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Cardiocephaloides Longicollis (Rudolphi, 1819) Dubois, 1982 (Strigeidae) Into the Gilthead Seabream Sparus Aurata L

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Cardiocephaloides Longicollis (Rudolphi, 1819) Dubois, 1982 (Strigeidae) Into the Gilthead Seabream Sparus Aurata L van Beest et al. Parasites Vectors (2019) 12:92 https://doi.org/10.1186/s13071-019-3351-9 Parasites & Vectors RESEARCH Open Access In vivo fuorescent cercariae reveal the entry portals of Cardiocephaloides longicollis (Rudolphi, 1819) Dubois, 1982 (Strigeidae) into the gilthead seabream Sparus aurata L. Gabrielle S. van Beest1,2*, Mar Villar‑Torres1, Juan Antonio Raga1, Francisco Esteban Montero1 and Ana Born‑Torrijos1,2 Abstract Background: Despite their complex life‑cycles involving various types of hosts and free‑living stages, digenean trematodes are becoming recurrent model systems. The infection and penetration strategy of the larval stages, i.e. cer‑ cariae, into the fsh host is poorly understood and information regarding their entry portals is not well‑known for most species. Cardiocephaloides longicollis (Rudolphi, 1819) Dubois, 1982 (Digenea, Strigeidae) uses the gilthead seabream (Sparus aurata L.), an important marine fsh in Mediterranean aquaculture, as a second intermediate host, where they encyst in the brain as metacercariae. Labelling the cercariae with in vivo fuorescent dyes helped us to track their entry into the fsh, revealing the penetration pattern that C. longicollis uses to infect S. aurata. Methods: Two diferent fuorescent dyes were used: carboxyfuorescein diacetate succinimidyl ester (CFSE) and Hoe‑ chst 33342 (NB). Three ascending concentrations of each dye were tested to detect any efect on labelled cercarial performance, by recording their survival for the frst 5 h post‑labelling (hpl) and 24 hpl, as well as their activity for 5 hpl. Labelled cercariae were used to track the penetration points into fsh, and cercarial infectivity and later encyst‑ ment were analysed by recording brain‑encysted metacercariae in fsh infected with labelled and control cercariae after 20 days of infection. Results: Although the diferent dye concentrations showed diverse efects on both survival and activity, intermedi‑ ate doses of CFSE did not show any short‑term efect on survival, permitting a brighter and longer recognition of cercariae on the host body surface. Therefore, CFSE helped to determine the penetration points of C. longicollis into the fsh, denoting their aggregation on the head, eye and gills region, as well as on the dorsal fn and the lower side. Only CFSE‑labelled cercariae showed a decreased number of encysted metacercariae when compared to control. Conclusions: Our study suggests that CFSE is an adequate labelling method for short‑term in vivo studies, whereas NB would better suit in vivo studies on long‑term performance. Cardiocephaloides longicollis cercariae seem to be attracted to areas near to the brain or those that are likely to be connected to migration routes to neuronal canals. Keywords: Cardiocephaloides longicollis, Cercarial penetration pattern, Cercarial survival and activity, Metacercarial encystment, Digenea *Correspondence: [email protected] 1 Cavanilles Institute for Biodiversity and Evolutionary Biology, Science Park, University of Valencia, P.O. Box 22 085, 46071 Valencia, Spain Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. van Beest et al. Parasites Vectors (2019) 12:92 Page 2 of 10 Background been previously employed to reveal, in particular, attach- Host-parasite interactions represent a useful model for a ment, distribution and development of monogenean better understanding of the evolution of animal life his- larvae on fsh (CFSE, [21, 22]), to localize protein kinase tory traits and behaviours. Digeneans (Platyhelminthes: C in cercariae (CFSE, [23]) and to discriminate live and Trematoda) are particularly suitable for experimental dead S. mansoni eggs (NB, [24]) and S. mansoni cercariae studies and, as they are highly diverse and spread all over exposed to human serum (NB, [25]). the world, they are becoming recurrent model systems For this study, cercariae of Cardiocephaloides longi- [1–5]. Generally, their complex life-cycles involve mul- collis (Rudolphi, 1819) Dubois, 1982 (Strigeidae) were tiple developmental stages and transmission events [6, labelled, allowing their tracking on fsh surfaces and thus 7]. In most life-cycles, the frst intermediate host, usu- their entry portals into them. Te cercariae of this dige- ally a gastropod, harbours larval stages (sporocysts or nean parasite penetrate the skin and migrate into the fsh rediae), which mature so that fully developed cercariae brain, where they encyst as metacercariae [26]. Te study are released into the water. In most cases, these larvae of their transmission to the next intermediate host is par- infect a second intermediate host within a certain period ticularly interesting as they infect fsh farm species such of time (hours to days), usually another mollusc or a fsh, as the gilthead seabream (Sparus aurata L.), which is one where they encyst as metacercariae before being con- of the most important marine fsh in the Mediterranean sumed by defnitive hosts, usually fsh, birds or mam- aquaculture, with prevalences of up to 53.9% [27]. Tere- mals, in which the parasites complete their life-cycles by fore, the present study aimed to investigate the penetra- sexual reproduction [8]. tion pattern of C. longicollis cercariae into fsh. Te use of Good timing of cercarial emergence in the target host fuorescent-labelling methods with cercariae is tested and habitat is crucial to ensuring contact with their host, due evaluated by analysing their efect on cercarial survival to the limited lifespan and energy reserves of cercariae and activity after 24 hours of labelling as well as on their needed until the infection of the second intermedi- viability to successfully infect and encyst in a fsh host. ate host [9, 10]. Terefore, glycogen reserves need to be optimized [11, 12]. Although some species are passively transmitted to the second intermediate host, generally Methods cercariae actively infect the next host, whether by chance, Parasite and host material invading the host anywhere along the entire body surface For obtaining Cardiocephaloides longicollis cercariae, the [13] or by a specifc infective strategy in particular areas. snail host Nassarius reticulatus was collected randomly For example, Centrocestus armatus cercariae specifcally during spring 2017 at the “Beach of the Eucalyptus” infect the host through the gills [14] and eye-fuke cer- (40°37′35.0″N, 0°44′31.0″E) in Els Alfacs Lagoon (Ebro cariae specifcally infect the fsh eyes by penetrating the Delta, Spain). After acclimatisation to laboratory con- gills and the skin (e.g. Diplostomum spathaceum, [15]). ditions, snails were screened for infections by incubat- Once cercariae fnd their host, a complex process starts, ing them individually in 96-well plates for 24 h at 25 °C, with distinct phases of attachment and penetration. Te 12:12h light:dark cycle and 35 psu salinity, thereafter penetration glands of cercariae play an important role in being checked for cercarial emergence under a stereomi- the penetration process into the host through the skin. croscope. To guarantee a sufcient quantity of emerged Cercariae-host interaction activates their proteases and cercariae during experiments, uninfected snails were immunomodulatory activities, facilitating entrance into artifcially infected: faecal samples were collected every the host, as shown in Schistosoma mansoni [16, 17]. two months for one year from an isolated, large colony Nevertheless, there are no common attachment or pen- of yellow-legged gull hosts Larus michahellis inhabit- etration strategies among trematodes and, despite being ing an island (of the coast of Benidorm, Spain, Western essential to understand trematodes transmission, these Mediterranean, 38°30′07.6″N, 0°07′47.4″W). Te faeces processes remain unknown for most species, mostly were checked under a stereomicroscope and the eggs because their study is highly difcult. were morphologically identifed according to Dubois In vivo fuorescent dyes can be an adequate tool to [28]. Identifcation was confrmed molecularly in random study cercarial penetration patterns into fsh. Tis samples as described in Born-Torrijos et al. [29]. Faeces method has been used with platyhelminths for several containing C. longicollis eggs were dropped into snails’ applications, including post-infection identifcation of aquaria, and snails were periodically checked to detect trematode genetic clones [4], lipid utilization in S. man- infected specimens as previously described. Only newly soni [18], individual cestode tracking within intermediate emerged cercariae (all less than 2 h old), gathered from a host [19] and quantifcation of trematode larval infec- pool of cercariae emerged from 12 diferent snail hosts, tion success [20]. Te dyes suggested in this study have were used in the present study. van Beest et al. Parasites Vectors (2019) 12:92 Page 3 of 10 A total of 51 juvenile specifc-pathogen-free (SPF) Penetration pattern on host surface gilthead
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