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Effect of environmental factors on survival and population growth of ciliated parasite, Mesanophrys sp. (Ciliophora: Scuticociliatia) infecting Portunus trituberculatus

Published online by Cambridge University Press:  04 November 2020

Summia Perveen ,
Yuhua Lei ,
Fei Yin Open the ORCID record for Fei Yin [Opens in a new window]  and
Chunlin Wang
Summia Perveen
Affiliation:
Key Laboratory of Applied Marine Biotechnology, Ministry of Education; Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture; School of Marine Sciences, Ningbo University, 818 Fenghua Road, Ningbo315211, P. R. China
Yuhua Lei
Affiliation:
Key Laboratory of Applied Marine Biotechnology, Ministry of Education; Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture; School of Marine Sciences, Ningbo University, 818 Fenghua Road, Ningbo315211, P. R. China
Fei Yin*
Affiliation:
Key Laboratory of Applied Marine Biotechnology, Ministry of Education; Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture; School of Marine Sciences, Ningbo University, 818 Fenghua Road, Ningbo315211, P. R. China
Chunlin Wang
Affiliation:
Key Laboratory of Applied Marine Biotechnology, Ministry of Education; Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture; School of Marine Sciences, Ningbo University, 818 Fenghua Road, Ningbo315211, P. R. China
*
Author for correspondence: Fei Yin, E-mail: Yinfei@nbu.edu.cn; Chunlin Wang, E-mail: Wangchunlin@nbu.edu.cn
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Abstract

Mesanophrys sp. is a newly identified parasitic ciliate infecting farmed swimming crab. To demonstrate the correlation between parasite development and environmental conditions, this study aimed to investigate the effect of temperature, salinity, pH and frequency of passage of parasite on survival, growth and body size of Mesanophrys sp. in vitro. The results revealed that survival, population density and growth rate of the parasite were highest at 12°C and decreased with increasing temperature from 16 to 26°C. In addition, the survival, population density and growth rate of Mesanophrys sp. were high at 20‰. When salinity was adjusted to levels lower (0–10‰) and higher (40–60‰) than 20‰, the parasite's survival and growth rate gradually declined. The optimal pH for parasite survival was 8.0, whereas its survival was inhibited at <4.5 or >9.5. Our result also showed that parasite body proportions (length:width) were significantly smaller at the highest temperature compared to the lower temperature, whereas different salinities had no significant effect. Furthermore, we introduced dynamic parasite culture systems in vitro where Mesanophrys sp. was cultured in medium-containing culture plates through continually reducing and halving the old medium into fresh. Application of this optimized dilution timing technique with fresh medium and sub-cultured enabled a continuous culture of parasites. Under this optimized condition, the highest population density and exponential growth rate of the parasite were achieved than that of a control group. This study will help to understand the ciliated parasite infection dynamics and provides new possibilities for in vitro parasite-associated studies.

Keywords

Mesanophrys sp.pHpopulation growthsalinityscuticociliatessurvivaltemperature
Type
Research Article
Information
Parasitology , Volume 148 , Issue 4 , April 2021 , pp. 477 - 485
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press.

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Footnotes

*

The authors contributed equally to this work.

References

Armstrong, DA, Burreson, EM and Sparks, AK (1981) A ciliate infection (Paranophrys sp.) in laboratory-held Dungeness crabs, Cancer magister. Journal of Invertebrate Pathology 37, 201–209.CrossRefGoogle Scholar
Arzul, I, Gagnaire, B, Bond, C, Bruno, C, Morga, B, Ferrand, S and Renault, T (2009) Effects of temperature and salinity on the survival of Bonamia ostreae, a parasite infecting flat oysters Ostrea edulis. Diseases of Aquatic Organisms 85, 67–75.CrossRefGoogle ScholarPubMed
Audemard, C, Carnegie, RB, Bishop, MJ, Peterson, CH and Burreson, EM (2008) Interacting effects of temperature and salinity on Bonamia sp. parasitism in the Asian oyster Crassostrea ariakensis. Journal of Invertebrate Pathology 98, 344–350.CrossRefGoogle ScholarPubMed
Auzoux-Bordenave, S (1995) In vitro sporulation of the clam pathogen Perkinsus atlanticus (Apicomplexa, Perkinsea) under various environmental conditions. Journal of Shellfish Research 14, 469–475.Google Scholar
Bodinier, C, Lorin-Nebel, C, Charmantier, G and Boulo, V (2009) Influence of salinity on the localization and expression of the CFTR chloride channel in the ionocytes of juvenile Dicentrarchus labrax exposed to seawater and freshwater. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 153, 345–351.CrossRefGoogle ScholarPubMed
Briffa, M, Bridger, D and Biro, PA (2013) How does temperature affect behavior. Multilevel analysis of plasticity, personality, and predictability in hermit crabs. Animal Behaviour 86, 47–57.CrossRefGoogle Scholar
Byrne, M, Cerra, A, Nishigaki, T and Hoshi, M (1997) Infestation of the testes of the Japanese sea star Asterias amurensis by the ciliate Orchitophyra stellarum: a caution against the use of this ciliate for biological control. Diseases of Aquatic Organism 28, 235–239.CrossRefGoogle Scholar
Cáceres-Martínez, J, Ortega, MG, Vásquez-Yeomans, R, García, TDJP, Stokes, NA and Carnegie, RB (2012) Natural and cultured populations of the mangrove oyster Saccostrea palmula from Sinaloa, Mexico, infected by Perkinsus marinus. Journal of Invertebrate Pathology 110, 321–325.CrossRefGoogle ScholarPubMed
Carnegie, RB, Stokes, NA, Audemard, C, Bishop, MJ, Wilbur, AE, Alphin, TD and Burreson, EM (2008) Strong seasonality of Bonamia sp. infection and induced Crassostrea ariakensis mortality in Bogue and Masonboro Sounds, North Carolina, USA. Journal of Invertebrate Pathology 98, 335–343.CrossRefGoogle ScholarPubMed
Cawthorn, RJ (1997) Overview of ‘bumper car’ disease – impact on the North American lobster fishery. International Journal for Parasitology 27, 167–172.CrossRefGoogle Scholar
Cheng, SH, Kâ, S, Kumar, R, Kuo, CS and Hwang, JS (2011) Effects of salinity, food level, and the presence of microcrustacean zooplankters on the population dynamics of rotifer Brachionus rotundiformis. Hydrobiologia 666, 289–299.CrossRefGoogle Scholar
Culloty, SC and Mulcahy, MF (1996) Season-, age-, and sex-related variation in the prevalence of bonamiasis in flat oysters (Ostrea edulis L.) on the south coast of Ireland. Aquaculture 144, 53–63.CrossRefGoogle Scholar
Deveney, M, Bayly, T, Johnston, C and Nowak, BF (2005) A parasite survey of farmed Southern bluefin tuna, Thunnus maccoyii (Castelnau). Journal of Fish Diseases 28, 279–284.CrossRefGoogle Scholar
Dumont, H, Sarma, SSS and Ali, A (2006) Laboratory studies on the population dynamics of Anuraeopsis fissa (Rotifera) in relation to food density. Freshwater Biology 33, 39–46.CrossRefGoogle Scholar
Edgerton, B, O'Donoughe, P, Wingfield, M and Owens, L (1996) Systemic infection of freshwater crayfish Cherax quadricarinatus by hymenostome ciliates of the Tetrahymena pyriformis complex. Diseases of Aquatic Organisms 27, 123–129.CrossRefGoogle Scholar
Fenchel, T (1968) The ecology of marine microbenthos III. The reproductive potential of ciliates. Ophelia 5, 123–136.CrossRefGoogle Scholar
Gómez-Gutiérrez, J, Peterson, WT, De Robertis, A and Brodeur, RD (2003) Mass mortality of krill caused by parasitoid ciliates. Science (New York, N.Y.) 301, 339.CrossRefGoogle ScholarPubMed
González, L and Carvajal, J (2003) Life cycle of Caligus rogercresseyi (Copepoda: Caligidae) parasite of Chilean reared salmonids. Aquaculture 220, 101–117.CrossRefGoogle Scholar
Goosen, N, Horemans, A, Hillebrand, S, Stumm, C and Vogels, G (1988) Cultivation of the sapropelic ciliate Plagiopyla nasuta Stein and isolation of the endosymbiont Methanobacterium formicicum. Archives of Microbiology 150, 165–170CrossRefGoogle Scholar
Harikrishnan, R, Balasundaram, C and Heo, MS (2010) Scuticociliatosis and its recent prophylactic measures in aquaculture with special reference to South Korea: taxonomy, diversity, and diagnosis of scuticociliatosis: Part I Control strategies of scuticociliatosis: Part II. Fish & Shellfish Immunology 29, 15–31.CrossRefGoogle ScholarPubMed
Heuch, PA, Knutsen, J, Knutsen, H and Schram, TA (2002) Salinity and temperature effects on sea lice over-wintering on sea trout (Salmo trutta) in coastal areas of the Skagerrak. Journal of the Marine Biological Association of the UK 82, 887–892.CrossRefGoogle Scholar
Heydarnejad, MS (2008) Survival of Paramecium caudatum at various pH values and under normoxic and hypoxic conditions. Pakistan Journal of Biological Sciences 11, 392–397.CrossRefGoogle ScholarPubMed
Iglesias, R, Paramá, A, Alvarez, M, Leiro, J, Fernández, J and Sanmartín Durán, M (2001) Philasterides dicentrarchi (Ciliophora, Scuticocilatida) as the causative agent of scuticociliatosis in farmed turbot Scophthalmus maximus in Galicia (NW Spain). Diseases of Aquatic Organisms 46, 47–55.CrossRefGoogle Scholar
Julia, AL, Clinton, BC, Ingo, E and Ian, DW (2007) Effect of water temperature on reproductive development of Benedenia seriolae (Monogenea: Capsalidae) from Seriola lalandi in Australia. Diseases of Aquatic Organisms 74, 235–242.Google Scholar
Karatayev, AY, Mastitsky, SE, Burlakova, LE, Molloy, DP and Vezhnovets, GG (2003) Seasonal dynamics of endosymbiotic ciliates and nematodes in Dreissena polymorpha. Journal of Invertebrate Pathology 83, 73–82.CrossRefGoogle ScholarPubMed
Kim, WS, Yoon, S-J, Kim, JM, Gil, JW and Lee, TW (2005) Effects of temperature changes on the endogenous rhythm of oxygen consumption in the Japanese flounder Paralichthys olivaceus. Fisheries Science 71, 471–478.CrossRefGoogle Scholar
Liu, X, Lei, Y, Ren, Z, Zhou, S, Qian, D, Yu, Y, Yin F and Wang, C (2020) Isolation, characterization and virulence of Mesanophrys sp. (Ciliophora: Orchitophryidae) in farmed swimming crab (Portunus trituberculatus) in eastern China. Journal of Fish Diseases 43, 1419–1429.CrossRefGoogle Scholar
Marcogliese, D (2001) Implication of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology-revue Canadienne De Zoologie 79, 1331–1352.CrossRefGoogle Scholar
Massana, Ramon, Stumm, Claudius K and Pedrós-Alió, Carlos (1994) Effects of Temperature, Sulfide, and Food Abundance on Growth and Feeding of Anaerobic Ciliates. Applied and Environmental Microbiology 60, 1317–1324. http://dx.doi.org/10.1128/AEM.60.4.1317-1324.1994CrossRefGoogle ScholarPubMed
Miller, DD and Marcus, NH (1994) The effects of salinity and temperature on the density and sinking velocity of eggs of the calanoid copepod Acartia tonsa Dana. Journal of Experimental Marine Biology and Ecology 179, 235–252.CrossRefGoogle Scholar
Mitchell, S, Rogers, E, Little, T and Read, A (2005) Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution; International Journal of Organic Evolution 59, 70–80.CrossRefGoogle ScholarPubMed
Möller, H (1978) The effect of salinity and temperature on the development and survival of fish parasites. Journal of Fish Biology 12, 311–323.CrossRefGoogle Scholar
Morado, JF and Small, EB (1994) Morphology and stomatogenesis of Mesanophrys pugettensis n. sp. (Scuticociliatida: Orchitophryidae), a facultative parasitic ciliate of the Dungeness crab, Cancer Magister (Crustacea: Decapoda). Transactions of the American Microscopical Society 113, 343–364.CrossRefGoogle Scholar
Morado, JF and Small, EB (1995) Ciliate parasites and related diseases of Crustacea: a review. Reviews in Fisheries Science 3, 275–354.CrossRefGoogle Scholar
Müller, H and Geller, W (1993) Maximum growth rates of aquatic ciliate protozoa: the dependence on body size and temperature reconsidered. Archiv fur Hydrobiologie 126, 315–327.Google Scholar
Nasirudeen, AMA, Tan, KSW, Singh, M and Yap, EH (2001) Programmed cell death in a human intestinal parasite, Blastocystis hominis. Parasitology 123, 235–246.CrossRefGoogle Scholar
Oliver, L, Fisher, W, Ford, S, Calvo, L, Burreson, E, Sutton, E and Gandy, JA (1998) Perkinsus marinus tissue distribution and seasonal variation in oysters Crassostrea virginica from Florida, Virginia and New York. Diseases of Aquatic Organisms 34, 51–61.CrossRefGoogle ScholarPubMed
Oltra, R and Todolf, R (1997) Effects of temperature, salinity, and food level on the life-history traits of the marine rotifer Synchaera Cecilia valentina, n. subsp. Journal of Plankton Research 19, 693–702.CrossRefGoogle Scholar
Paquin, P, Santore, R, Wu, K, Kavvadas, C and Toro, D (2000) The biotic ligand model: a model of the acute toxicity of metals to aquatic life. Environmental Science and Policy 3, 175–182.CrossRefGoogle Scholar
Péqueux, A (1995) Osmotic regulation in crustaceans. Journal of Crustacean Biology 15, 1–60.CrossRefGoogle Scholar
Perrigault, M, Buggé, DM and Allam, B (2010) Effect of environmental factors on survival and growth of quahog Parasite Unknown (QPX) in vitro. Journal of Invertebrate Pathology 104, 83–89.CrossRefGoogle ScholarPubMed
Queiroga, FR, Marques-Santos, LF, De Medeiros, IA and Da Silva, PM (2016) Effects of salinity and temperature on in vitro cell cycle and proliferation of Perkinsus marinus from Brazil. Parasitology 143, 475–487.CrossRefGoogle ScholarPubMed
Sarma, SSS, Elguea-Sánchez, B and Nandini, S (2002) Effect of salinity on competition between the rotifers Brachionus rotundiformis Tschugunoff and Hexarthra jenkinae (De Beauchamp) (Rotifera). Hydrobiologia 474, 183–188.CrossRefGoogle Scholar
Small, HJ, Neil, DM, Taylor, AC, Bateman, K and Coombs, GH (2005) A parasitic scuticociliate infection in the Norway lobster (Nephrops norvegicus). Journal of Invertebrate Pathology 90, 108–117.CrossRefGoogle Scholar
Stickle, W, Kozloff, E and Story, S (2007) Physiology of the ciliate Orchitophrya stellarum and its experimental infection of Leptasterias spp. Canadian Journal of Zoology 85, 201–206.CrossRefGoogle Scholar
Thieltges, D, Dolch, T, Krakau, M and Poulin, R (2010) Salinity gradient shapes distance decay of similarity among parasite communities in three marine fishes. Journal of Fish Biology 76, 1806–1814.CrossRefGoogle ScholarPubMed
Thomas, MB and Blanford, S (2003) Thermal biology in insect-parasite interactions. Trends in Ecology and Evolution 18, 344–350.CrossRefGoogle Scholar
Umeda, K, Shimokawa, J and Yoshinaga, T (2013) Effects of temperature and salinity on the in vitro proliferation of trophozoites and the development of zoosporangia in Perkinsus olseni and P. honshuensis, both infecting Manila clam. Fish Pathology 48, 13–16.CrossRefGoogle Scholar
Umeda, K, Yang, X, Waki, T, Yoshinaga, T and Itoh, N (2020) The effects of environmental and nutritional conditions on the development of Perkinsus olseni prezoosporangia. Experimental Parasitology 209, 107827.CrossRefGoogle ScholarPubMed
van Banning, P (1991) Observations on bonamiasis in the stock of the European flat oyster, Ostrea edulis, in the Netherlands, with special reference to the recent developments in Lake Grevelingen. Aquaculture 93, 205–211.CrossRefGoogle Scholar
Wiąckowski, K, Hryniewiecka-Szyfter, Z and Babula, A (1999) How many species are in the genus Mesanophrys (Protista, ciliophora, facultative parasites of marine crustaceans). European Journal of Protistology 35, 379–389.CrossRefGoogle Scholar
Xie, Xi, Zhao, Wen and Yang, Miao (2013) Combined influence of water temperature, salinity and body size on energy budget in the sea cucumber Apostichopus japonicus Selenka. Fisheries Science 79, 639–646. http://dx.doi.org/10.1007/s12562-013-0627-4CrossRefGoogle Scholar
Yu, Y, Liu, X, Lei, Y, Zhou, S, Jin, S, Qian, D, Xie, X, Yin, F and Wang, C (2020) Anti-parasitic effects and toxicity of formalin on the parasite Mesanophrys sp. of the swimming crab Portunus trituberculatus. Experimental Parasitology 12, 107886.CrossRefGoogle Scholar
Zander, C (1998) Ecology of host parasite relationships in the Baltic Sea. Die Naturwissenschaften 85, 426–436.CrossRefGoogle ScholarPubMed
Zhang, S and Song, W (2000) Experimental ecology studies on the marine ciliate Paranophrys magna II: the effect of temperature and salinity on the population growth. Chinese Journal of Applied and Environmental Biology 6, 227–231.Google Scholar
Zhang, S, Ma, H and Song, W (2001) Experimental ecology studies on the marine ciliate Paranophrys magna III: the effect of pH on the population growth. Chinese Journal of Applied and Environmental Biology 7, 244–247.Google Scholar
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