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      Beyond Symbiosis: Cleaner Shrimp Clean Up in Culture

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      PLoS ONE
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          Abstract

          Cleaner organisms exhibit a remarkable natural behaviour where they consume ectoparasites attached to “client” organisms. While this behaviour can be utilized as a natural method of parasitic disease control (or biocontrol), it is not known whether cleaner organisms can also limit reinfection from parasite eggs and larvae within the environment. Here we show that cleaner shrimp, Lysmata amboinensis, consume eggs and larvae of a harmful monogenean parasite, Neobenedenia sp., in aquaculture. Shrimp consumed parasite eggs under diurnal (63%) and nocturnal (14%) conditions as well as infectious larvae (oncomiracidia) diurnally (26%). Furthermore, we trialled the inclusion of cleaner shrimp for preventative parasite management of ornamental fish, Pseudanthias squamipinnis, and found shrimp reduced oncomiracidia infection success of host fish by half compared to controls (held without shrimp). Fish held without cleaner shrimp exhibited pigmentation changes as a result of infection, possibly indicative of a stress response. These results provide the first empirical evidence that cleaner organisms reduce parasite loads in the environment through non-symbiotic cleaning activities. Our research findings have relevance to aquaculture and the marine ornamental trade, where cleaner shrimp could be applied for prophylaxis and control of ectoparasite infections.

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          Most cited references15

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          Salmon lice – impact on wild salmonids and salmon aquaculture

          Salmon lice, Lepeophtheirus salmonis, are naturally occurring parasites of salmon in sea water. Intensive salmon farming provides better conditions for parasite growth and transmission compared with natural conditions, creating problems for both the salmon farming industry and, under certain conditions, wild salmonids. Salmon lice originating from farms negatively impact wild stocks of salmonids, although the extent of the impact is a matter of debate. Estimates from Ireland and Norway indicate an odds ratio of 1.1:1-1.2:1 for sea lice treated Atlantic salmon smolt to survive sea migration compared to untreated smolts. This is considered to have a moderate population regulatory effect. The development of resistance against drugs most commonly used to treat salmon lice is a serious concern for both wild and farmed fish. Several large initiatives have been taken to encourage the development of new strategies, such as vaccines and novel drugs, for the treatment or removal of salmon lice from farmed fish. The newly sequenced salmon louse genome will be an important tool in this work. The use of cleaner fish has emerged as a robust method for controlling salmon lice, and aquaculture production of wrasse is important towards this aim. Salmon lice have large economic consequences for the salmon industry, both as direct costs for the prevention and treatment, but also indirectly through negative public opinion.
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            Parasites of the superorganism: are they indicators of ecosystem health?

            The concept of ecosystem health is derived from analogies with human health, which subsequently leads to the implication that the ecosystem has organismal properties, a 'superorganism' in the Clementsian sense. Its application and usefulness has been the subject of a contentious debate; yet, the term 'ecosystem health' has captured the public's imagination and woven its way into the current lexicon, even incorporated into public policy. However, the application of parasites as bioindicators of ecosystem health poses a curious conundrum. Perceptions of parasites range from mild distaste to sheer disgust among the general public, the media, environmental managers and non-parasitologists in the scientific community. Nevertheless, the biological nature of parasitism incorporates natural characteristics that are informative and useful for environmental management. The helminths in particular have evolved elegant means to ensure their transmission, often relying on complex life cycle interactions that include a variety of invertebrate and vertebrate hosts. The assemblage of these diverse parasites within a host organism potentially reflect that host's trophic position within the food web as well as the presence in the ecosystem of any other organisms that participate in the various parasite life cycles. Perturbations in ecosystem structure and function that affect food web topology will also impact upon parasite transmission, thus affecting parasite species abundance and composition. As such, parasite populations and communities are useful indicators of environmental stress, food web structure and biodiversity. In addition, there may be useful other means to utilise parasitic organisms based on their biology and life histories such as suites or guilds that may be effective bioindicators of particular forms of environmental degradation. The challenge for parasitology is to convince resource managers and fellow scientists that parasites are a natural part of all ecosystems, each species being a potentially useful information unit, and that healthy ecosystems have healthy parasites.
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              Combined effects of parasites and contaminants on animal health: parasites do matter.

              The cumulative effects of multiple stressors are becoming a priority concern for ecotoxicologists, ecologists and conservation biologists working to understand threats to ecosystems and species. In that context, parasites and pathogens are increasingly a focus of attention. Parasites interact with natural and anthropogenic stressors to increase mortality and reduce animal health in myriad ways in a wide spectrum of host and parasite taxa. The combined effects of parasites and other stressors can reduce either resistance or tolerance to infection. Recommendations are provided to guide further research. Crown Copyright © 2010. Published by Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                23 February 2015
                2015
                : 10
                : 2
                : e0117723
                Affiliations
                [001]Centre for Sustainable Tropical Fisheries and Aquaculture, College of Marine and Environmental Sciences, James Cook University, Townsville, Queensland, Australia
                Institute of Marine Research, NORWAY
                Author notes

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

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

                Article
                PONE-D-14-45623
                10.1371/journal.pone.0117723
                4338302
                25706952
                df7a13f1-11da-4355-91aa-155f90d84901
                Copyright @ 2015

                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

                History
                : 10 October 2014
                : 31 December 2014
                Page count
                Figures: 4, Tables: 0, Pages: 11
                Funding
                KSH and TAM received funding for this research from the Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University ( http://research.jcu.edu.au/stfa). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Data are available from the James Cook University Research Database: http://doi.org/10.4225/28/547E5E41F35B0.

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