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].