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Reproductive Strategies of the Insidious Fish Ectoparasite, Neobenedenia sp. (Capsalidae: Monogenea)

1 , 2 , 1 , *

PLoS ONE

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      Abstract

      Fish monogeneans are lethal parasites in aquaculture. We provide the first experimental evidence that a notorious fish monogenean, Neobenedenia sp., can produce viable eggs in isolation for three consecutive generations. We infected individual, isolated, farmed barramundi, Lates calcarifer (Bloch) with a single oncomiracidium (larva) of the hermaphroditic monogenean Neobenedenia sp. Isolated parasites reached sexual maturity at day 10 post-hatch (24°C, 35‰) and laid ∼3,300 embryonated eggs over 17 days. Egg production rapidly increased following sexually maturity on day 10 (58±15 eggs) and peaked on day 15 (496±68 eggs) before gradually decreasing. Neobenedenia sp. exhibited egg laying and egg hatching rhythms. Parasites laid eggs continuously, but egg production increased in periods of darkness (64.3%), while the majority of oncomiracidia (81%) emerged from eggs in the first three hours of light. Eggs laid by isolated ‘parent’ parasites hatched and individual emerging oncomiracidia were used to infect more individual, isolated fish, with three consecutive, isolated, parasite generations (F1, F2 and F3) raised in the laboratory. Infection success and egg hatching success did not differ between generations. Our data show that one parasite, in the absence of a mate, presents a severe threat to captive fish populations.

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      Most cited references 28

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      Are there general laws in parasite ecology?

       R Poulin (2007)
      As a scientific discipline matures, its theoretical underpinnings tend to consolidate around a few general laws that explain a wide range of phenomena, and from which can be derived further testable predictions. It is one of the goals of science to uncover the general principles that produce recurring patterns in nature. Although this has happened in many areas of physics and chemistry, ecology is yet to take this important step. Ecological systems are intrinsically complex, but this does not necessarily mean that everything about them is unpredictable or chaotic. Ecologists, whose grand aim is to understand the interactions that govern the distribution, abundance and diversity of living organisms at different scales, have uncovered several regular patterns, i.e. widely observable statistical tendencies, in the abundance or diversity of organisms in natural ecosystems. Some of these patterns, however, are contingent, i.e. they are only true under particular circumstances; nevertheless, the broad generality of many patterns hints at the existence of universal principles. What about parasite ecology: is it also characterized by recurring patterns and general principles? Evidence for repeatable empirical patterns in parasite ecology is reviewed here, in search of patterns that are consistently detectable across taxa or geographical areas. The coverage ranges from the population level all the way to large-scale patterns of parasite diversity and abundance (or biomass) and patterns in the structure of host-parasite interaction networks. Although general laws seem to apply to these extreme scales of studies, most patterns observed at the intermediate scale, i.e. the parasite community level, appear highly contingent and far from universal. The general laws uncovered to date are proving valuable, as they offer glimpses of the underlying processes shaping parasite ecology and diversity.
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        The capsalidae (Monogenea: Monopisthocotylea): a review of diversity, classification and phylogeny with a note about species complexes.

        The Capsalidae are monogeneans parasitizing 'skin', fins and gills of marine fishes. Some capsalids are pathogenic to cultivated fish and a few have caused epizootic events. It is a cosmopolitan family with broad host associations (elasmobranchs and teleosts, including sturgeons). Approximately 200 capsalid species are placed in nine subfamilies and 44-46 genera, some of which are well known (Benedenia, Capsala, Entobdella, Neobenedenia). Sturgeons host two capsalid species (Nitzschiinae) and 15 species in five genera are reliably reported from elasmobranchs. The combination of ancient (shark, ray, sturgeon) and modem (teleost) host fish lineages indicates that capsalid evolution is likely a blend of coevolution and host-switching, but a family phylogeny has been lacking due to deficient knowledge about homologies. The current phenetic subfamilial classification is discussed in detail using a preliminary phylogeny generated from large subunit ribosomal DNA sequence data from representatives of five subfamilies. Monophyly of the Capsalidae is supported by possession of accessory sclerites. Hypotheses are proposed for the possible radiation of capsalids. A suggestion that Neobenedenia melleni, a pathogenic species atypical due to its broad host-specificity (>100 host teleost species from >30 families in five orders), may be a complex of species is supported from genetic evidence. This may explain peculiarities in biology, taxonomy, host associations and geographic distribution of N. 'melleni' and has implications for fish health. Holistic studies using live and preserved larval and adult capsalid specimens and material for genetic analysis are emphasised to further determine identity, phylogeny and details of biology, especially for pathogenic species.
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          Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas?

          Monogeneans (flatworms) are among the most host-specific of parasites in general and may be the most host-specific of all fish parasites. Specificity, in terms of a restricted spatial distribution within an environment, is not unique to parasites and is displayed by some fungi, insects, birds, symbionts and pelagic larvae of free-living marine invertebrates. The nature of cues, how "habitats" are recognised and how interactions between partners are mediated and maintained is of interest across these diverse "associations". We review some experiments that demonstrate important factors that contribute to host-specificity at the level of infective stages (larvae of oviparous monogeneans; juveniles of viviparous gyrodactylids) and adult parasites. Recent research on immune responses by fish to monogenean infections is considered. We emphasise the critical importance of host epidermis to the Monogenea. Monogeneans live on host epidermis, they live in its products (e.g. mucus), monopisthocotyleans feed on it, some of its products are "attractants" and it may be an inhospitable surface because of its immunological activity. We focus attention on fish but reference is made to amphibian hosts. We develop the concept for a potential role in host-specificity by the anterior adhesive areas, either the specialised tegument and/or anterior secretions produced by monogeneans for temporary but firm attachment during locomotion on host epithelial surfaces. Initial contact between the anterior adhesive areas of infective stages and host epidermis may serve two important purposes. (1) Appropriate sense organs or receptors on the parasite interact with a specific chemical or chemicals or with surface structures on host epidermis. (2) A specific but instant recognition or reaction occurs between component(s) of host mucus and the adhesive(s) secreted by monogeneans. The chemical composition of fish skin is known to be species-specific and our preliminary analysis of the chemistry of some monogenean adhesives indicates they are novel proteins that display some differences between parasite families and species.
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            Author and article information

            Affiliations
            [1 ]Marine Parasitology Laboratory, Centre for Sustainable Tropical Fisheries and Aquaculture and the School of Marine and Tropical Biology, James Cook University, Queensland, Australia
            [2 ]Aquatic Environment and Fish Pathology Department, Faculty of Animal Science and Aquaculture, Vietnam National University of Agriculture, Hanoi, Vietnam
            Temasek Life Sciences Laboratory, Singapore
            Author notes

            Competing Interests: The authors have declared that no competing interests exist.

            Conceived and designed the experiments: KSH. Performed the experiments: TDH. Analyzed the data: TDH KSH. Contributed reagents/materials/analysis tools: KSH. Wrote the paper: KSH TDH.

            Contributors
            Role: Editor
            Journal
            PLoS One
            PLoS ONE
            plos
            plosone
            PLoS ONE
            Public Library of Science (San Francisco, USA )
            1932-6203
            2014
            29 September 2014
            : 9
            : 9
            25264931
            4181869
            PONE-D-14-11687
            10.1371/journal.pone.0108801
            (Editor)

            This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

            Counts
            Pages: 7
            Funding
            This work was funded by an AusAID Scholarship ( www.ausaid.gov.au) awarded to TDH. The Australian Society for Parasitology ( http://parasite.org.au/) provided a Student Travel Award for TDH to present this research at the annual conference in Launceston, Tasmania, Australia in 2012. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Categories
            Research Article
            Biology and Life Sciences
            Agriculture
            Aquaculture
            Developmental Biology
            Life Cycles
            Parasitic Life Cycles
            Parasitology
            Ectoparasites
            Parasite Physiology
            Zoology
            Animal Behavior
            Animal Sexual Behavior
            Helminthology
            Custom metadata
            The authors confirm that all data underlying the findings are fully available without restriction. Data are available from the James Cook University Research Database: https://research.jcu.edu.au/researchdata/published/detail/d9eda2a2d49ef0b1ab4de74a2c77c826/.

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