Co-infection with Trichodina (Ciliophora: Trichodinidae) and Aeromonas caviae synergistically changes the hematology and histopathology of Asian seabass Lates calcarifer

##plugins.themes.bootstrap3.article.sidebar##

PDF
DOI https://doi.org/10.13057/biodiv/d220834
Issue
Vol. 22 No. 8 (2021)
Section
Articles

##plugins.themes.bootstrap3.article.main##

SUFARDIN ♥
Department of Fisheries, Faculty of Marine Science and Fisheries, Universitas Hasanuddin. Jl Perintis Kemerdekaan Km. 10, Makassar 902425, South Sulawesi, Indonesia
SRIWULAN
Parasite and Fish Disease Laboratory, Faculty of Marine Science and Fisheries, Universitas Hasanuddin. Jl Perintis Kemerdekaan Km. 10, Makassar 902425, South Sulawesi, Indonesia
HILAL ANSHARY
Parasite and Fish Disease Laboratory, Faculty of Marine Science and Fisheries, Universitas Hasanuddin. Jl Perintis Kemerdekaan Km. 10, Makassar 902425, South Sulawesi, Indonesia

Abstract

Abstract. Sufardin, Sriwulan, Anshary H. 2021. Co-infection with Trichodina (Ciliophora: Trichodinidae) and Aeromonas caviae synergistically changes the hematology and histopathology of Asian seabass Lates calcarifer. Biodiversitas 22: 3371-3382. Consequential interaction contributed by parasitic and bacterial infections in fish has received little attention and impact of co-infection is mostly undescribed. This study identifies and describes notable damage arising from the co-infection of Trichodina and Aeromonas caviae infecting the seabass Lates calcarifer. A completely randomized experiment was performed with 4 infection treatments (healthy fish; fish naturally infected with Trichodina sp.; healthy fish injected with A. caviae; fish naturally infected with Trichodina sp. and injected with A. caviae) and 3 replicates. Fish were obtained from the Takalar Brackish Aquaculture Institute, South Sulawesi, Indonesia. The data were statistically tested using linear regression analysis. The results showed bacterial pathogenicity, lymphocyte percentage, and histopathological quantification were statistically different (P < 0.05). Meanwhile, the number of erythrocytes and leukocytes, the percentages of monocytes and neutrophils were not significantly different (P > 0.05) between treatments. The non-infected fish showed no cell inflammation and necrosis, very little hemorrhage (liver and gills), negligible hemorrhage and melano-macrophages (kidney). Kidneys and liver were the most damaged organs of co-infected fish, with a large number of inflammatory cells, hemorrhages, vacuoles, melano-macrophages, scar tissue, inflammation and necrosis. Infection with Trichodina sp. presented less damage than the co-infection of A. caviae and Trichodina sp. In conclusion, single infection showed a mild pathological impact, meanwhile, the co-infection of Trichodina sp and A. caviae contribute significantly to fish’s health.

##plugins.themes.bootstrap3.article.details##

References
Abdel-Latif HMR, Dawood MAO, Menanteau-Ledouble S, El-Matbouli M. 2020. The nature and consequences of co-infections in tilapia: A review. Journal of Fish Disease 14 pp. DOI: 10.1111/jfd.13164
Adel M, Dadar M, Khajavi SH, Pourgholam R, Karimí B, Velisek J. 2017. Hematological, biochemical and histopathological changes in Caspian brown trout (Salmo trutta caspius Kessler, 1877) following exposure to sublethal concentrations of chlorpyrifos. Toxin Reviews 36: 73 - 79.
Alapide-Tendencia EV, de la Pena LD. 2001. Bacterial Diseases. In: Health Management in Aquaculture (G.D.Lio-po, C.R.Lavilla & E.R.Cruz-Lacierda, eds). Aquaculture Department Southeast Asian Fisheries Development Centre, Philippines 25 - 41.
Alejo A, Tafalla C. 2011. Chemokines in teleost fish species. Development and Comparative Immunology 35: 1215 - 1222. DOI: 10.1016/j.dci.2011.03.011.
Amlacher E. 1970. Textbook of fish disease. Publication Nepture City. New Jersey. USA.
Anderson DP. 1974. Fish Immunology. In: Disease of Fishes. Vol. 4. T.F.H. Publication. Inc Ltd. The British Crown Colony of Hongkong.
Anggraini RD, Abdullah AD, Qadar H. 2018. Analisis kesesuaian perairan untuk budidaya ikan kerapu bebek (cromileptes altivelis) di Perairan Pulau Tegal Teluk Lampung. Jurnal Rekayasa dan Teknologi Budidaya Perairan 6 (2): 719 - 728. [Indonesian]
Bandilla M, Valtonen ET, Suomalainen LR, Aphalo PJ, Hakalahti T. 2006. A link between ectoparasite infection and susceptibility to bacterial disease in rainbow trout. International Journal for Parasitology 36 (9): 987 - 991. https://doi.org/10.1016/j.ijpara.2006.05.001
Bowers JM, Mustafa A, Speare DJ, Conboy GA, Brimacombe M, Sims DE, Burka JF 2000. The physiological response of Atlantic salmon, Salmo salar L., to a single experimental challenge with sea lice Lepeophtheirus salmonis. Journal of Fish Disease 23: 165 - 172.
Burgos-Aceves MA, Cohen A, Smith Y, Faggio C. 2018. MicroRNAs and their role on fish oxidative stress during xenobiotic environmental exposures. Ecotoxicololgy and Environmental Safety 148: 995 - 1000.
Busch S, Dalsgaard I, Buchmann K. 2003. Concomitant exposure of rainbow trout fry to Gyrodactylus derjavini and Flavobacterium psychrophilum: effects on infection and mortality of host. Veterinary Parasitology 117: 117 - 122.
Cerezuela R, Guardiola FA, González P, Meseguer J, Esteban MÁ. 2012. Effects of dietary Bacillus subtilis, Tetraselmis chuii, and Phaeodactylum tricornutum, singularly or in combination, on the immune response and disease resistance of sea bream (Sparus aurata L.). Fish and Shellfish Immunology 33: 342 - 349.
Cusack R, Cone D. 1985. A report of bacterial microcolonies on the surface of Gyrodactylus (Monogenea). Journal of Fish Diseases 8 (1): 125 - 127.
Doherty CP. 2007. Host-Pathogen Interactions: The Role of Iron 1-3. The Journal of Nutrition 137: 1341-1344. DOI: 10.3945/ajcn.113.076133
Eissa AE, Zaki MM, Abdel-Aziz A. 2010. Flavobacterium columnare/Myxobolus tilapiae concurrent infection in the earthen pond reared Nile tilapia (Oreochromis niloticus) during the early summer. Interdisciplinary Bio Central 2 (2): 5.1 - 5.9.
Espinosa C., Esteban, M.A., Cuesta, A. 2019. Dietary administration of PVC and PE microplastics produces histological damage, oxidative stress and immunoregulation in European seabass (Dicentrarchus labrax L.) Fish and Shellfish Immunology. DOI: https://doi.org/10.1016/j.fsi.2019.10.072
Evans J, Klesius P, Pasnik D, Shoemaker C. 2007. Influence of natural Trichodina sp. parasitism on experimental Streptococcus iniae or Streptococcus agalactiae infection and survival of young channel catfish Ictalurus punctatus (Rafinesque). Aquaculture Research 38 (6): 664 - 667.
Figueroa C, Bustos P, Torrealba D, Dixon B, Soto C, Conejeros P, Gallardo JA. 2017. Coinfection takes its toll: sea lice override the protective effects of vaccination against a bacterial pathogen in Atlantic salmon. Scientific Reports 7: 17817
Forouhar VM, Mohamadi YA, Hedayati A, Faggio C. 2018. Histopathological lesions and toxicity in common carp (Cyprinus carpio L. 1758) induced by copper nanoparticles. Microscopy Research and Technique 81: 724 - 729.
Fujaya Y. 2002. Fisiologi Ikan. Direktorat Jenderal Pendidikan Nasional, Makasar. [Indonesian]
Goda AMAS, Ahmed SR, Nazmi HM, Aboseif A, Taha MKS, Fadda SH, Baromh MZ, El-Haroun E, Davies S. 2020. Assessment of a high protein distillers dried grain (HP-DDG) augmented with phytase in diets for European seabass, Dicentrarchus labrax fingerlings on growth performance, hematological status, immune response and related gut and liver histology. Aquaculture. https://doi.org/10.1016/j.aquaculture.2020.735617
Guttman JA, Finlay BB. 2009. Biochimica et Biophysica Acta Tight junctions as targets of infectious agents. (BBA) – Biomembranes 1788: 832–841. DOI: 10.1016/j.bbamem.2008.10.028
Howell K, de Leeuw E. 2018. Cell adhesion properties of human defensins, Biochemical and Biophysical Research Communications 502: 238 - 242. DOI: 10.1016/J.BBRC.2018.05.150
Hu Y, Zhao Y, Tang F. 2005. Redescription and new distribution of Trichodinids hyperparasitis. Chinese Journal of Zoology 40: 91 - 91.
Ibraheem AS, Önalan S, Arabaci M. 2017. Investigation of zoonotic disease pathogens (Aeromonas hydrophila, Pseudomonas fluorescens, Streptococcus iniae) seen in carp farms in the Northern Iraq-Erbil region by molecular methods. International Conference on Advances in Natural and Applied Sciences, AIP Conference Proceedings. 1833 (1): 020077-1 - 020077-7. DOI: 10.1063/1.4981725
Irmawati, Umar MT, Husain AAA, Malina AC, Kadir NN, Alimuddin. 2020. Distribution and character of Asian seabass (Lates calcarifer Bloch, 1970) in South Sulawesi. IOP conference series: earth and environmental science 564: 9 pp.
Kathirkaman P, Ayyaru G, Serelathan MV, Singaravel V, Gunasekaran T. 2018. Innate immunological responses of Asian seabass, Lates calcarifer (Bloch, 1790) for experimentally challenged Aeromonas hydrophila infection. Comparative Clinical Pathology. 5 pp. https://doi.org/10.1007/s00580-018-2683-8
Khan RA. 2004. Disease outbreaks and mass mortality in cultured atlantic cod, Gadus morhua L., associated with Trichodina murmanica (Chiliophora). Journal of Fish Disease 27: 181 - 184
Kresno SB. 2001. Imunologi: Diagnosis dan Prosedur Laboratorium. Edisi Ketiga. Fakultas Kedokteran. Universitas Indonesia. Jakarta. 437 Halaman. [Indonesian]
Lhorente JP, Gallardo JA, Villanueva B, Caraba?o MJ, Neira R. 2014. Disease resistance in Atlantic Salmon (Salmo salar): coinfection of the intracellular bacterial pathogen Piscirickettsia salmonis and the sea louse Caligus rogercresseyi. PLoS One 9 (4): e95397. DOI: 10.1371/journal.pone.0095397
Li J, Ni XD, Liu YJ, Lu CP. 2011. Detection of three virulence genes alt, ahp and aerA in Aeromonas hydrophila and their relationship with actual virulence to zebrafish. Journal of Applied Microbiology 110: 823 - 830.
Lom J. 1995. Trichodinid ciliates (Peritrichida: Urceolariidae) from some marine fishes. Folia Parasitologica 17: 113 - 125.
Magnadottir B. 2010. Immunological control of fish diseases. Marine Biotechnology 12: 361 - 379.
Maharajan A, Rufus KM, Paruruckumani PS, Ganapirya V. 2016. Histopathology biomarker responses in Asian seabass, Lates calcarifer (Bloch) exposed to copper. The Journal of Basic & Applied Zoology 77: 21 - 30.
Mangunwardoyo W, Ismayasari R, Riany E. 2010. Uji patogenisitas dan virulensi Aeromonas hydrophila stanier pada ikan nila (Oreochromis niloticus lin.) melalui postulat Koch. Jurnal Riset Akuakultur 5 (2): 245 - 255. [Indonesian]
Moustafa EM, Dawood MAO, Assar DH, Omara AA, Elbialy ZI, Farrag FA, Shukry M, Zayed MM. 2020. Modulatory effects of fenugreek seeds powder on the histopathology, oxidative status, and immune related gene expression in Nile tilapia (Oreochromis niloticus) infected with Aeromonas hydrophila. Aquaculture 515: 12 pp. https://doi.org/10.1016/ j.aquaculture. 2019.734589
Mulia DS. 2003. Pengaruh Vaksin Debris Sel Aeromonas hydrophila Dengan Kombinasi Cara Vaksinasi dan Booster terhadap Respon Imun dan Tingkat Perlindungan Relatif pada Lele Dumbo (Clarias gariepinus Burchell). [Thesis]. Sekolah pascasarjana, Universitas Gadjah Mada, Yogyakarta. [Indonesian]
Nuria MC, Astutu EP, Sumantri. 2010. Antibacterial Activities of Ethyl Acetate Fraction of Methanol Extract From Sosor Bebek Leaves (Kalanchoe pinnata Pers.). Mediagro 6 (2): 51 - 61. [Indonesian]
Plumb JA. 1997. Infectious diseases of tilapia. In: Tilapia aquaculture in the Americas (ed by B.A. Costa-Pierce & J.E. Rakocy), World Aquaculture Society, Bataon Rouge, Louisiana. pp 212 - 228.
Sarono A, Nitimulyo KH, Leluno IYB, Widodo, Thaib N, Haryani EBS, Haryanto S, Triyanto, Ustadi, Kusumahati AN, Novianti, Setianingsih SW. 1993. Hama dan Penyakit Ikan Karantina Golongan Bakteri. Kerjasama Pusat Karantina Pertanian dan Fakultas Pertanian Jurusan Perikanan, Universitas Gajah Mada. Yogyakarta. [Indonesian]
Scott SJ, Bollinger TK. 2014. Flavobacterium columnare: an important contributing factor to fish die-off in southern lakes of Saskatchewan, Canada. Journal of Veterinary Diagnostic Investigation 26: 832 - 836.
Shoemaker CA, Xu D, Klesius PH, Evans JJ. 2008. Concurrent infections (Parasitism and bacterial disease) in Tilapia. Paper presented at the Proceedings of the 8th International Symposium on Tilapia in Aquaculture Cairo, Egypt.
Steinel NC, Bolnick DI. 2017. Melanomacrophage centers as a histological indicator of immune function in fish and other poikilotherms. Frontiers in Immunology 8: 827 - 827.
Sufardin, Sriwulan, Anshary H. 2021. Bacteria associated with Trichodina sp. infection of barramundi, Lates calcarifer in a fish farm in South Sulawesi, Indonesia. AACL Bioflux 14 (1): 643 - 654.
Supriyadi H, Mangunwiryo H, Maryono, Effendi J. 1995. Pencegahan penyakit bakterial pada ikan gurame dengan cara vaksinasi. Jurnal Penelitian Perikanan Indonesia 1 (4): 28 - 35. [Indonesian]
Surat keputusan badan karantina ikan pengendalian mutu dan keamanan hasil perikanan. 2015. Petunjuk teknis pemantauan Hama dan penyakit ikan karantina. badan karantina ikan pengendalian mutu dan keamanan hasil perikanan. Jakarta. [Indonesian]
Tang FH, Zhao YJ, Tang AK. 2005. Presence of ectoparasitic trichodinids (Ciliophora, Oligohymeno-phorea, Peritrichida) on the gills of cultured freshwater fish, Carassius auratus in Chongqing, China, with the description of a new species of the genus Trichodina. Acta Zootaxa Sinica 30 (1): 35 - 40.
Tang HG, Wu TX, Zhao ZY, Pan XD. 2008. Effects of fish protein hydrolysate on growth performance and humoral immune response in large yellow croaker Pseudosciaena crocea R. Journal of Zhejiang University Science B 9 (9): 684 - 690.
Tizard I. 1982. Veterinary Immunology, An Introduction. Ed Ke-3. W,B. Saunders Company, Canada.
Tkachenko H, Kurhaluk N, Andriichuk A, Gasiuk E, Beschasniu S. 2014. Oxidative stress biomarkers in liver of sea trout (Salmo trutta m. trutta L.) affected by ulcerative dermal necrosis syndrome. Turkish Journal of Fisheries and Aquatic Science 14: 391 - 402.
Umasugi S, Burhanuddin A. 2015. Analisis Prevalensi dan Intensitas Ektoparasit Ikan Kerapu Tikus (Cromileptes altevalis) di Keramba Jaring Apung Perairan Teluk Kayeli Kabupaten Buru. Jurnal Ilmiah Agribisnis dan Perikanan 8 (1): 20 halaman. DOI: 10.29239/j.agrikan.8.1.13-20. [Indonesian]
Urawa S. 1992. Trichodina truttae Muller, 1937 (Ciliophora: Peritrichida) on juvenile chum salmon (Oncorhynichus keta): pathogenicity and host-parasite interaction. Fish pathology 27: 29 - 37.
Vallejos-Vidal E, Reyes-López F, Teles M, MacKenzie S. 2016. The response of fish to immunostimulant diets. Fish and Shellfish Immunology 56: 34 - 69.
Vasemägi A, Visse M, Kisand V. 2017. Effect of Environmental Factors and an Emerging Parasitic Disease on Gut Microbiome of Wild Salmonid Fish. American society for Microbiology, mSphere 2 (6): e00418-17. https://doi.org/10.1128/mSphere.00418-17.
Wedemeyer GA, Yasutake WT. 1977. Clinical methods for the assessment of the effect environment stress on the fish health. Technical Papers of the US Fish and Wildlife Service. U.S. Department of the Interior Fish and Wildlife Service 89: 1 - 17.
Williams EH, Bunkley LW. 1996. Parasites off shore big game fishes of Puerto Rico and the Western Atlantic. Puerto Rico. Department of Natural Environmental Resources and University of Puerto Rico, Rio Piedras.
Xu DH, Shoemaker CA, LaFrentz BR. 2014. Enhanced susceptibility of hybrid tilapia to Flavobacterium columnare after parasitism by Ichthyophthirius multifiliis. Aquaculture 430: 44 - 49.
Xu DH, Shoemaker CA, Martins ML, Pridgeon JW, Klesius PH. 2012. Enhanced susceptibility of channel catfish to the bacterium Edwardsiella ictaluri after parasitism by Ichthyophthirius multiiliis. Veterinary Microbiology 158: 216 - 219.
Yakin MA, Limin S, Suryadi S. 2018. Pengaruh pemberian pakan dengan kadar protein berbeda terhadap performa pertumbuhan ikan kakap putih (Lates calacrifer) di Keramba Jaring Apung. Jurnal Sains Teknologi Akuakultur 2 (1): 12 - 19. [Indonesian]
Yang Y, Yu H, Li H, Wang A. 2016. Transcriptome profiling of grass carp (Ctenopharyngodon idellus) infected with Aeromonas hydrophila, Fish and Shellfish Immunololgy 51: 329 - 336. DOI: 10.1016/j.fsi.2016.02.035
Zafran, Harada T, Koesharyani, Yuasa K, Hatai K. 1998. Indonesian hatchery reared seabass larvae (Lates calcarifer), associated with viral nervous necrosis (VNN). IFR Journal 4 (1): 19 - 22.
Zafran, Rosa D, Mahardika K. 2019. Prevalensi ektoparasit pada ikan budidaya di karamba jaring apung di teluk kaping, buleleng, Bali. Journal of Fisheries and Marine Research 3 (1): 32 - 40. [Indonesian]
Zapata A, Diez B, Cejalvo T, Gutiérrez-de Frías C, Cortés A. 2006. Ontogeny of the immune system of fish. Fish and Shellfish Immunology 20: 126 - 136.
Zhang X, Shen Y, Xu X, Zhang M, Bai Y, Miao Y, Fang Y, Zhang J, Wang R, Li J. 2018. Transcriptome analysis and histopathology of black carp (Mylopharyngodon piceus) spleen infected by Aeromonas hydrophila. Fish and Shellfish Immunology. DOI: 10.1016/j.fsi.2018.09.047