Control of Hysterothylacium Sp
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Aquaculture 494 (2018) 37–44 Contents lists available at ScienceDirect Aquaculture journal homepage: www.elsevier.com/locate/aquaculture Control of Hysterothylacium sp. (Nematoda: Anisakidae) in juvenile pirarucu T (Arapaima gigas) by the oral application of essential oil of Piper aduncum Amanda Curiel Trentin Corrala, Marieta Nascimento de Queiroza, Sanny Maria de Andrade-Portob, German Augusto Murrieta Moreyc, Francisco Celio Maia Chavesd, Valdelira Lia Araújo Fernandese, Eduardo Akifumi Onoa, ⁎ Elizabeth Gusmão Affonsoe, a Nilton Lins University, Av. Professor Nilton Lins 3259, Parque das Laranjeiras, 69058-030 Manaus, AM, Brazil b Federal University of Amazonas – UFAM, Faculdade de Ciências Agrárias, Departamento de Ciências Pesqueiras, Laboratório de Sanidade de Animais Aquáticos, Avenida Rodrigo Otávio, 6200, Setor Sul, Coroado, 69080-000 Manaus, AM, Brazil c Federal University of Paraná – UFPR, Laboratório de Ecologia Molecular e Parasitologia Evolutiva, rua XV de novembro, 1299, 80060-000 Curitiba, PR, Brazil d Empresa Brasileira de Pesquisa Agropecuária – EMBRAPA, Rodovia AM 10, km 29, s/n, 69010-970 Manaus, AM, Brazil e National Amazonia Research Institute - INPA, Coordenação de Tecnologia e Inovação, Avenida André Araújo 2936, 69067-375 Manaus, AM, Brazil ARTICLE INFO ABSTRACT Keywords: The nematode Hysterothylacium sp. (Nematoda, Anisakidae) may cause significant economic losses in fish pro- Farming duction. In order to control the nematode larvae in juvenile pirarucu (52 ± 3.2 g), the efficacy of essential oil Phytotherapic drug (EO) of Piper aduncum when added to feed was evaluated. Chemical analysis of the EO composition had been Helminths performed previously, showing that 92% of the substance was dillapiole. After the palatability test, the efficacy Amazon of the EO was evaluated (0, 32, 48, 56, and 64 mL/kg) at 7 and 15 days, based on the blood parameters and the parasite load of the fish. The results showed significant differences for hematocrit and corpuscular constants at 7 days and for total proteins at 15 days between the treatment groups and the control group (without EO). The parasitic indices showed a prevalence of 100% for stage L3 larva of the nematode Hysterothylacium sp. At 7 and 15 days, the values of average intensity, average abundance, and intensity of parasites decreased with increasing EO concentration, and at 15 days, these were significantly lower between the treatment group and the control group, with an efficacy of 76.21% for 64 mL/kg. Thus, the EO of P. aduncum demonstrates anthelmintic potential in the control of nematode larvae in pirarucu without affecting fish homeostasis. 1. Introduction spinulosa Diesing, 1939 (Araújo et al., 2009); Nilonema senticosum (Mathews et al., 2014); the monogenoids Dawestrema cycloancistrium The production of the pirarucu Arapaima gigas (Osteoglossiformes, Price & Nowlin, 1967; Dawestrema cycloancistrioides Kritsky, Boeger & Arapaimatidae), an endemic species in the Amazon region, has been Thatcher, 1985 (Araújo et al., 2009; Andrade-Porto et al., 2015; increasing each year despite the various obstacles encountered in its Marinho et al., 2013; Serrano-Martínez et al., 2015); Trichodina sp.; farming (IBGE, 2017). The initial phase of farming is considered the Trichodina heterodentata (Miranda et al., 2012); Ichthyobodo sp.; Ich- most critical for the survival due to nutritional and health problems, thyophthirius multifiliis (Marinho et al., 2013); Piscinoodinium pillulare and consequently, when post-larval loss is included, mortality can be as (Protozoa) (Araújo et al., 2009; Serrano-Martínez et al., 2015); Poly- high as 80% (Araújo et al., 2009; Marinho et al., 2013; Serrano- acanthorhynchus macrorhynchus Diesing, 1856 (Acanthocephala); Ca- Martínez et al., 2015; Andrade-Porto et al., 2015). ballerotrema brasiliense (Digenea); and Schizochoerus liguloides (Cestoda) Such losses have been attributed primarily to high infestation by (Marinho et al., 2013). Recently, the first record of larvae in the third and/or to infections caused by pathogens, particularly parasites. The stage (L3) of Hysterothylacium sp. (Nematoda, Anisakidae) was de- literature describes numerous species of parasites of pirarucu in farming scribed from South America, detected in the intestine, stomach, and systems, including the following intestinal nematodes: Camallanus tri- pyloric caeca of specimens of pirarucu juveniles grown in the Amazon dentatus Drasche, 1884; Terranova serrata Drasche, 1884; Goezia (Andrade-Porto et al., 2015). This nematode, when occurring at a high ⁎ Corresponding author at: Department of Technology and Innovation, National Amazonia Research Institute, Av. André Araújo 2936, P.O. Box 478, 69060-001 Manaus, AM, Brazil. E-mail address: [email protected] (E.G. Affonso). https://doi.org/10.1016/j.aquaculture.2018.04.062 Received 17 September 2017; Received in revised form 27 April 2018; Accepted 30 April 2018 Available online 11 May 2018 0044-8486/ © 2018 Elsevier B.V. All rights reserved. A.C.T. Corral et al. Aquaculture 494 (2018) 37–44 infection rate, can cause intestinal obstruction and lack of appetite in 45% powdered crude protein (CP) at 2-hour intervals. After this, the fish, causing significant economic losses in fish production; in addition, plankton was replaced by 2000 mL of water with increasing amounts of the presence of this nematode in food fish arises the concern to public feed at each feeding. After 15 days, the fish began to feed only on health because of indications that it may present a zoonotic potential powdered feed, and gradually, the size of the granules was increased (Balbuena et al., 2000; Felizardo et al., 2009; Andrade-Porto et al., until the fish were ingesting 4-mm granules of feed. 2015; Ribeiro et al., 2017). Recently, Ribeiro et al. (2017), assessed the During the fattening period, the fish were fed to satiation twice pathogenic potential of the third stage larvae of Hysterothylacium daily, with commercially extruded 4-mm feed for carnivorous fish (45% deardorffoverestreetorum in mammals and observed that this parasite CP) being used, until the fish reached the desired weight. Twenty-four can activate both cellular and humoral immune responses. Also, it can hours prior to the beginning of each experiment (palatability and effi- stimulate the immune system which may result in severe allergies and cacy tests), the fish went through food deprivation for gastrointestinal gastrointestinal manifestations. These results contribute to the better emptying. Before distributing the fish to the experimental units, a understanding of human anisakidosis, considering the lack of knowl- sample of 10 animals was removed to evaluate the parasitic load (Eiras edge regarding the immune response and allergic reaction of these et al., 2006). larvae in humans. This work was undertaken with the approval of the Committee for Several chemicals have been tested and used for the control of en- Ethics in Research in the Use of Animals (Comitê de Ética em Pesquisa doparasites and ectoparasites of fish. However, disadvantages exist, no Uso de Animais – CEUA) (Prot No. 023/2013). such as high treatment costs, toxicity for the animal or for humans, and the possibility of resistance by parasites to the active substances, in addition to the serious risks the chemicals pose to the environment, 2.2. Extracting the essential oil among others (Pahor-Filho et al., 2015). A practical, economical, and effective alternative that is gaining prominence in global aquaculture The leaves of P. aduncum were collected and dried at Embrapa are products from medicinal plants (Wang et al., 2011; Banerjee and Western Amazon (Embrapa Amazônia Ocidental) in Manaus, Brazil. For Saha, 2013; Reverter et al., 2014; Valladão et al., 2015; Andrade et al., complete removal of moisture, the leaves were kept at 45 °C, in ovens 2016; Hashimoto et al., 2016). Brazil, which holds the largest floristic with continuous air circulation, for 48 h and then were stored in bags at biodiversity of the planet and whose traditional population frequently 20 °C until the extraction of the essential oil. For this, the standard uses medicinal plants for treating various diseases, is taking advantage method of drag by water vapor was used in the Experimental Station of of this potential to produce phytotherapic drugs in disease control in Tropical Forestry of INPA. The hydrodistillation of the material was different sectors of animal production, including in fish farming (Souza- carried out in a semi-industrial-scale plant with a capacity of 20 kg, in Chagas et al., 2016; Ellse et al., 2016). which three machining operations were conducted, which resulted in Among the studied plants of medicinal interest, emphasis is being an oil extraction yield of 3.12%. given to the spiked pepper, Piper aduncum, which is widely distributed ff in the American tropics. The pharmacological e ects of its essential oil 2.3. Chemical composition of the essential oil of P. aduncum have shown efficacy in the control of pests and microorganisms, and it is important for agriculture because of its insecticidal, fungicidal, bac- The sample of essential oil of P. aduncum was subjected to analysis tericidal, acaricidal, molluscicidal, and parasiticidal characteristics to define its chemical composition using mass spectrometry (GC–MS (Orjala et al., 1993; Baldoqui et al., 1999; Almeida et al., 2009; Flores model GC2010/QP2010 Plus – Shimadzu Scientific Instruments, Kyoto, et al., 2009; Dal Picolo et al., 2014). The essential oil of P. aduncum Japan) at the Biotechnology