5=d06337b68fd961feb03fa6b0d9e04cedCAS |
Bowles, J., Blair, D., and McManus, D. P. (1995). A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103–109.
| A molecular phylogeny of the human schistosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntVaqt7w%3D&md5=bd3e2065359b17442eca6dce5ec75ffcCAS |
Chapman, A., Hobbs, R. P., Morgan, D. L., and Gill, H. S. (2006). Helminth parasitism of Galaxias maculatus (Jenyns 1842) in southwestern Australia. Ecology of Freshwater Fish 15, 559–564.
| Helminth parasitism of Galaxias maculatus (Jenyns 1842) in southwestern Australia.Crossref | GoogleScholarGoogle Scholar |
Coleman, R. A., Pettigrove, V., Raadik, T. A., Hoffmann, A. A., Miller, A. D., and Carew, M. E. (2010). Microsatellite markers and mtDNA data indicate two distinct groups in dwarf galaxias, Galaxiella pusilla (Mack) (Pisces: Galaxiidae), a threatened freshwater fish from south-eastern Australia. Conservation Genetics 11, 1911–1928.
| Microsatellite markers and mtDNA data indicate two distinct groups in dwarf galaxias, Galaxiella pusilla (Mack) (Pisces: Galaxiidae), a threatened freshwater fish from south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Coleman, R. A., Weeks, A. R., and Hoffmann, A. A. (2013). Balancing genetic uniqueness and genetic variation in determining conservation and translocation strategies: a comprehensive case study of threatened dwarf galaxias, Galaxiella pusilla (Mack) (Pisces: Galaxiidae). Molecular Ecology 22, 1820–1835.
| Balancing genetic uniqueness and genetic variation in determining conservation and translocation strategies: a comprehensive case study of threatened dwarf galaxias, Galaxiella pusilla (Mack) (Pisces: Galaxiidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvFyns7g%3D&md5=0c6a8cb680144af839883c79b03e2695CAS |
Coleman, R. A., Hoffmann, A. A., and Raadik, T. A. (2015). A review of Galaxiella pusilla (Mack) (Teleostei: Galaxiidae) in south-eastern Australia with a description of a new species. Zootaxa 4021, 243–281.
| A review of Galaxiella pusilla (Mack) (Teleostei: Galaxiidae) in south-eastern Australia with a description of a new species.Crossref | GoogleScholarGoogle Scholar |
Collyer, M. L., and Stockwell, C. A. (2004). Experimental evidence for costs of parasitism for a threatened species, White Sands pupfish (Cyprinodon tularosa). Journal of Animal Ecology 73, 821–830.
| Experimental evidence for costs of parasitism for a threatened species, White Sands pupfish (Cyprinodon tularosa).Crossref | GoogleScholarGoogle Scholar |
Gordon, D. M., and Rau, M. E. (1982). Possible evidence for mortality induced by the parasite Apatemon gracilis in a population of brook sticklebacks (Culaea inconstans). Parasitology 84, 41–47.
Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
| MRBAYES: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=573b3c35dde42776a97cee27686fecc4CAS |
Humphries, P. (1983). Aspects of the biology of the dwarf galaxiid, Galaxiella pusilla (Mack) (Salmoniformes: Galaxiidae). B.Sc.(Honours) Thesis, Monash University, Melbourne.
Kuiter, R. H. (2005). More on dwarf galaxias. Fishes of Sahul 19, 160–163.
Locke, S. A., McLaughlin, J. D., Dayanandan, S., and Marcogliese, D. J. (2010). Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. International Journal of Parasitology 40, 333–343.
| Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvFGhtrc%3D&md5=a46b92d75e9b7316e84c78ebf9fd446cCAS |
Lyndon, A. R. (2001). Low intensity infestation with the heartfluke Apatemon gracilis does not affect short-term growth performance in rainbow trout. Bulletin of the European Association of Fish Pathologists 21, 263–265.
Mawson, P. M., Angel, L. M., and Edmonds, S. J. (1986). A checklist of helminths from Australian birds. Records of the South Australian Museum 19, 219–325.
Merck (2005). ‘The Merck Veterinary Manual.’ 9th edn. (Merck and Co Inc.: NJ, USA.)
Morgan, J. A. T., and Blair, D. (1998). Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial COI and NDI genes for distinguishing among Echinostoma species (Trematoda). Parasitology 116, 289–297.
| Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial COI and NDI genes for distinguishing among Echinostoma species (Trematoda).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlajtr0%3D&md5=6f94dd3c51e695d61aba66eb0776cd4bCAS |
Moszczynska, A., Locke, S. A., McLaughlin, J. D., Marcogliese, D. J., and Crease, T. J. (2009). Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, 75–82.
| Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlslOjsbs%3D&md5=ee9fde4ed47a331d5659f8a9304eaf87CAS |
Negm-Eldin, M., and Davies, R. W. (2002). Morphology and life cycle of Apatemon hypseleotris species novum from Australia including metacercariae viability and encystment. Deutsche Tierarztliche Wochenschrift 109, 306–314.
| 1:STN:280:DC%2BD38vgvVantQ%3D%3D&md5=30822ffeaed41137fbc30de3b945f217CAS |
Peakall, R., and Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetics software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GENALEX 6: genetic analysis in Excel. Population genetics software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Posada, D., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=c9ee1adef2331f28d1d5507fcef6a791CAS |
Ronquist, F., and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MRBAYES 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=0c2f748fc03492aa22ecbea263701f2cCAS |
Smith, S. J., and Hickman, J. L. (1983). Two strigeoid trematodes, Apatemon (Apatemon) gracilis (Rudolphi, 1819) and Diplostomum (Dolichorchis) galaxiae n.sp., which encyst in the freshwater fish Galaxias auratus Johnston in Lake Crescent, Tasmania. Papers and Proceedings of the Royal Society of Tasmania 117, 21–39.
Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
| MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrsL8%3D&md5=8c05a6eef65dbcd17583f67c5aecdaf5CAS |
Tort, L., Watson, J. J., and Priede, I. G. (1987). Changes in in vitro heart performance in rainbow trout, Salmo gairdneri Richardson, infected with Apatemon gracilis (Digenea). Journal of Fish Biology 30, 341–347.
| Changes in in vitro heart performance in rainbow trout, Salmo gairdneri Richardson, infected with Apatemon gracilis (Digenea).Crossref | GoogleScholarGoogle Scholar |
Wager, R. (1996). Galaxiella pusilla. The IUCN Red List of Threatened Species 1996: e.T8820A12934389. Available at:
Walsh, P. S., Metzgar, D. A., and Higuschi, R. (1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10, 506–513.
| 1:STN:280:DyaK3MzivFSjtw%3D%3D&md5=fbfe149c94507c4ea1ae8f10cfb7151dCAS |
Zhang, Z., Schwartz, S., Wagner, L., and Miller, W. (2000). A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7, 203–214.
| A greedy algorithm for aligning DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktl2qsrY%3D&md5=0ae958ab5e379c85ea5195fbb7bbbb45CAS |
