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Experimental Infection Model with the Bivalvulid Enteromyxum Leei

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Experimental Infection Model with the Bivalvulid Enteromyxum Leei Institute of Parasitology, Biology Centre CAS Folia Parasitologica 2020, 67: 024 doi: 10.14411/fp.2020.024 http://folia.paru.cas.cz Research Article Experimental infection model with the bivalvulid Enteromyxum leei (Myxidiidae) in the sharpsnout seabream, Diplodus puntazzo (Sparidae), and evaluation of the antiparasitic efficacy of a functional diet Morgane A. Henry1, Fotini Kokou1,2, Oswaldo Palenzuela3, George Pyrenis1 and George Rigos1 1 Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Anavissos, Attiki, Greece; 2 Aquaculture and Fisheries Group, Wageningen Institute of Animal Sciences, Wageningen University, Wageningen, The Netherlands; 3 Institute of Aquaculture Torre de la Sal (IATS-CSIC), Castellón, Spain. Abstract: An infection model for sharpsnout seabream Diplodus puntazzo (Walbaum) challenged with the myxosporean Enteromyxum leei (Diamant, Lom et Dyková, 1994), resembling the natural infection conditions, was used to evaluate the antiparasitic efficacy of a functional diet. Fish of an average weight of 12.5 ± 1.2 g were delivered either a functional (included as feed supplement at 0.3% levels) or a control extruded diet. After four weeks of administration of the experimental diets, fish were challenged with the parasites (cohabitation with infected donors; donor: recipient ratio 1 : 1). The experiment was terminated four weeks after the start of the chal- lenge. At the end of the experiment, growth and feeding (specific growth rate and feed efficiency), as well as immunological parameters (respiratory burst activity, antibacterial activities, hemoglobin concentration, anti-protease activity and ceruloplasmin activity) were measured along with cumulative mortality and total parasitic count in the gut. No significant difference was evident with regard to growth and feeding performance, mortality, gut parasitic load or immunological parameters as the parasitical challenge significantly affected both the performance of the control and functional diet fed fish. However, there was a less prominent impact on antibacterial, anti-protease and ceruloplasmin activity in fish fed with the functional diet. Overall, the present study validated the experimental co- habitation infection model and evaluated the efficacy of a functional ingredient as an antiparasitic agent, showing some potential effects on the fish immune response. Keywords: Cohabitation parasitical challenge, Myxosporea, immune response, hemoglobin, inflammation, gut parasite, parasite intensity, parasite prevalence, qPCR. The farming of sharpsnout seabream, Diplodus pun- varez-Pellitero et al. 2008, Sitjà-Bobadilla and Palenzuela tazzo (Walbaum), was considered quite promising in its 2011). The disease courses faster and with higher mortality first attempts in the 1990s and early 2000s because of a when water temperatures are high (Palenzuela 2006, Alva- fast growth and a high market value (Favaloro et al. 2002, rez-Pellitero et al. 2008, Sánchez-García et al. 2014). Favaloro and Mazzola 2003, Hernández et al. 2008). De- Enteromyxum leei, as most species of Enteromyxum spite the successful early stage rearing of this species, it Palenzuela, Redondo et Álvarez-Pellitero, 2002, is directly has been abandoned in most aquaculture enterprises in the transmitted by fish-to-fish contact favouring the propaga- Mediterranean due to enteromyxosis, a disease caused by tion of the parasite in intense farming conditions. Fish can the myxozoan parasite Enteromyxum leei (Diamant, Lom be infected through exposure to a contaminated water, by et Dyková, 1994) (syn. Myxidium leei) (Diamant et al. cohabitation with infected fish or by ingestion of pre-sporo- 1994, Le Breton and Marques 1995, Diamant 1997, Rigos gonic developmental stages (Diamant 1997). Specifically, et al. 1999, Athanasopoulou et al. 2001, Golomazou et al. in enteromyxosis, trophozoites of E. leei are responsible 2006). for the parasite proliferation in the host, by invading new This parasite is responsible of serious epizootic out- intestinal areas but also for the transmission to healthy fish breaks with severe catarrhal enteritis, which usually causes when they are released from faecal products of infected high fish mortality under extreme cachectic conditions few individuals (Cuadrado et al. 2010). weeks after introduction to the on-growing net cages (Al- Address for correspondence: Morgane A. Henry, Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, 46.7 km Athens – Sounio Ave, 19013 Anavissos, Attiki, Greece. Phone: +30 229 10 76 493; Fax: +30 229 10 76 323; E-mail: [email protected] This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. doi: 10.14411/fp.2020.024 Henry et al.: Functional diet against enteromyxosis in sharpsnout seabream 16 * 12000 c ) l b d b / 14 g ( 10000 n o 12 bc i t a r 8000 t 10 n * e c a n 8 Control 6000 ontrol o a c ab Functional unctional n i 6 b 4000 a o l g 4 o m 2000 e 2 H heliminescence activity heliminescence activity (R) 0 0 0W 4W 0W 4W Fig.Figure 2. Chemiluminescence 2. Chemiluminescence activity activity (Relative (Relative Luminescent Luminescent Units) in the whole Units) Fig. 1. Hemoglobin concentration (g/dl blood) in the fresh blood blood of fish fed control or functional diets for 4 weeks before (0W) and 4 weeks of fish fed control or functional diets for 4 weeks before (0W) and in the(4W) whole after the blood parasitical of fish challenge fed bycontrol cohabitation. or functional Bars represent diets mean for ± 4 S.E.weeks 4 weeks (4W) after the parasitical challenge by cohabitation. Bars beforeDifferent (0W) letters and represent 4 weeks a significant (4W) difference after the between parasitical treatments challenge of the log10- by represent mean ± S.E. Different letters represent a significant dif- cohabitation.transformed data Bars (One represent-Way ANOVA, mean P=0.001). ± S.E. The Different asterisk shows letters a significant represent -16 difference of the transform data between the 2 sampling times (General Linear ference between treatments (One-Way ANOVA, P = 3.5 × 10 ). a significantMethod, P=0.0003). difference Sample size, between n=15 at 0W; treatments n=42 at 4W. of the log10-transformed The asterisk shows a significant difference between the 2 sam- data (One-Way ANOVA, P = 0.001). The asterisk shows a signif- pling times (General Linear Method, P = 1.9 × 10-7). Sample size, icant difference of the transform data between the two sampling n = 15 at 0W; n = 42 at 4W. times (General Linear Method, P = 0.0003). Sample size, n = 15 at 0W; n = 42 at 4W. There are currently no prescription medicines effective Peloponnesus) to the indoor facilities of the Hellenic Centre for against this parasite and most attempts to control it in the Marine Research (HCMR) in Athens, Greece. Maintenance of field and/or in experimental trials have failed (Sitjà-Boba- sharpsnout seabream in land tanks ensures the avoidance of in- dilla et al. 2008, Sánchez-García et al. 2014). However, fection with Enteromyxum leei, which is inevitably initiated when empirical evidence in the farms and recent laboratory-con- fish enter the sea cages. Upon arrival, 30 fish were examined (mi- trolled experiments have shown promising results in the croscopic observation of fresh smears of the intestine) to ascertain control of enteromyxosis in gilthead seabream, Sparus the absence of the parasite. Fish were maintained in 250 l fibre- aurata (Linnaeus) using some functional feed additives glass tanks supplied with open-flow water along with aeration and (Palenzuela et al. 2017, Piazzon et al. 2017, Picard-Sánchez temperature ranging from 18–20 oC. The animals were given a et al. 2019). commercial diet until they reached a size of 12.5 ± 1.2 g, and were Functional feed additives are currently the focus for then transferred to a large (50 m3) inland cement tank and equally disease prevention and control, with the aim to reduce the distributed (300 fish) in six identical net cages (1 3;m 50 fish/cage). antimicrobial control agents as well as to reduce the en- Three of these cages served as the control group and the three vironmental risks (Defoirdt et al. 2011). These include a remaining cages as the functional diet group. In this environment, wide range of ingredients, such as probiotics, phytobiotics, experimental fish were delivered either control or functional ex- yeast extracts or organic acids, which can act in multiple truded diets prepared in the facilities. The functional diet includ- ways that promote the immune system and may reduce the ed Sanacore® GM, a commercial natural health promoting feed parasitic infections. Natural compounds with anti-parasitic additive (Adisseo, Dendermonde, Belgium) at 0.3% inclusion activity can directly affect gut parasites or indirectly affect levels. The composition of the diets is provided in Table 1. ectoparasites through their effects on blood or the composi- Throughout the trial, feed consumption was daily recorded. tion and quantity of the mucus (Coutteau 2016). Four weeks after the initiation of the dietary trial, a challenge To our knowledge, scarce studies exist so far regarding trial was performed for an additional four-week-period by cohab- the effects of functional feed additives on the sharpsnout itation with diseased fish. More specifically,
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