TREPAR-1331; No. of Pages 7

The butterfly effect: parasite diversity,environment, and emerging disease inaquatic wildlifeRobert D. Adlard1, Terrence L. Miller2, and Nico J. Smit3

1 Natural Environments Program, Queensland Museum, South Brisbane, QLD 4101, Australia2 School of Marine and Tropical Biology, James Cook University, Cairns, QLD 4870, Australia3 Unit for Environmental Sciences and Management, North-West University, Potchefstroom 2520, South Africa

Review

Aquatic wildlife is increasingly subjected to emergingdiseases often due to perturbations of the existing dy-namic balance between hosts and their parasites. Accel-erating changes in environmental factors, together withanthropogenic translocation of hosts and parasites, actsynergistically to produce hard-to-predict disease out-comes in freshwater and marine systems. These out-comes are further complicated by the intimate linksbetween diseases in wildlife and diseases in humansand domestic animals. Here, we explore the interactionsof parasites in aquatic wildlife in terms of their biodiver-sity, their response to environmental change, theiremerging diseases, and the contribution of humans anddomestic animals to parasitic disease outcomes. Thiswork highlights the clear need for interdisciplinaryapproaches to ameliorate disease impacts in aquaticwildlife systems.

Connectivity of aquatic wildlife parasitesIt is intuitive that aquatic wildlife systems do not exist asdiscrete units but rather they interact seamlessly withneighbouring environments through a variety of inputsand outputs that together create a dynamic ecosystem.Although this overarching statement is undeniable andholds true for all sectors of the environment, it is onlyrecently that the intimate links between diseases in wild-life and diseases in humans and domestic animals havebeen emphasised [1,2]. These observations have promptedtransdisciplinary approaches in surveillance, health as-sessment, and monitoring to provide predictive modelsallowing timely response to the emergence of disease[3]. Such approaches should ideally also provide earlyindicators of environmental changes that may impact eco-system health.

A review on parasitic zoonoses and wildlife [4] focussedfurther attention on the complex interplay between humanand wildlife diseases through the One Health interactiontriad and proposed that research into parasite biodiversityin wildlife should not only provide an inventory of parasites,

1471-4922/

� 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2014.11.001

Corresponding author: Adlard, R.D. (robert.adlard@qm.qld.gov.au).Keywords: aquatic parasites; wildlife; biodiversity; environment; emerging disease.

but also include an assessment of the impacts that suchpathogens may have on nonwildlife hosts. Equally, similarconsideration should be given to the contraflow of human ordomestic animal parasites and how they may affect wildlifehealth.

The aquatic ecosystem, central to this review, is broadlydivided in freshwater and marine components. Althoughthe former accounts for only 0.8% of global surface area, itis critical to the survival of many organisms, and is subjectto some of the most ecosystem-altering perturbations [1].By contrast, the marine component covers 71% of the globe,but it too shows recent and relatively rapid environmentalchanges and acts as the final sink for land-based inputsthat impact initially on biodiverse coastal ecosystems.

A survey of the literature shows that parasitologistshave focussed their studies on aquatic wildlife throughseveral drivers that include: biodiversity stocktakes; iden-tification of causative agents in events of aquatic wildlifemortality and morbidity; focussed prevention and remedi-ation attempts for aquatic parasites pathogenic in bothaquaculture and harvest fisheries; multidirectional aquat-ic parasite flow between wildlife and aquaculture; andcurrent and projected impacts of often anthropogenic en-vironmental change on the incidence, prevalence, andpathogenicity of aquatic parasites. Given these drivers,we have framed this review to cover aquatic parasites interms of their biodiversity, response to environmentalchange, and emerging diseases and disease interactionswith nonwildlife species.

Biodiversity of aquatic parasitesParasites are extraordinarily diverse in aquatic ecosys-tems, where parasitism likely first arose, long before ter-restrial life came into existence. Evidence for such anancient association is increasingly recognised in the fossilrecord through distinct pathology or morphologically in-duced change that parasites cause to their long-dead hosts[5]. The vast diversity and richness of parasites we observetoday in aquatic systems reflects this long evolutionaryhistory, with representatives of nearly all known parasiticlineages of life found in marine and freshwater environ-ments [6]. Among the most biodiverse parasites knownfrom aquatic ecosystems are the cestodes, monogeneans,trematodes, and myxozoans, with thousands of species

Trends in Parasitology xx (2014) 1–7 1

Review Trends in Parasitology xxx xxxx, Vol. xxx, No. x

TREPAR-1331; No. of Pages 7

known from eachgroup[7]. Many protozoan parasite groupsare potentially more diverse than the metazoan groupslisted above, but have not yet received the same focussedtaxonomic scrutiny [8–14]. Knowledge of this diversityunderpins our efforts to examine and characterise in detailthe intricate ecology, life cycles, pathological impacts, andevolution of parasites and their hosts in aquatic systems.However, even addressing what parasite species exist in anycomplex aquatic ecosystem is a daunting task in itself.

How many parasites exist in the aquatic ecosystems of

the world?

Recent efforts to estimate the number of parasite speciesthat exist worldwide highlight the difficulties and limita-tions involved in producing robust estimates and the over-whelming task it is to formally characterise the fauna.Similar to prokaryotic organisms, the genetic, ecological,and biological boundaries that constitute some asexuallyand sexually reproducing eukaryotic parasite ‘species’ areoften unclear. Biologists [15,16] have debated the limita-tions of the ‘biological species concept’, focussing on threeelements of concern: (i) taxonomy; (ii) evolution; and(iii) biological diversity assessment, which has led to thedesignation of an entire field within taxonomy, ‘Eidonomy’,which seeks to address the ‘species problem’ [17]. What isclear from the ongoing debate on species definition is that itwill likely require whole genomics, informatics technolo-gies, and systems analyses that lie far in the future toadequately address the ‘species problem’ and facilitateconsensus among biologists.

Species have been described as being as fundamental tobiology as the elements are to chemistry [18]. This is aneloquent analogy, but based on some estimates [18,19],5 � 3 million species exist on Earth today, of which only1.5 million are formally named, further highlighting the gapto fill before we have as comprehensive an understanding ofthe biological world as our colleagues do of the chemicalworld. Our lack of knowledge of the basic ‘elements’ isparticularly emphasised when attempting to estimate thebiodiversity of parasite taxa [20–22]. Poulin examined ourcurrent understanding of parasite biodiversity [22] by ex-ploring: how many parasite species and active parasitetaxonomists are there? And, how does parasite diversityvary across host space and across geographical space?Our understanding of these questions has been fundamen-tally changed in many ways by recent genetic technologiesand analyses, which have revealed a vast diversity of crypticparasite taxa, as well as detailed information about hostspecificity, life cycles, and pathology [22,23]. Poulin pointsout that, despite all we do know about the diversity ofparasites, we cannot currently estimate how many parasitespecies exist with any accuracy in relative or absolute terms[22]. This holds true even for some of the most taxonomicallyscrutinised parasite groups inhabiting complex aquatic eco-systems (e.g., trematodes of Great Barrier Reef fishes);however, key patterns are emerging that help answer thequestions explored by Poulin [20–22].

Ways forward?

Documenting and preserving the biodiversity of the worldis a pressing issue, given the threats to many species and

2

ecosystems from a rapidly changing climate, invasive spe-cies, and anthropomorphic impacts, some of which we coverhere [18]. Parasite taxonomy and systematics provide afoundation for our understanding of parasitism in aquaticecosystems [16,24–29]. However, characterising this diver-sity requires substantial human and monetary resources,so most research into the foreseeable future will undoubt-edly continue to focus on parasites of human or commercialsignificance [18,22,26,30,31]. Nonetheless, efforts are be-ing directed towards accelerating and streamlining taxo-nomic discovery, dissemination, and database compilation,leading to initiatives such as ‘cybertaxonomy’ or ‘evolution-ary informatics’ [26,28,29,32,33]. It is clear that we do nothave the expertise, technology, and resources to formallydocument and characterise the entire parasite fauna of theaquatic ecosystems of the world. Perhaps an achievablegoal for those of us working on aquatic parasites is to makeconcerted efforts to preserve and lodge as many parasitesamples (DNA or whole specimens) as possible into long-term collections (e.g., museums). Preserving more than ascientific description, specimen, or short DNA sequenceagainst future need will help contribute snapshot knowl-edge of the rich diversity of parasitic life in the aquaticecosystems of the world [17–19,22,24–26,28,30,33–39].Given the current actual and potential threats to speciesinhabiting aquatic ecosystems, it is imperative that such aprocess be initiated now.

Environmental changeAlthough heavily debated throughout the previous centu-ry, the potential threat of global climate change to livingorganisms on Earth is now indisputable [40]. The predictedincrease in global temperatures has direct abiotic as wellas indirect biological consequences. The latter includesshifts in species distribution, timing of reproduction,change in physiological functioning, and change in inter-specific relationships [41]. Given the nature and complexi-ty of the parasitic lifestyle, parasites are, as a group, one ofthe most susceptible to global climate change. This effect isfurther exacerbated due to parasites usually exhibiting anarrow environmental tolerance and a tight trophic depen-dency. Parasites of aquatic organisms are sensitive totemperature change [42], because it directly impacts theirlife cycle, transmission, and host biology. In addition, italso influences their biodiversity and geographical distri-bution, with both these directly linked to that of theirhosts. To date, the main focus of research related to theprediction of the effect of global climate change on aquaticparasites was on vector-borne diseases of humans, withlimited information available on the implication of climatechange on parasites of wildlife [42].

Climate change: biodiversity and distribution

Parasites are usually excluded from general biodiversitysurveys of aquatic ecosystems; however, the parasitic spe-cies might in fact constitute half of all biodiversity [43]. Fur-thermore, despite the bad press that parasites usuallyreceive, it has been shown [44] that a parasite-rich ecosys-tem equals a healthy one. Thus, it is of utmost importancethat we consider the influence of environmental change onaquatic parasite biodiversity and distribution, because

Review Trends in Parasitology xxx xxxx, Vol. xxx, No. x

TREPAR-1331; No. of Pages 7

changes in both will affect ecosystem health. Both parasitediversity and distribution are closely linked to that of thehost; thus, any change in the conservation status and/ordistribution of the host will directly impact that of theparasite. For example, the threat of global temperatureincrease to brown trout, Salmo trutta, has been demon-strated [45]. This species in turn is host to at least 46 spe-cies of helminths, excluding any of the other parasiticgroups, such as crustaceans and protozoans [46]. Thethreat of local extirpation due to temperature increaseto this host species is also a major threat to at least someof its parasites.

It is generally accepted that temperature increase hap-pens fastest at the polar and boreal regions [41]. Thisresults in a general shift of parasite distribution north-wards, resulting in a change in distribution but not neces-sarily an increase in geographic range [47]. The bestexample of this is the northward expansion along theAtlantic coast of North America of the oyster parasitePerkinsus marinus [48]. This change in distribution dueto increase in water temperature was originallyhypothesised [49], then more recently tested and subse-quently supported [50].

Climate change impact on aquatic hosts

Shifts in parasite geographical range due to climate changebring parasites into contact with potential immunological-ly naıve hosts. To understand the potential impact ofparasites due to host switching, one only has to considerthe devastating effect of parasites that were introducedwith their non-native hosts into aquatic systems all overthe world. For example, in Europe, the swim bladdernematode (Anguillicoloides crassus) switched hostsfrom the introduced Asian eel (Anguilla japonica) to wildEuropean eels (Anguilla anguilla), causing significantmortalities among wild stock [51]. Host switching in themarine environment is less studied, but does exist. Forexample, the rhizocephalan barnacle, Loxothylacus pano-paei, which is native to the Gulf of Mexico and southernFlorida, was introduced to Chesapeake Bay on the AtlanticCoast of the USA in 1964, where it now parasitises threecrab species [52]. Parasite pathogenicity to the host canalso be amplified as a result of increased temperature. Forexample, outbreaks in California of the parasitic copepodLernaea cyprinacea, which causes serious malformationsin foothill yellow-legged frogs (Rana boylii), was directlylinked to unusually warm summers [53].A laboratory studyof rainbow trout, Oncorhynchus mykiss, infected with theprotist, Ichthyophonus sp., demonstrated more rapid onsetof the disease and more severe host reaction at highertemperatures [54]. Parasites, as poikilotherms, react toan increase in temperature by accelerating growth rates,development, and maturation[55], and likely complete evencomplex lifecycles much quicker than at lower temperatures[42]. Thus, the potential effect of climate change on parasiticlife cycles is one of the most important aspects to considerwhen modelling or predicting future change.

Environmental change and aquatic parasite life cycles

Life cycles of parasites of aquatic animals range fromdirect (e.g., monogeneans and some crustaceans), single

intermediate host or vector (e.g., blood protozoa) to multi-ple intermediate hosts and free-living stages (e.g., hel-minths). The sheer complexity of their life history makespredictions on how they will respond to environmentalchange difficult. Fish parasitic isopods from the familyGnathiidae have parasitic juveniles and free-living adultswith life cycles that range from 2 years in the polar region,to 1 year in temperate regions, and 2 months at the tropics[56,57]. These parasites have also been implicated asvectors of blood protozoa [58,59]. With life-cycle lengthseemingly dependent on temperature, a warming environ-ment can shorten the life-cycle duration and also the rate ofblood parasite transmission. In trematodes, the effects ofhigher temperature on all the different life stages are wellstudied. Increase in host (snail) metabolic activity, due tohigher temperatures, enhances cercarial production and,thus, cercarial output, one of the key components of thetransmission success of a trematode [60,61]. In the marineenvironment, aquatic parasite life cycles often depend onthe synchronicity of the parasite and host populationdynamics, where the parasites require a brief seasonaloverlap of their definitive and intermediate hosts[42]. The cestode, Triaenophorus crassus, depends on thebrief overlap of its definitive host (pike), and two interme-diate hosts (a copepod and coregonid fish) during the firstmonths of summer in shallow coastal waters. If climatechange results in a breakdown in synchronicity in thepresence of the three hosts, it can lead to a disruption ofthe life cycle of the parasite and potential extinction of itslocal population [42].

Thus, it is clear that the effects of environmental changeon the parasites of aquatic animals are not straight for-ward or easy to predict, which further complicates futureconservation and management plans, specifically relatedto disease outbreaks in the aquatic environment. It isparticularly imperative that future research focusses onthe role of changing temperature in the life cycles ofaquatic parasites coupled with holistic studies of host–parasite interactions.

Emerging disease in aquatic wildlife and associatedinteractionsThe emergence of parasitic disease in aquatic wildlife isdriven largely by environmental, ecological, and socioeco-nomic factors. An analysis of global reports of emergingdisease in farmed fish and shellfish revealed that 80% ofreports originate from developed countries (dominated byreports from Europe and North America), which contributeless than 6% to global production in aquaculture, whilemany reports (48%) focus on disease in salmonids eventhough they represent only 12% of global production[62]. Such reporting bias is similarly reflected in an analy-sis of human emerging disease with events concentrated inhigher latitudes [63]. In both cases, the bias reflects aconcentration of effort in research and surveillance inwealthier, developed countries, a condition that is likelyfurther accentuated for reports of emerging diseases ofaquatic wildlife.

Parasite introduction through infected host transloca-tions, spillover infections from domestic animals into wildpopulations, and changing environmental conditions that

3

Review Trends in Parasitology xxx xxxx, Vol. xxx, No. x

TREPAR-1331; No. of Pages 7

act to increase the prevalence and virulence of existing, orfacilitate new, disease, can all act either individually orsynergistically to cause emerging disease in aquatic wild-life [64,65].

There are some classical examples of translocation andspillover into aquatic wildlife populations in both finfishand shellfish. Myxobolus cerebralis, the agent of salmonidwhirling disease, spread globally from Europe through thetranslocation of infected fish but was able to colonise newlocalities only due to the global distribution of its otherobligate host, the aquatic tubificid worm [66]. The severityof the impact on wild fish populations was spectacular,with local extinctions in rivers of the Pacific northwest ofthe USA and elsewhere. Decades after the initial translo-cation, there are now renewed attempts to establish ge-netically resistant strains of rainbow trout that may givewild stocks the opportunity to return to somethingapproaching their former levels [67]. Equally devastating,and again demonstrating anthropogenic translocation foraquaculture spilling over to wild populations, was theemergence of the microcell parasite Bonamia ostreae inthe European flat oyster, Ostrea edulis. The parasite origi-nated in California, where it infected O. edulis that hadpreviously been translocated to the USA, then the infectionwas presumably moved back to Europe (France) with spatfrom a Californian hatchery (i.e., an endemic species com-ing back to its original home having been outside itsgeographic range) [68]. This clearly demonstrates that areturned endemic species poses the same risk as an exoticand can transmit severe infection to local cultured and wildstocks [65]. Bonamia ostreae then spread to all Europeanstocks of O. edulis, again either by translocation for cultureor through transport of infected oysters fouling the hullsof ships, the parasite became established in wild stocksof oysters, where it continues to exist as a reservoir ofinfection.

The devastating impact of chytridiomycosis in amphi-bians was triggered by a drying climate in Costa Rica thatlimited the area of optimal moist habitat, increased amphib-ian density, and, thus, increased encounters facilitatingtransmission of the fungal pathogen, Batrachochytriumdendrobatidis. Indeed, this is considered a compelling caseof a climate-driven disease as an immediate threat to wild-life biodiversity [69]. Following the outbreak in CentralAmerica, there followed a catastrophic decline in amphi-bians in both Central America and Australia, with a patternof infection consistent with the introduction of a virulentpathogen into a naıve population [70]. Recently, it wasshown [71] that Australian amphibian populations werealso subject to myxozoan parasite infections , which mayexplain population losses in chytrid-free areas. The inva-sive cane toad (Rhinella marinum) acquires and sharesnative amphibian myxozoans and then becomes a sourceof spillback infections to wildlife after developing a highprevalence of disease (up to 42%) ; that is, the introducedinvasive host amplifies the infection , causing loss of en-demic wildlife [71]. In locations currently free of invasivecane toads, alternative pathways of infection have beenidentified and include anthropogenic movement of fruitboxes together with infected frogs to southern Australianmarkets [72].

4

In 1998, significant mortality and morbidity wasreported in Chinook salmon [73] being cultured in Cali-fornia to supplement stocks of this endangered fish. A‘rosette agent’ was isolated that caused systemic inflam-mation and granulomatous lesions in a variety of tissues ofinfected individuals. The infectious organism was mostlikely shed into the water via urine or through the intes-tine, gills, skin, and spawning fluids. Experimental infec-tions established that virulence was high in Chinook andCoho salmon with rainbow, brown, and brook trout show-ing infection but less susceptibility to this agent. The agentgrew slowly after initial infection and was not easilyidentified in young fish by histological methods, raisingthe concern that many infected individuals would not beeasily recognised [73]. A few years later [74], it wasreported that populations of the European endemic cypri-nid, Leucaspius delineatus (sunbleak), were suffering mor-tality and almost complete inhibition of spawning due to anintracellular ‘rosette agent’. It appears that the invasiveAsian topmouth gudgeon, Pseudorasbora parva, intro-duced decades before and rapidly spread throughoutEurope, is a healthy carrier of the infectious agent nowconfirmed to be Sphaerothecum destruens [75]. Theseevents highlight an emerging pathogen that combinesthe following attributes: broad host specificity (salmonids,cyprinids); difficulty of diagnosis in early infections; isrelatively benign in some species, which can then act asreservoir hosts; being translocated with an invasive hostinto naıve populations; and has severe impacts on bothaquaculture of finfish and endemic fish biodiversity. Clear-ly, understanding the epidemiology of such generalistpathogens is critical to our understanding and manage-ment of emerging disease.

In a study of the parasite fauna of 40 exotic species, themost dominant parasites (67%) were spillback infectionsfrom endemic hosts to exotic hosts, with 70% of exotic hostsacquiring four or more endemic species of parasite. Equallyconcerning is that 38 of the 40 hosts assessed had acquiredparasites that were generalists (i.e., had relatively low hostspecificity) [76]. Invasive exotic hosts, such as the cane toadand the topmouth gudgeon mentioned above, not onlyprovide an effective increased density of susceptible hoststo maintain pathogen populations, but can also mask aninfection through controlling pathogen intensity at lowlevels, thus confounding diagnosis of such infections.

The last example of translocation that we review hereinvolves the only finfish parasite listed as notifiable by theOffice Internationale des Epizooties, the emergence ofthe fish pathogenic monogenean, Gyrodactylus salaris, inEurope following introduction to Norway from Sweden.The impacts of this translocation have been the subjectof many publications and reviews (see [77] for a compre-hensive coverage of the parasite and [78] for its use as anexample of import risk assessment) but of interest in thiscontext is that G. salaris was first described from Atlanticsalmon (Baltic strain) in Sweden without reports of severedisease. The parasite appeared to be acting as though ithad reached a dynamic balance with its host, presumablyas a result of a long host–parasite history with selectionpressure favouring low pathogenicity towards the hostand low virulence of the parasite. Even though Atlantic

Review Trends in Parasitology xxx xxxx, Vol. xxx, No. x

TREPAR-1331; No. of Pages 7

salmon in Norway (Atlantic strain) fulfils the biologicalrequirements to be considered the same taxonomic species(i.e., Salmo salar), introduction of G. salaris to a naıvestock of genetically separate Atlantic salmon resulted inhigh virulence, high susceptibility, and severe disease[65]. The clear message from this example, and from there-introduction of O. edulis infected with B. ostreae fromthe USA back into Europe, is that while taxonomicconspecificity of the host may prevent the introduction ofexotic invasive animals, it does not equate to zero risk fordisease introduction. Past provenance and genetic driftthrough stock separation are powerful forces that impacthost–pathogen interactions.

These and other studies suggest that the major pathwayfor emerging disease in aquatic wildlife is anthropogenictranslocation of infected hosts for aquaculture. Other casesof disease emergence in aquatic systems have beenreviewed elsewhere [1,70,79,80], and a review of diseasein Asian aquaculture suggests that 25–30 infectious agentshave already been translocated into southeast Asiathrough the increased globalisation of trade in live aquaticanimals and their products and through the expansion ofthe ornamental fish trade [81]. Recently, it was estimatedthat international trade for the aquarium industry movesover 1 billion ornamental fish per year between the100 countries involved in the trade, providing a broadpathway for the incursion of exotic pathogens togetherwith the potential for establishment of invasive exoticspecies of fish [82]. Such hosts, if susceptible to endemicaquatic pathogens, could provide an increased populationfor infection or, conversely, could become a parasite sink ifparasite life cycles are not viable in that host.

As emphasised in the preceding cases, the emergence ofnew disease, or re-emergence of known disease in a morevirulent form, in the aquatic environment is indisputablylinked to human activity, which in turn can have signifi-cant impact on aquatic wildlife populations and aquaticbiodiversity. It has been demonstrated [83] that intensivefarming (e.g., aquaculture) provides a powerful evolution-ary selection on parasites towards faster maturation, ear-lier transmission, and, thus, probably higher virulence. Atthe start of this review, we highlighted the movementtowards a whole-system approach that incorporated con-cepts such as One Health; now, with the addition of suchpowerful, short-term evolutionary mechanisms, the chal-lenge appears to be defining the margins of what actuallyconstitutes the ‘whole system’.

Concluding remarksIn this review, we focussed on the extraordinary parasiticdiversity of aquatic systems and the challenges posed ineven defining what species exist, let alone in recognisingtheir potential impacts in an environment where biologicaland physicochemical characters are changing at an unprec-edented rate and parasitic disease events are increasing infrequency. Accurate and unambiguous identification ofpathogens (morphological and molecular taxonomy andsystematics) is a critical starting point for wildlife manage-ment. However, also required is information on geographicrange, transmission, host specificity, pathogenicity, andenvironmental tolerances, to provide mechanisms for the

control of these disease agents. Furthermore, any attemptsat aquatic biosecurity control require capacity to recogniseendemic and exotic parasites, a significant task, particularlyin regions of high diversity. Indeed, recent syntheses havesuggested that most emerging disease will conform to bio-diversity gradients that increase towards the tropics [63],where research effort is low. As a corollary, legislativearrangements for the control of disease should recognisebiological ecosystem boundaries rather than political jur-isdictions to enable meaningful control strategies [65].

It is also clear that the environmental changes in eco-systems have profound and unpredictable impacts onaquatic wildlife that may then threaten biodiversity andbe intimately connected to human health and wellbeing[2]. Changes can be as simple and direct as infective stagesof proliferative kidney disease of fish emerging frombryozoans due to increasing temperatures [79] or, morecomplex, such as chemical pollutants accumulating atsubclinical levels that can then increase host susceptibili-ty. In semifield trials, it was demonstrated that whenherring from polluted coastal areas were fed on by a groupof seals, it resulted in quantifiably impaired immunologicalfunction in the seals due to chronic exposure to persistentlipophilic chemical pollutants [84]. Equally, aquatic para-sites themselves, particularly ectoparasites of fishes andparasite life stages exposed to the environment, are sus-ceptible to toxic pollutants [85] and temperature changes,with downstream effects that potentially alter populationparameters of their hosts. Parasites of wild aquatic ani-mals are a natural and constant presence where theyprovide population regulation (e.g., through impacts onfecundity and mortality of fish in even pristine habitats[86,87]) with disease sustained at ‘background’ levels[44,79]. When such population regulatory factors change,shifts in the host–parasite interaction can either producesignificant emergent disease or break a parasite cycle withconcomitant destabilising effects for the host populationnow freed from a powerful regulatory force.

Whether aquatic wildlife disease pathways involveamplified transmission from aquaculture or through an-thropogenic translocation of parasites, and whether envi-ronmental change has augmented the severity directly orthrough affecting host susceptibility, once a parasitic dis-ease enters a wild population it is generally consideredimpossible either to control or to eradicate [65]. Theresponses of aquatic wildlife to such an incursion may thenrun the spectrum from catastrophic population decline topermanent maintenance of pathogens at low pathogenicityand low prevalence, rendering the disease agent undetect-able, but providing a reservoir of infection for future trans-mission [76].

Data from the Food and Agriculture Organisation of theUN show that aquaculture production has climbed from2006 to 2012, from just over 52% to almost 73% of capturefishery production, a trend that is likely to continue toaccelerate. With such socioeconomic pressures on food pro-duction, host and parasite translocations will increase pro-portionally and the potential for emergence of parasiticdisease in aquatic wildlife will grow to unprecedented levels.Understanding pathogen interactions and recognising the‘butterfly effect’, the complex but intimate associations of

5

Review Trends in Parasitology xxx xxxx, Vol. xxx, No. x

TREPAR-1331; No. of Pages 7

wildlife, domestic animals, and human health, are criticalfor our future wellbeing.

References1 Johnson, P.T.J. and Paull, S.H. (2011) The ecology and emergence of

diseases in fresh waters. Freshwater Biol. 56, 638–6572 Daszak, P. et al. (2001) Anthropogenic environmental change and the

emergence of infectious diseases in wildlife. Acta Trop. 78, 103–1163 Aguirre, A.A. and Tabor, G.M. (2008) Global factors driving emerging

infectious diseases impact on wildlife populations. In AnimalBiodiversity and Emerging Diseases: Prediction and Prevention(Sparagano, O.A.E. et al., eds), pp. 1–3, Wiley

4 Thompson, R.C.A. (2013) Parasite zoonoses and wildlife: one health,spillover and human activity. Int. J. Parasitol. 43, 1079–1088

5 Klompmaker, A.A. et al. (2014) Parasites in the fossil record: a cretaceousfauna with isopod-infested decapod crustaceans, infestation patternsthrough time, and a new ichnotaxon. PLoS ONE 9, e92551

6 Rohde, K. (2005) Marine Parasitology, CSIRO Publishing7 WoRMS (2014) World Register of Marine Species, WoRMS8 Abdelmohsen, U.R. et al. (2014) Actinomycetes from Red Sea sponges:

sources for chemical and phylogenetic diversity. Mar. Drugs 12,2771–2789

9 Berney, C. et al. (2013) Vampires in the oceans: predatory cercozoanamoebae in marine habitats. ISME J. 7, 2387–2399

10 Hartikainen, H. et al. (2014) Lineage-specific molecular probing revealsnovel diversity and ecological partitioning of haplosporidians. ISME J.8, 177–186

11 Kagami, M. et al. (2014) Mycoloop: chytrids in aquatic food webs. Front.Microbiol. 5, 166

12 Lepelletier, F. et al. (2014) Dinomyces arenysensis gen. et sp. nov.(Rhizophydiales, Dinomycetaceae fam. nov.), a chytrid infectingmarine dinoflagellates. Protist 165, 230–244

13 Lepelletier, F. et al. (2014) Parvilucifera rostrata sp. nov. (Perkinsozoa),a novel parasitoid that infects planktonic dinoflagellates. Protist 165,31–49

14 Neuhauser, S. et al. (2014) Cross-kingdom host shifts of phytomyxidparasites. BMC Evol. Biol. 14, 33

15 de Meeus, T. et al. (2003) Species concepts: what for? Trends Parasitol.19, 425–427

16 de Meeus, T. et al. (2004) Response to Vilas and Paniagua: analyzingthe structure of biodiversity. Trends Parasitol. 20, 258–259

17 Dubois, A. (2011) Species and ‘strange species’ in zoology: do we need a‘unified concept of species’? C. R. Palevol 10, 77–94

18 Costello, M.J. et al. (2013) Can we name earth’s species before they goextinct? Science 339, 413–416

19 Appeltans, W. et al. (2012) The magnitude of global marine speciesdiversity. Curr. Biol. 22, 2189–2202

20 Cribb, T. et al. (2014) Trematodes of the Great Barrier Reef: emergingpatterns of diversity and richness in coral reef fishes. Int. J. Parasitol.44, 929–939

21 Dobson, A. et al. (2008) Homage to Linnaeus: how many parasites? Howmany hosts? Proc. Natl. Acad. Sci. U.S.A. 105, 11482–11489

22 Poulin, R. (2014) Parasite biodiversity revisited: frontiers andconstraints. Int. J. Parasitol. 44, 581–589

23 Miller, T.L. et al. (2011) Taxonomic approaches to and interpretation ofhost specificity of trematodes of fishes: lessons from the Great BarrierReef. Parasitology 138, 1710–1722

24 Guralnick, R.P. et al. (2012) It’s not about technology, but communitypractice: a response to Scotland and Wood. Trends Ecol. Evol. 27, 417–418

25 Joppa, L.N. et al. (2012) Taxonomy that matters: response to Bacher.Trends Ecol. Evol. 27, 66

26 Pimm, S.L. (2012) Biodiversity: not just lots of fish in the sea. Curr.Biol. 22, R996–R997

27 Pimm, S.L. et al. (2014) The biodiversity of species and their rates ofextinction, distribution, and protection. Science 344, 987

28 Scheffers, B.R. et al. (2012) What we know and don’t know aboutEarth’s missing biodiversity. Trends Ecol. Evol. 27, 501–510

29 Sluys, R. (2013) The unappreciated, fundamentally analytical nature oftaxonomy and the implications for the inventory of biodiversity. Biodiv.Conserv. 22, 1095–1105

30 Vilas, R. and Paniagua, E. (2004) Analyzing the structure ofbiodiversity. Trends Parasitol. 20, 257–258

6

31 Wood, C.L. et al. (2014) Fishing drives declines in fish parasitediversity and has variable effects on parasite abundance. Ecology95, 1929–1946

32 Maddison, D.R. et al. (2012) Ramping up biodiversity discovery viaonline quantum contributions. Trends Ecol. Evol. 27, 72–77

33 Parr, C.S. et al. (2012) Evolutionary informatics: unifying knowledgeabout the diversity of life. Trends Ecol. Evol. 27, 94–103

34 Brooks, D.R. and Hoberg, E.P. (2001) Parasite systematics in the 21stcentury: opportunities and obstacles. Trends Parasitol. 17, 273–275

35 Costello, M.J. et al. (2014) Strategies for the sustainability of onlineopen-access biodiversity databases. Biol. Conserv. 173, 155–165

36 Cribb, T.H. and Bray, R.A. (2011) Trematode families and genera: havewe found them all? Trends Parasitol. 27, 149–154

37 Favret, C. (2014) Cybertaxonomy to accomplish big things in aphidsystematics. Insect Sci. 21, 392–399

38 Kunz, W. (2002) When is a parasite species a species? Trends Parasitol.18, 121–124

39 McKenzie, F.E. (2001) Biodiversity strikes home. Trends Parasitol. 17,263

40 Karvonen, A. et al. (2010) Increasing water temperature and diseaserisks in aquatic systems: Climate change increases the risk of some, butnot all, diseases. Int. J. Parasitol. 40, 1483–1488

41 Pickles, R.S.A. et al. (2013) Predicting shifts in parasite distributionwith climate change: a multitrophic level approach. Global ChangeBiol. 19, 2645–2654

42 Marcogliese, D.J. (2001) Implications of climate change for parasitismof animals in the aquatic environment. Can. J. Zool. 79, 1331–1352

43 Toft, C.A. (1986) Communities of parasites with parasitic life-styles. InCommunity Ecology (Diamond, J.M. and Case, T.J., eds), pp. 445–463,Harper & Row

44 Hudson, P.J. et al. (2006) Is a healthy ecosystem one that is rich inparasites? Trends Ecol. Evol. 21, 381–385

45 Almodovar, A. et al. (2012) Global warming threatens the persistence ofMediterranean brown trout. Global Change Biol. 18, 1549–1560

46 Poulin, R. and Mouillot, D. (2003) Host introductions and thegeography of parasite taxonomic diversity. J. Biogeogr. 30, 837–845

47 Lafferty, K.D. (2009) The ecology of climate change and infectiousdiseases. Ecology 90, 888–900

48 Lafferty, K. and Kuris, A. (2005) Parasitism and environmentaldisturbances. In Parasitism and Ecosystems (Thomas, F. et al., eds),pp. 113–123, Oxford University Press

49 Cook, T. et al. (1998) The relationship between increasing sea-surfacetemperature and the northward spread of Perkinsus marinus (Dermo)disease epizootics in oysters. Estuar. Coast. Shelf Sci. 46, 587–597

50 Ford, S.E. and Chintala, M.M. (2006) Northward expansion of a marineparasite: testing the role of temperature adaptation. J. Exp. Mar. Biol.Ecol. 339, 226–235

51 Kirk, R.S. (2003) The impact of Anguillicola crassus on European eels.Fish. Manag. Ecol. 10, 385–394

52 Torchin, M.E. et al. (2002) Parasites and marine invasions.Parasitology 124, S137–S151

53 Kupferberg, S.J. et al. (2009) Parasitic copepod (Lernaea cyprinacea)outbreaks in foothill yellow-legged frogs (Rana boylii) linked tounusually warm summers and amphibian malformations innorthern California. Copeia 529–537

54 Kocan, R. et al. (2009) Effects of temperature on disease progressionand swimming stamina in Ichthyophonus-infected rainbow trout,Oncorhynchus mykiss (Walbaum). J. Fish Dis. 32, 835–843

55 Magnuson, J.J. et al. (1997) Potential effects of climate changes onaquatic systems: Laurentian Great Lakes and Precambrian ShieldRegion. Hydrol. Process. 11, 825–871

56 Ferreira, M.L. et al. (2009) A new species of gnathiid (Crustacea:Isopoda) parasitizing teleosts from Lizard Island, Great BarrierReef, Australia. J. Parasitol. 95, 1066–1075

57 Smit, N.J. and Davies, A.J. (2004) The curious life-style of the parasiticstages of gnathiid isopods. Adv. Parasitol. 58, 289–391

58 Curtis, L.M. et al. (2013) Gnathia aureamaculosa, a likely definitivehost of Haemogregarina balistapi and potential vector forHaemogregarina bigemina between fishes of the Great Barrier Reef,Australia. Int. J. Parasitol. 43, 361–370

59 Davies, A.J. and Smit, N.J. (2001) The life cycle of Haemogregarinabigemina (Adeleina: Haemogregarinidae) in South African hosts. FoliaParasitol. 48, 169–177

Review Trends in Parasitology xxx xxxx, Vol. xxx, No. x

TREPAR-1331; No. of Pages 7

60 Mas-Coma, S. et al. (2009) Climate change effects on trematodiases,with emphasis on zoonotic fascioliasis and schistosomiasis. Vet.Parasitol. 163, 264–280

61 Studer, A. et al. (2010) Parasites and global warming: net effects oftemperature on an intertidal host-parasite system. Mar. Ecol. Prog.Ser. 415, 11–22

62 Thrush, M.A. et al. (2012) Monitoring emerging diseases of fish andshellfish using electronic sources. Transbound. Emerg. Dis. 59,385–394

63 Jones, K.E. et al. (2008) Global trends in emerging infectious diseases.Nature 451, 990–994

64 Harvell, C.D. et al. (1999) Review: Marine ecology: emerging marinediseases – climate links and anthropogenic factors. Science 285,1505–1510

65 Peeler, E.J. et al. (2011) Non-native aquatic animals introductionshave driven disease emergence in Europe. Biol. Invasions 13,1291–1303

66 Whipps, C.M. et al. (2004) Myxobolus cerebralis internal transcribedspacer 1 (ITS-1) sequences support recent spread of the parasiteto North America and within Europe. Dis. Aquat. Organ. 60,105–108

67 Fetherman, E.R. et al. (2014) Survival and reproduction ofMyxobolus cerebralis-resistant rainbow trout introduced to theColorado River and increased resistance of age-0 progeny. PLoSONE 9, e96954

68 Elston, R.A. et al. (1986) Occurence and significance of bonamiasis inEuropean flat oysters Ostrea edulis in North America. Dis. Aquat.Organ. 2, 49–54

69 Pounds, J.A. et al. (2006) Widespread amphibian extinctions fromepidemic disease driven by global warming. Nature 439, 161–167

70 Daszak, P. et al. (1999) Emerging infectious diseases and amphibianpopulation declines. Emerg. Infect. Dis. 5, 735–748

71 Hartigan, A. et al. (2011) A suspected parasite spill-back of two novelMyxidium spp. (Myxosporea) causing disease in Australian endemicfrogs found in the invasive cane toad. PLoS ONE 6, e18871

72 Hartigan, A. et al. (2012) Emerging myxosporean parasites ofAustralian frogs take a ride with fresh fruit transport. Parasit.Vectors 5, 208

73 Arkush, K.D. et al. (1998) Pathology associated with the rosette agent,a systemic protist infecting salmonid fishes. J. Aquat. Anim. Health 10,1–11

74 Gozlan, R.E. et al. (2005) Biodiversity: disease threat to European fish.Nature 435, 1046

75 Gozlan, R.E. et al. (2009) Identification of a rosette-like agent asSphaerothecum destruens, a multi-host fish pathogen. Int. J. Parasitol.39, 1055–1058

76 Kelly, D.W. et al. (2009) Parasite spillback: a neglected concept ininvasion ecology? Ecology 90, 2047–2056

77 Bakke, T.A. et al. (2007) The biology of gyrodactylid monogeneans: the‘Russian–doll killers’. Adv. Parasitol. 64, 161–376

78 Peeler, E.J. et al. (2007) The application of risk analysis in aquaticanimal health management. Prev. Vet. Med. 81, 3–20

79 Okamura, B. and Feist, S.W. (2011) Emerging diseases in freshwatersystems. Freshwater Biol. 56, 627–637

80 Poulin, R. et al. (2011) Biological invasions and the dynamics ofendemic diseases in freshwater ecosystems. Freshwater Biol. 56,676–688

81 Bondad-Reantaso, M.G. et al. (2005) Disease and health managementin Asian aquaculture. Vet. Parasitol. 132, 249–272

82 Whittington, R.J. and Chong, R. (2007) Global trade in ornamentalfish from an Australian perspective: the case for revised importrisk analysis and management strategies. Prev. Vet. Med. 81, 92–116

83 Mennerat, A. et al. (2010) Intensive farming: evolutionary implicationsfor parasites and pathogens. Evol. Biol. 37, 59–67

84 de Swart, R.L. et al. (1994) Impairment of immune function in harborseals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23,155–159

85 Lafferty, K.D. (2008) Ecosystem consequences of fish parasites.J. Fish Biol. 73, 2083–2093

86 Adlard, R.D. and Lester, R.J.G. (1994) Dynamics of the interactionbetween the parasitic isopod, Anilocra pomacentri, and the coral reeffish, Chromis nitida. Parasitology 109, 311–324

87 Adlard, R.D. and Lester, R.J.G. (1995) The life cycle and biology ofAnilocra pomacentri (isopoda, Cymothoidae), an ectoparasite isopodof the coral reef fish, Chromis nitida (Perciformes, Pomacentridae).Aust. J. Zool. 43, 271–281

7