Advertisement
  • Loading metrics

New Paradigms to Help Solve the Global Aquaculture Disease Crisis

  • Grant D. Stentiford ,

    Contributed equally to this work with: Grant D. Stentiford, Kallaya Sritunyalucksana, Timothy W. Flegel, Bryony A. P. Williams, Boonsirm Withyachumnarnkul, Orn Itsathitphaisarn, David Bass

    grant.stentiford@cefas.co.uk

    Affiliation Pathology and Molecular Systematics Team, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth, United Kingdom

  • Kallaya Sritunyalucksana ,

    Contributed equally to this work with: Grant D. Stentiford, Kallaya Sritunyalucksana, Timothy W. Flegel, Bryony A. P. Williams, Boonsirm Withyachumnarnkul, Orn Itsathitphaisarn, David Bass

    Affiliation Shrimp-virus interaction laboratory, Animal Biotechnology Research unit, National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Bangkok, Thailand

  • Timothy W. Flegel ,

    Contributed equally to this work with: Grant D. Stentiford, Kallaya Sritunyalucksana, Timothy W. Flegel, Bryony A. P. Williams, Boonsirm Withyachumnarnkul, Orn Itsathitphaisarn, David Bass

    Affiliation Center of Excellence for Shrimp Molecular Biology and Biotechnology (Centex Shrimp), Faculty of Science, Mahidol University, Bangkok, Thailand

  • Bryony A. P. Williams ,

    Contributed equally to this work with: Grant D. Stentiford, Kallaya Sritunyalucksana, Timothy W. Flegel, Bryony A. P. Williams, Boonsirm Withyachumnarnkul, Orn Itsathitphaisarn, David Bass

    Affiliation Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom

  • Boonsirm Withyachumnarnkul ,

    Contributed equally to this work with: Grant D. Stentiford, Kallaya Sritunyalucksana, Timothy W. Flegel, Bryony A. P. Williams, Boonsirm Withyachumnarnkul, Orn Itsathitphaisarn, David Bass

    Affiliation Center of Excellence for Shrimp Molecular Biology and Biotechnology (Centex Shrimp), Faculty of Science, Mahidol University, Bangkok, Thailand

  • Orn Itsathitphaisarn ,

    Contributed equally to this work with: Grant D. Stentiford, Kallaya Sritunyalucksana, Timothy W. Flegel, Bryony A. P. Williams, Boonsirm Withyachumnarnkul, Orn Itsathitphaisarn, David Bass

    Affiliations Center of Excellence for Shrimp Molecular Biology and Biotechnology (Centex Shrimp), Faculty of Science, Mahidol University, Bangkok, Thailand, Department of Biochemistry, Faculty of Science, Mahidol University, Bangkok, Thailand

  • David Bass

    Contributed equally to this work with: Grant D. Stentiford, Kallaya Sritunyalucksana, Timothy W. Flegel, Bryony A. P. Williams, Boonsirm Withyachumnarnkul, Orn Itsathitphaisarn, David Bass

    Affiliations Pathology and Molecular Systematics Team, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth, United Kingdom, Life Sciences, Natural History Museum, London, United Kingdom

New Paradigms to Help Solve the Global Aquaculture Disease Crisis

  • Grant D. Stentiford, 
  • Kallaya Sritunyalucksana, 
  • Timothy W. Flegel, 
  • Bryony A. P. Williams, 
  • Boonsirm Withyachumnarnkul, 
  • Orn Itsathitphaisarn, 
  • David Bass
PLOS
x

Disease as a Barrier to Production

Despite significant under-representation in the global debate surrounding food security [1, 2], seafood (including fish, invertebrates, and algae) is the most highly traded of all food commodities [3], playing a key role in nutritional and financial security, particularly in developing economies [1]. The rising population (over 9 billion by 2050) and expanding middle income sector pose critical challenges to global human health related to nutritional deficiency [4]. Furthermore, a flat-lining capture fishery means aquaculture production must effectively double over this period to satisfy demand [5]. Forty years after the Food and Agriculture Organization of the United Nations (FAO) Technical Conference on Aquaculture [6], the implicit forecast in the Kyoto Declaration has largely been fulfilled with global aquaculture growing to rival production from the capture fishery [7]. The Bangkok Declaration, which followed recommended key requirements for development beyond 2000, identified management of animal health by cooperative action at national, regional, and inter-regional levels as “an urgent requirement for sustaining growth” [8]. Whereas significant progress has been made in identification, diagnostics, treatment, and zone management of disease in certain sectors (e.g., the European Atlantic salmon industry), recalcitrant issues (such as those associated with sea lice infestation) can remain significant barriers to expansion [9]. In other sectors, infectious diseases caused by viral, bacterial, and eukaryote pathogens continue to impose major yield-limiting effects on production. Industry-wide losses to aquatic animal diseases exceed US$6 billion per annum [10], rivaling in magnitude the projected proportional losses experienced in terrestrial livestock sector due to diseases such as foot-and-mouth disease [11]. In certain sectors (e.g., shrimp), infectious diseases are causing particularly devastating economic and social impacts, with total losses exceeding 40% of global capacity [12]. Emergent diseases, often with cryptic or syndromic aetiology (such as early mortality syndrome in shrimp), have collapsed production in nations across Asia [13], confirming disease as the major constricting factor for expansion of the aquaculture industry to 2050 [14]. Increasingly globalised trading of seafood between net exporting and importing nations expands the geographical range over which these effects are felt [7]. In this context, 50 early-career scientists from the United Kingdom and Thailand met with industry professionals and policymakers in March 2016 to consider the future challenge of managing disease in global aquaculture and to discuss new paradigms for mitigating their negative effects. This Opinion summarises major outcomes of those discussions and proposes a need to refocus strategic scientific and policy priorities relating to aquatic animal health in support of an expanding and sustainable industry to 2050.

Understanding Complex Systems

Aquatic environments impose a constant and omnipresent risk of pathogen exposure to resident hosts, perhaps even more so than terrestrial systems [15]. Poor knowledge of background microbial diversity in farm systems leads to frequent emergence of previously unknown pathogens, surprising farmers and creating shock in the wider value chain [16,17,18]. Scientific (pathology, systematics, diagnostics) and political (trade legislation, listing) responses to emergence are largely reactive and often slow [19], facilitating local–global transfer of pathogens via trading in live animals and products [20]. Historic focus on the development of case descriptions and fulfilment of Koch’s postulates for specific (listed) pathogens have undoubtedly been critical in notifying the wider community of emergent issues but arguably have politicised (and popularised) research on specific facets of those pathogens. This has been at the cost of investigating the very context (e.g., microbiomes, physicochemical conditions, host response) in which they are allowed to manifest as yield-limiting disease. In addition, whilst cost–benefit analyses have focussed on freedom from or eradication of the most politicised pathogens [21], less effort has been placed on management of nonlisted “production diseases” that may severely impact yields. This creates friction between industry operatives and the scientific evidence base that is funded by national research monies to support that industry. Whilst striving for disease freedom will remain a key aim in countries/systems where more stringent biosecurity processes are already in place, the avoidance of disease outbreaks by management of pond and animal microbiomes (rather than attempting to eliminate the presence of given pathogens) may provide a more viable means of mitigating losses in certain open systems in the future [22]. High throughput sequencing (HTS) applied to open aquatic systems is rapidly increasing our knowledge of prokaryotic and eukaryotic diversity and the complex symbiotic arena in which they exist [23]. Application of so-called “environmental DNA” (eDNA) approaches to aquaculture pond systems (e.g., in outbreak and non-outbreak scenarios) will provide this much-needed context for conditions surrounding disease emergence by detecting specific pathogens of consequence to farmed hosts or those elements of the microbiome that facilitate their emergence as disease agents [24]. Improved definition of a “pathobiome” within hosts may be expected to supersede an historic focus on specific pathogens as sole perpetrators of yield-limiting disease [25]. A shift from single-pathogen to pathobiome concepts may also expose a wider target to which pond management strategies can be applied [26]. While these concepts are not necessarily new (the microbiology of diverse aquaculture systems has been studied and manipulated extensively [27]), the application of modern HTS approaches will not only accelerate our understanding of the complex trophic (e.g., prokaryotic, eukaryotic) structures that exists within such systems but also the effect of intervention on eventual health outcomes for farmed animals living there [28]. Similar concepts are reported in other large agri-systems (e.g., relating the microbiome to global pollinator health) [29] or, conversely, the contribution of microbial consortia to disease suppression in soils [30]. Investigating the common set of conditions that allow disease to emerge across diverse hosts and biomes clearly provides a nexus for future research, allowing aquaculture to benefit from parallel advances in agriculture, botany, zoology, and medical disciplines [31].

Equipping the Host

The ability for farmed hosts to tolerate the pond environment is, of course, critical as well. Vaccination will retain a central role in the mitigation of known and emerging diseases in finfish [32], with intelligent use of autogenous (“emergency”) vaccines showing high potential for rapid deployment following detection of emergent diseases [33]. The scenario is different for invertebrates, in which traditional vaccination is not possible. Here, solutions based around better knowledge of the genome (of host and pathogen) are required. Despite multibillion-dollar annual production metrics for aquatic livestock like tilapia and shrimp, until recently, a lack of publicly available genomic data has hampered progress in understanding host–pathogen interaction, selective breeding, and development of therapeutics [34, 35]. Particularly for shrimp, the problems associated with high-frequency genomic sequence repeats [34] may be overcome by application of longer-read sequencing technologies alongside other shorter-read technologies to allow for accurate assembly and characterisation. Open publication of such data as a “public good” will fast track new therapeutics [36] and provide increased acceptance of the importance of endogenous, viral-like elements in genetic immunity [37] (and, when deemed socially acceptable, in the production of edited-genome lines of fish [38], molluscs [39], and crustaceans [40]). Standardised approaches to pathogen (or pathobiome) sequencing and open data access must coincide with these developments [36]. The basis for controlling progression from infection to disease in farmed hosts will benefit from a better understanding of fundamental mechanisms for pathogen tolerance in wild hosts where host background genetic diversity is higher [41] and where exposure to pathogens may have left an inherited legacy of natural resistance [42, 43]. In this way, hatchery supply of specific-pathogen-free (SPF) larvae (produced with confirmed freedom from certain pathogens, though not necessarily “tolerant” to the microbiome or pathobiome of the receiving farm) should be augmented by provision of more diverse and broadly resilient lines, produced via well-managed selective breeding programmes, and potentially augmented using emerging genetic technologies (such as SNP arrays [44]). An ability to mitigate nonlisted production diseases [45] to deliver direct benefit to farm yield and profit is essential [46].

Policy and People

To date, national and international research programmes relating to aquaculture health have largely reflected a supranational focus on listed diseases, the occurrence of which can limit free trading [19, 21]. While clearly important in averting global pandemics due to emerging disease, this strategy is insufficient to prevent the impact of nonlisted production diseases in limiting yield from Low Income Food Deficit Countries (LIFDCs), where most of the current and future aquaculture industry is based. In this context, mitigating production diseases has largely been considered the responsibility of the industry itself. But times are changing. By setting time-bound global production growth targets to 2050, which in turn feed national production targets [5], there will be increasing need to focus on yield-limiting (rather than just trade-limiting) diseases. Aligning academic, government, and industry research funding programs is critically required. In doing so, defining basic research needs (e.g., on host and pathogen genomics) must cater to tangible translation (e.g., to rapid diagnostics) and application (e.g., pondside testing by farmers or government). This faster translation to “point-of-need” bridges the gap between farmer, scientist, and policymaker and defines the proportional investment required in aquatic animal health for public good at the national and international levels [21]. Networking of national strategies (and reference laboratory systems) will not only align investment but help to address a relative global deficit in trained aquatic health professionals and academics focussed on aquatic animal disease. Marginal improvements that reduce the global burden of disease in aquaculture will convert to direct benefits for yield, profit, poverty alleviation, and food security for producer nations [14]. More significant interventions, including those which capitalise on automated detection of pathogens and other remote sensing applications [47], have significant potential for mitigating the most important yield-limiting production diseases and will improve the insurability of the global aquaculture sector, promoting inward investment and assuring production targets to 2050 are met in a sustainable manner [7].

Acknowledgments

The authors wish to thank the early-career scientists, industry professionals, and policymakers attending the Newton Fund Researcher Links Programme workshop in Thailand entitled “Scientific, technological and social solutions for sustainable aquaculture in Thailand: a key player in global aquatic food supply” in March 2016, whose contributions helped to form the opinions outlined in this paper.

References

  1. 1. Béné C, Barange M, Subasinghe R, Pinstrup-Andersen P, Merino G, Hemre GI, Williams M. Feeding 9 billion by 2050 –Putting fish back on the menu. Food Sec. 2015;
  2. 2. Allison EH, Delaporte A, Hellebrandt de Silva D. Integrating fisheries management and aquaculture development with food security and livelihoods for the poor. Report submitted to the Rockefeller Foundation. Norwich: School of International Development, University of East Anglia. 2013.
  3. 3. FAO. Food and Agriculture Organization of the UN (FAO) (2012) The State of the World Fisheries and Aquaculture. 2012. FAO, Rome, Italy.
  4. 4. Golden CD, Allison EH, Cheung WWL, Dey MM, Halpern BS, McCauley DJ, Smith M, Vaitla B, Zeller D, Myers SS. Fall in fish catch threatens human health. Nature. 2016; 534: 317–320. pmid:27306172
  5. 5. Waite R, Beveridge M, Brummett R, Castine S, Chaiyawannakarn N, Kaushik S, Mungkung R, Nawapakpilai S, Phillips M. Improving Productivity and Environmental Performance of Aquaculture. Working Paper, Instalment 5 of Creating a Sustainable Food Future. Washington, DC: World Resources Institute. 2015. http://www.worldresourcesreport.org
  6. 6. FAO. Report on the FAO Technical Conference on Aquaculture, Kyoto, Japan, 26 May– 2 June 1976. FAO Fish. Rep. 1976; 188: 93p.
  7. 7. Jennings S, Leocadio AM, Jeffrey KR, Metcalfe JD, Katsiadaki I, Auchterlonie NA, Mangi SC, Pinnegar JK, Ellis T, Peeler EJ, Luisetti T, Baker-Austin C, Brown M, Catchpole TL, Clyne FJ, Dye SR, Edmonds NJ, Hyder K, Lee J, Lees DN, Morgan OC, O'Brien CM, Oidtmann B, Posen PE, Ribeiro Santos A, Taylor NGH, Turner AD, Townhill BL, Verner-Jeffreys DW, Stentiford GD. Aquatic food security: trends, challenges and solutions for a single nation embedded in a dynamic global web of producers, processors and markets. Fish Fisher. 2016;
  8. 8. FAO. Aquaculture Development Beyond 2000; the Bangkok Declaration and Strategy. Conference on Aquaculture in the Third Millennium, 20–25 February 2000. Bangkok. Thailand. NACA. Bangkok and FAO. Rome. 2000; 27p.
  9. 9. Rogers LA, Bateman AW, Connors BM Frazer LN, Godwin SC, Krkošek M, Lewis MA, Peacock SJ, Rees EE, Revie CW, Schlägel UE. Lessons from sea louse and salmon epidemiology. Phil. Trans. R. Soc. B (2016); 371 20150203; pmid:26880836
  10. 10. World Bank. Reducing disease risks in aquaculture. World Bank Report #88257-GLB. 2014.
  11. 11. Bio-Era (Bio Economic Research Associates). Economic impact of selected infectious diseases. See http://www.bio-era.net/reports/biosecurity/bsec_econ_impact.html. (2008).
  12. 12. Israngkura A, Sae-Hae S. A review of economic impacts of aquatic animal disease. In: Arthur JR, Phillips MJ, Subasinghe RP, Reantaso MB, McCrae IH (Eds): Primary Aquatic Animal Health Care in Rural, Small-scale Aquaculture Development, Technical Proceedings of the Asia Regional Scoping Workshop. FAO Fisheries Technical Paper 406, FAO, Rome. 2002; pp. 55–61.
  13. 13. Lee C-T, Chen IT, Yang Y-T, Ko T-P, Huang Y-T, Huang J-Y, Huang M-F, Lin S-J, Chen C-Y, Lin S-S, Lightner DV, Wang H-C, Wang AHJ, Wang H-C, Hor L-I, Lo C-F. The opportunistic marine pathogen Vibrio parahaemolyticus becomes virulent by acquiring a plasmid that expresses a deadly toxin. Proc Nat Acad Sci. 2015; www.pnas.org/cgi/doi/10.1073/pnas.1503129112
  14. 14. Stentiford GD, Neil DM, Peeler EJ, Shields JD, Small HJ, Flegel TW, Vlak JM, Jones B, Morado F, Moss S, Lotz J, Bartholomay L, Behringer DC, Hauton C, Lightner DV. Disease will limit future food supply from global crustacean fishery and aquaculture sectors. J Invertebr Pathol. 2012; 110: 141–147. pmid:22434002
  15. 15. Oidtmann B, Peeler E, Lyngstad T, Brun E, Jensen BB, Stärk KDC. Risk-based methods for fish and terrestrial animal disease surveillance. Prevent Vet Med. 2013; 112: 13–26
  16. 16. Lightner DV, Redman RM, Pantoja CR, Tang KFJ, Noble BL, Schofield P, Mohney LL, Nunan LM, Navarro SA. Historic emergence, impact and current status of shrimp pathogens in the Americas. J Invertebr Pathol. 2012; 110: 174–183. pmid:22434000
  17. 17. Flegel TW. Historic emergence, impact and current status of shrimp pathogens in Asia. J Invertebr Pathol. 2012; 110:166–173 pmid:22429834
  18. 18. Shinn AP, Pratoomyot J, Bron JE, Paladini G, Brooker EE, Brooker AJ. Economic costs of protistan and metazoan parasites to global mariculture. Parasitol. 2014; 142: 196–270.
  19. 19. Lightner DV. Global transboundry disease politics: The OIE perspective. J Invertebr Pathol. 2012; 110: 184–187. pmid:22434003
  20. 20. Jones B. Transboundary movement of shrimp viruses in crustaceans and their products: A special risk? J Invertebr Pathol. 2012; 110: 196–200. pmid:22434004
  21. 21. Peeler EJ, Otte MJ. Epidemiology and economics support decisions about freedom from aquatic animal disease. Trans Emerg Dis. 2015; 63: 266–277.
  22. 22. Bentzon-Tilia M, Sonnenschein EC, Gram L. Monitoring and managing microbes in aquaculture—Towards a sustainable industry. Microb Biotechnol. 2016;
  23. 23. Karsenti E, Acinas SG, Bork P, Bowler C, De Vargas C, Raes J, Sullivan M, Arendt D, Benzoni F, Claverie J-M, Follows M, Gorsky G, Hingamp P, Ludicone D, Jaillon O, Kandels-Lewis S, Krzic U, Not F, Ogata H, Pesant S, Reynaud EG, Sardet C, Sieracki ME, Speich S, Velayoudon D, Weissenbach J, Wincker P, the Tara Oceans Consortium. A Holistic Approach to Marine Eco-Systems Biology. PLoS Biol 2011; 9: e1001177. pmid:22028628
  24. 24. Bass D, Stentiford GD, Littlewood T, Hartikainen H. Diverse applications of environmental DNA methods in parasitology. Trends Parasitol 2015; 31: 499–513. pmid:26433253
  25. 25. Gilbert JA, Quinn RA, Debelius J, Xu ZZ, Morton J, Garg N, Jansson JK, Dorrestein PC, Knight R. Microbiome-wide association studies link dynamic microbial consortia to disease. Nature 2016; 535: 94–103. pmid:27383984
  26. 26. De Schryver P, Defoirdt T, Sorgeloos P. Early mortality syndrome outbreaks: a microbial management issue in shrimp farming? PLoS Pathog 2014; 10: e1003919. pmid:24763380
  27. 27. Moriarty DJW. The role of microorganisms in aquaculture ponds. Aquaculture 1997; 151: 1–4.
  28. 28. De Schryver P, Defoirdt T, Sorgeloos P. Early mortality syndrome outbreaks: a microbial management issue in shrimp farming? PLoS Pathog 2014; 10: e1003919. pmid:24763380
  29. 29. Engel P, Kwong WK, McFrederick Q, Anderson KE, Barribeau SM, Chandler JA, Cornman RS, Dainat J, de Miranda JR, Doublet V, Emery O, Evans JD, Farinelli L, Flenniken ML, Granberg F, Grasis JA, Gauthier L, Hayer J, Koch H, Kocher S, Martinson VG, Moran N, Munoz-Torres M, Newton I, Paxton RJ, Powell E, Sadd BM, Schmid-Hempel P, Schmid-Hempel R, Song SJ, Schwarz RS, vanEngelsdorp D, Dainat B. The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions. MBio. 2016; 7: e02164–15. pmid:27118586
  30. 30. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, Piceno YM, DeSantis TZ, Andersen GL, Bakker PA, Raaijmakers JM. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science. 2011; 332: 1097–1100. pmid:21551032
  31. 31. Stentiford GD, Becnel J, Weiss L, Keeling P, Didier E, Williams B, Bjornson S, Kent M, Freeman MA, Brown MJF, Troemel E, Roesel K, Sokolova Y, Snowden KF, Solter L. Microsporidia—emergent pathogens in the global food chain. Trends Parasitol. 2015; 32, 336–348.
  32. 32. Gudding R, van Muiswinkel WB. A history of fish vaccination: Science-based disease prevention in aquaculture. Fish and Shellfish Immunology 2013; 35: 1683–1688. pmid:24099805
  33. 33. Fukushima HCS, Leal CAG, Cavalcante RB, Figueiredo HCP, Arijo S, Moriñigo MA, Ishikawa M, Borra RC, Ranzani-Paiva MJT. Lactococcus garvieae outbreaks in Brazilian farms Lactococcosis in Pseudoplatystoma sp.–development of an autogenous vaccine as a control strategy. J Fish Dis 2016;
  34. 34. Xia JH, Bai Z, Meng Z, Zhang Y, Wang L, Liu F, Jing W, Wan ZY, Li J, Lin H, Yue GH. Signatures of selection in tilapia revealed by whole genome resequencing. Sci Rep 2015; 5: 14168. pmid:26373374
  35. 35. Yu Y, Zhang X, Yuan J, Li F, Chen X, Zhao Y, Huang L, Zheng H, Xiang J. Genome survey and high-density genetic map construction provide genomic and genetic resources for the Pacific White Shrimp Litopenaeus vannamei. Sci Rep. 2015; 5: 15612. pmid:26503227
  36. 36. Korshkari P, Vaiwsri S, Flegel TW, Ngamsuriyaroj S, Sonthayanon B, Prachumwat A. ShrimpGPAT: a gene and protein annotation tool for knowledge sharing and gene discovery in shrimp. BMC Genom. 2014; 15: 506.
  37. 37. Aswad A, Katzourakis A. Paleovirology and virally derived immunity. Trends Ecol Evolut 2012; 27: 627–636.
  38. 38. Edvardsen RB, Leininger S, Kleppe L, Skaftnesmo KO, Wargelius A. Targeted mutagenesis in Atlantic salmon (Salmo salar L.) using the CRISPR/Cas9 system induces complete knockout individuals in the F0 generation. PLoS ONE 2014; 9: e108622. pmid:25254960
  39. 39. Perry KJ, Henry JQ. CRISPR/Cas9-mediated genome modification in the mollusc, Crepidula fornicata. Genesis. 2015; 53; 237–244. pmid:25529990
  40. 40. Martin A, Serano JM, Jarvis E, Bruce HS, Wang J, Ray S, Barker CA, O’Connell LC, Patel NH. CRISPR/Cas9 Mutagenesis Reveals Versatile Roles of Hox Genes in Crustacean Limb Specification and Evolution. Current Biology. 2016; 26: 14–26 pmid:26687626
  41. 41. van Houte S, Ekroth AKE, Broniewski JM, Chabas H, Ashby B, Bondy-Denomy J, Gandon S, Boots M, Paterson S, Buckling A, Westra ER. The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 2016;
  42. 42. Medzhitov R, Schneider DS, Soares MP. Disease Tolerance as a Defense Strategy. Science. 2012; 335: 936–941. pmid:22363001
  43. 43. Verbruggen B, Bickley LK, Santos EM, Tyler CR, Stentiford GD, Bateman KS, van Aerle R. de novo assembly of the Carcinus maenas transcriptome and characterization of innate immune system pathways. BMC Genomics. 2015; 16: 458. pmid:26076827
  44. 44. Tsai HY, Robledo D, Lowe NR, Bekaert M, Taggart JB, Bron JE, Houston RD. Construction and annotation of a high density SNP linkage map of 1 the Atlantic salmon (Salmo salar) genome. G3 Genes, Genomes and Genetics. 2016;
  45. 45. Nir O. What are Production Diseases, and How do We Manage Them? Acta Vet Scand. Suppl. (2003); 98: 21–32.
  46. 46. Cock J, Salazar M, Rye M. Strategies for managing disease in non-native shrimp populations. Rev Aquacult 2015;
  47. 47. Hindson BJ, Makarewicz AJ, Setlur US, Henderer BD, McBride MT, Dzenitis JM. APDS: the autonomous pathogen detection system. Biosensors and Bioelectronics 2005; 20, 1925–1931. pmid:15741059