Monogenea: Capsalidae) Infecting Farmed Barramundi (Lates Calcarifer)
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Parasitol Res DOI 10.1007/s00436-015-4375-5 ORIGINAL PAPER Effects of temperature and salinity on the life cycle of Neobenedenia sp. (Monogenea: Capsalidae) infecting farmed barramundi (Lates calcarifer) Alexander K. Brazenor & Kate S. Hutson Received: 4 September 2014 /Accepted: 4 February 2015 # Springer-Verlag Berlin Heidelberg 2015 Abstract Effective parasite management can be achieved Keywords Aquaculture . Treatment . Asian sea bass . through strategically timed treatments that break the life cycle. Monogenea . Neobenedenia . Egg hatching We examined the effects of temperature (2 °C increments from 22 to 34 °C) and salinity (0, 11, 22, 35, 40‰) on the life cycle (embryonation period, hatching success, oncomiracidia (larvae) longevity, infection success, and time to sexual matu- Introduction rity) of Neobenedenia sp. (Monogenea: Capsalidae), a harm- ful ectoparasite of farmed marine fishes. Experiments were Integrated parasite management of farmed stock requires com- conducted in controlled conditions in the laboratory. The life prehensive and accurate knowledge of parasite life cycles and cycle was faster in warm, high saline conditions compared to the influence of environmental parameters to be effective. In cooler conditions (10–13 days between 26–32 °C, 40‰;15– agriculture, parasite management may include a combination 16 days between 22–24 °C at 40‰). Warm seawater and high of chemical treatments, resistant stock breeds and grazing pas- saline conditions (24–32 °C, 35–40‰) improved egg hatch- ture management practices such as fallowing or alternative ing success, reduced time to sexual maturity, and resulted in species grazing (Barger and Southcott 1978;Baker1996; parasites reaching sexual maturity at a larger size (at 30– Barger 1997; Waller 1997; Stromberg and Averbeck 1999). 32 °C) compared to cooler conditions (22 °C). In contrast, The aquaculture industry is, comparatively, in its infancy and cool, hypersaline conditions (22 °C, 40‰) increased knowledge of parasite/fish biology is not always sufficient to oncomiracidia longevity and infection success. Linear and enable efficient and effective treatments. One method of man- quantile regression models were used to construct an interac- aging ectoparasites in aquaculture is to administer treatments tive, online parasite management interface to enable strategic at times that disrupt or break the life cycle of the parasite. The treatment of parasites in aquaculture corresponding to ob- life cycle is interrupted by initially killing parasites on the served temperature and salinity variation on farms in the tro- host. Successive treatments are temporally coordinated to oc- pics. It was recommended that farmers treat their stock more cur after all eggs have hatched but before new parasite recruits frequently during summer (27–31 °C) when parasites can reach sexual maturity and contribute new eggs into the system complete their life cycle more quickly. Nevertheless, farmers (Tubbs et al. 2005). Essential to this method is the accurate should be aware of the potential for increased Neobenedenia determination of embryonation periods and time to sexual sp. infections during winter months (21–26 °C) due to in- maturity at a range of environmental parameters, allowing creased infection success. for treatments to be tailored to particular localities and farms (Hirayama et al. 2009). Effective administration of this meth- od results in lower re-infection rates, ultimately necessitating fewer treatments (Tubbs et al. 2005). Coordinated treatments : A. K. Brazenor (*) K. S. Hutson designed to improve the efficiency of parasite management Marine Parasitology Laboratory, Centre for Sustainable Tropical are recommended and have been successful in controlling Fisheries and Aquaculture and the College of Marine and parasites in agriculture including cow and sheep nematodes Environmental Sciences, James Cook University, Townsville, Queensland 4811, Australia (Bumgarner et al. 1986;Stuedemannetal.1989; Kelly et al. e-mail: [email protected] 2010) and sea lice outbreaks on salmon farms (Costello 2004), Parasitol Res whereas issues such as a lack of life cycle understanding and 1790) (Perciformes: Latidae) (Table 1). This enabled strategi- improperly coordinated treatments have been implicated in cally timed management recommendations that can be tai- reduced management efficiency (Bravo et al. 2008; Bravo lored to temperature and salinity conditions on aquaculture et al. 2013). Management strategies are not routinely imple- farms. mented for Monogenean infections due to a lack of knowledge of parasite life cycle parameters. Monogeneans in the family Capsalidae are a threat to the Materials and methods aquaculture industry as some species have been responsible for epizootic events (Deveney et al. 2001; Whittington Ethics statement 2004). Species of the genus Neobenedenia Yamaguti 1963, (Monogenea: Capsalidae) are known to be harmful ectopar- This work was conducted using barramundi, or Asian sea bass asites and have been recorded from over 100 teleost species, (L. calcarifer)—Neobenedenia sp. model system with all pro- many of which are important tropical and subtropical fin fish cedures approved by the James Cook University Animal species in marine aquaria and aquaculture (Whittington and Ethics Committee (A1579). Neobenedenia sp. used in exper- Horton 1996; Ogawa and Yokoyama 1998;Hirazawaetal. iments were collected from a private land in north 2004; Ogawa et al. 2006; Whittington 2012). Their direct Queensland, Australia. Future permissions should be directed life cycle, short generation time and filamentous eggs, which to Coral Coast Barramundi Pty Ltd. entangle on structure, cause difficulties in managing infec- tions and large numbers of parasites can become present in a system over a short period of time (Jahn and Kuhn 1932; Parasite collection, temperature and salinity treatments Ogawa et al. 1995; Ogawa et al. 2006). Neobenedenia spp. graze on the epithelial surface of their host and feed- A laboratory infection of Neobenedenia sp. (Fig. 1)sourced ing habit on host fish causes inflammation, dermal ulcer- from farmed marine L. calcarifer was established and ation and allows the ingress of secondary infections (Kaneko et al. 1988). Table 1 Life cycle parameters of Neobenedenia sp. infecting Lates calcarifer in various temperature/salinity combinations Current management methods for capsalid Monogeneans involve immersing (‘bathing’) infected fish in hydrogen per- Temperature Salinity F/LH OL SM LC oxide, formalin or freshwater (Ernst et al. 2002; Ogawa et al. (°C) (‰) (days) (hours) (days) (days) 2006), which only temporarily relieves stock of infection by 22 22 6–82±0.0–– removing attached parasite stages (Whittington 2012). These 35 6–7 37±3.3 12 18 treatment methods are ineffective in killing embryos within 40 7–8 49±1.5 9 16 eggs (Sharp et al. 2004;Militzetal.2013) and re-infection can 24 22 – 5±0.5 –– occur immediately following treatment of stock. Bathing con- 35 4–5 22±0.8 11 15 tinues to be the most commonly used management practice for 40 4–5 31±1.1 12 15 Monogenean infections and is widely used in the treatment of 26 22 – 2±0.0 12 – Gyrodactylus spp. epizootics (Schmahl and Mehlhorn 1988; 35 4–519±1.47 11 Schmahl and Taraschewski 1987; Santamarina et al. 1991; 40 4–5 28±2.6 6 10 Buchmann and Bresciani 2001; Buchmann and Kristensson 28 22 – 3±0.5 –– 2003; Schelkle et al. 2011). Although promising results have 35 4–5 11±0.7 9 13 been recorded from the administration of praziquantel through – intubation, the oral administration of anthelminthics has been 40 4 5 10±1.0 9 13 – hindered by palatability issues (Williams et al. 2007;Hardy- 30 22 4 93±0.58 12 – Smith et al. 2012; Forwood et al. 2013) and variable efficacy 35 4 68±0.86 10 – between species (Hirazawa et al. 2013). 40 4 67±0.46 10 –– Data on parasite life cycle parameters in a variety of tem- 32 22 4 2±0.3 – perature and salinity conditions enables more accurate bathing 35 4 88±0.86 10 – regimes and can improve the efficacy of current farm practice. 40 4 86±0.38 12 The aim of this study was to investigate the effects of temper- 34 22 9 2±0.0 –– ature and salinity on the life cycle parameters (embryonation 35 – 7±1.2 12 – period, hatching success, oncomiracidia longevity, infection 40 6–96±0.98 14 success and time to sexual maturity) of Neobenedenia sp. in F/LH time to first and last hatch, OL average oncomiracidia longevity± order to develop an interactive strategic management tool for SE (OL), SM minimum time to sexual maturity; LC minimum time to the treatment of farmed barramundi (Lates calcarifer, Bloch, completion of life cycle (LC) Parasitol Res maintained to ensure a continuous source of parasites for ex- salinities including freshwater (0‰), hyposaline (11 and 22 perimentation (see Militz et al. 2013). Experimental ‰), seawater (35‰), and hypersaline solutions (40‰) were L. calcarifer were sourced from a freshwater hatchery and chosen to represent extreme salinity fluctuations observed in acclimated to 35‰ seawater for 24 h prior to experimentation. open, semi-closed and closed aquaculture systems used to farm Fish were not previously exposed to Neobenedenia sp. infec- L. calcarifer in tropical climates. Hyposaline solutions (11 and tion. The species of Neobenedenia sp. investigated in this 22‰) were prepared by mixing distilled water and filtered study is presently unidentified to species level due to the ab- seawater to the desired concentration in a sterile container. sence of diagnostic