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Monogenea: Capsalidae) from Seriola Rivoliana (Almaco Jack) in Bahía De La Paz, BCS Mexico

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Monogenea: Capsalidae) from Seriola Rivoliana (Almaco Jack) in Bahía De La Paz, BCS Mexico Parasitology Research (2019) 118:3267–3277 https://doi.org/10.1007/s00436-019-06460-1 FISH PARASITOLOGY - ORIGINAL PAPER Effects of temperature on the life cycle of Neobenedenia sp. (Monogenea: Capsalidae) from Seriola rivoliana (Almaco jack) in Bahía de La Paz, BCS Mexico Isabel Valles-Vega1 & Felipe Ascencio1 & Teresa Sicard-González1 & Carlos Angulo1 & Emma J. Fajer-Avila2 & Roxana Bertha Inohuye-Rivera1 & Juan Carlos Pérez-Urbiola1 Received: 12 December 2018 /Accepted: 11 September 2019 /Published online: 31 October 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Seriola rivoliana cultivated in Mexico are infected by Neobenedenia sp. (Monogenea: Capsalidae), resulting in dermal ulceration and subsequent bacterial invasion that can cause fish death. This study assesses the effects of temperature over hatching success, oncomiracidia longevity, and infection success. The experimental design consisted of culturing the parasite at temperatures ranging between 16 and 32 °C. The oncomiracidia infection success, time to sexual maturity, and size at sexual maturity of Neobenedenia sp. were examined only at three temperatures (20 °C, 24 °C, and 30 °C). Experiments were conducted under controlled conditions in the laboratory. The oncomiracidia development was found to be faster at warmer temperatures (4–5days between 24 and 30 °C) than in colder treatments (7–11 days between 18 and 20 °C). Hatching success and oncomiracidia longevity were higher at 24 °C and 26 °C. At 20 °C, 24 °C, and 30 °C, infection success was greater than 90%. Additionally, the laid eggs were observed at 9, 12, and 15 days at 30 °C, 24 °C, and 30 °C, respectively. The results of this study will allow for improving the temporal schedule of applications of treatments against Neobenedenia sp. by the function of temperatures. In conclusion, it is recommended to treat fish more frequently if the temperature in cultures is higher than 24 °C, because Neobenedenia sp. development is faster. As an alternative, the fish could be moved to deeper and cooler waters. Keywords Capsalidae . Neobenedenia . Early development . Sexual maturity . Water temperature . Seriola rivoliana Introduction been recorded to be infected by Neobenedenia species, (Rubio-Godoy et al. 2011;Brazenoretal.2018), including Monogeneans Capsalidae are marine parasites (Ogawa 1996; S. rivoliana (Valenciennes, 1833) which is a recently Whittington et al. 2001; Tubbs et al. 2005). Within these spe- exploited species of Mexican aquaculture farms (Avilés- cies, the genus Neobenedenia hasbeenrecognizedasanec- Quevedo and Castello-Orvay 2004). toparasite of farmed fish around the world (Ogawa et al. 1995; Infection of Seriola spp. by capsalids like N. girellae Hirazawa et al. 2010; Trasviña-Moreno et al. 2017). Along the (Hargis 1955) can cause hemorrhage, inflammation, and mu- Pacific and Atlantic coast of Mexico, several fish species have cus hyperproduction (Paperna 1991). Heavily infected fish may also stop feeding and in some cases, the fish may rub Section Editor: Guillermo Salgado-Maldonado against the sea-cage nets resulting in dermal ulceration and subsequent bacterial invasion (Leong and Colorni 2002). * Juan Carlos Pérez-Urbiola Hence, Neobenedenia spp. can cause serious health problems [email protected] in farmed fish. Neobenedenia spp., as well as other monogenean, have a 1 Centro de Investigaciones Biológicas del Noroeste (CIBNOR) S.C., Km. 1, Carretera a San Juan de La Costa BEl Comitán^, 23097 La direct life cycle that does not require an intermediate host in Paz, Baja California Sur, Mexico order to complete their biological cycle (Rohde 1993). They 2 Centro de Investigación en Alimentación y Desarrollo, A. C., Unidad are able to reproduce rapidly, and produce eggs that often Mazatlán en Acuicultura y Manejo Ambiental, Av. Sábalo Cerritos become entangled in the sea-cage netting, leading, in many s/n, C.P., 82010 Mazatlán, Sinaloa, Mexico cases, to re-infection of the farmed fish (Ernst et al. 2002). 3268 Parasitol Res (2019) 118:3267–3277 It is well-known that eggs are more resistant than other Neobenedenia sp. in aquaculture systems. Hence, the present developmental stages to anti-helmintic agents such as study describes temperature effects on the life cycle of praziquantel or other cleaning treatments including baths of Neobenedenia sp. from S. rivoliana. freshwater, hydrogen peroxide, and formalin (Thoney and Hargis 1991; Morales-Serna et al. 2018). Due to this high resistance of eggs, fish are at risk of being re-infected and it Material and methods is difficult to control species of Neobenedenia in aquaculture systems (Diggles et al. 1993; Yoshinaga et al. 2000). Initial experimental settings Neobenedenia spp. infections commonly occur with the onset of summer when higher temperatures reduce the time Adults of capsalids were collected from Almaco jack of hatching and age of maturity (Bondad-Reantaso et al. 1995; (S. rivoliana) juvenile fish maintained in ponds at the Kinami et al. 2005; Hirazawa et al. 2010). In this regard, Northwest Biological Research Centre (CIBNOR). The fish Brazenor and Hutson (2015) have shown that hatching time were anesthetized with a solution of eugenol (3 ml × 100 l−1) for Neobenedenia sp. from Lates calcarifer varied between 6– as recommended by Boijink et al. (2016). Living parasites 8daysat22°Cand4–6 days at 24 °C and 30 °C. In addition, were carefully removed from the fish skin and some selected N. girellae eggs hatched in a temperature range between 18 specimens were fixed with formaldehyde and changed to 70% and 30 °C, but did not hatch at 15 °C (Bondad-Reantaso et al. ethanol and stained with Gomori’s trichrome, cleared with 1995). Thus, temperature has an effect on the development of salicylate and mounted in permanent preparations with the early stages of N. girellae (based on Brazenor et al. 2018) synthetic resins, for identification purposes. Adults of collected in Japan and Australia. capsalids were identified as Neobenedenia sp. based on the N. girellae can infect a wide variety of hosts (i.e., Lates description of Whittington and Horton (1996) and some of calcarifer (Bloch, 1790), Paralichthys olivaceus (Temminck them were deposited in the Parasitological Collection of the & Schlegel, 1846), S. lalandi (Valenciennes, 1833), Natural History Museum at Universidad Autónoma de Baja S. quinqueradiata (Temminck & Schlegel, 184), California Sur (CPMHN-UABCS) with the accession number Rachycentron canadum (Linnaeus, 1766), and other species), 725 (Fig. 1). within tropical regions of the Pacific and Atlantic Oceans To collect enough parasites for the experiments, we first (Brazenor et al. 2018). This is unusual because ~ 80% of all transferred 35 adults of Neobenedenia sp., from the skin of monogeneans infect a single species and they are usually dis- Almaco jack to a six-well flat-bottom culture vessel where tributed in one ocean basin (Rohde 1979; Byrnes and Rohde 1992; Whittington 1998). A recent study based on genetic analysis showed that spe- cies other than N. girellae have infected cultured S. lalandi and wild fish off the Northern coast of Chile (Sepúlveda and González 2019). This allows for the possibility that Neobenedenia form a complex of cryptic species that may adapt to their local conditions (Whittington 2004). This is relevant because a misunderstanding of the true delineation of parasitic species may affect diagnostic, control, and eradi- cation programs. Thus, an accurate knowledge of the life cycle of Neobenedenia sp. and the influence of temperature will help to design specific temporal schedules of treatments by the function of temperature to better combat this parasite (Tubbs et al. 2005; Nadler and Perez-Ponce De León 2011). The carangid Seriola rivoliana (Almaco jack) is currently being cultured in Bahía de La Paz, BCS, Mexico, where the surface water temperature varies during the annual cycle from 20.5 °C in the winter to 31 °C in the summer (Obeso-Nieblas et al. 2008; Guevara-Guillén et al. 2015). However, the influ- ence of water temperature on oncomiracidia development, Fig. 1 Ventral view of an adult Neobenedenia sp., stained with Gomori’s hatching success, oncomiracidia longevity, and infection suc- trichrome. aa, anterior attachment organ; ah, anterior hamulus; as, cess and time to sexual maturity of Neobenedenia sp. from accessory sclerite; e, egg; g, germarium; h, haptor; m, marginal valve; ic, internal fertilization chamber; oo, ootype; p, pharynx; pe, penis; ph, S. rivoliana has not been previously investigated. This infor- posterior hamulus; t, testis; te, tendon; u, uterus; vd, vas deferens; vf, mation is useful for developing strategies to better control vitelline follicle; vr, vitelline reservoir. Scale bars represent 200 μm Parasitol Res (2019) 118:3267–3277 3269 they deposited eggs. In the culture vessels, the eggs developed determined when the eggs appeared empty and were charac- into oncomiracidia larvae and, then they were used for infect- terized by a clear color and an open operculum (see Fig. 2). ing Almaco jack juveniles (average weight 150 ± 50 g) in the laboratory. The infections were carried out in two tanks of Hatching success and times 600 l. In each tank, three fish were placed and conditions were kept constant (salinity 36 ± 1 ppt, dissolved oxygen 5.5 ± Hatching success was evaluated in another set of tubes with 0.5 mg O2/l, temperature 25 ± 1 °C, and natural photoperiod). the nylon threads with 35 eggs, which were incubated at Fish were fed twice a day with a commercial diet (EWOS® 16 °C, 18 °C, 20 °C, 22 °C, 24 °C, 26 °C, 28 °C, 30 °C, and Canada Ltd., Vancouver, British Columbia, Canada) and at 32 °C (three replicates per temperature) in SITMA. Tubes daily feeding rate of 3% of the body weight. were monitored every 24 h under a stereomicroscope with All experiments were made in a water bath system and both incident and transmitted light and a third of the water thermal control was by the thermic simulator called SITMA was replaced daily. (from the Spanish BMarine Thermic Simulator^), which was When a stage 3 egg was detected, we looked for the developed at CIBNOR (Sicard-Gonzalez 2006).
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