Tommy L. F. Leung

More rapid and severe disease outbreaks for aquaculture at the tropics: implications for food security

1. Aquaculture is replacing capture fisheries in supplying the world with dietary protein. Although disease is a major threat to aquaculture production, the underlying global epidemiological patterns are unknown. 2. We analysed disease outbreak severity across different latitudes in a diverse range of aquaculture systems. 3. Disease at lower latitudes progresses more rapidly and results in higher cumulative mortality, in particular at early stages of development and in shellfish. 4. Tropical countries suffer proportionally greater losses in aquaculture during disease outbreaks and have less time to mitigate losses. 5. Synthesis and applications. Disease can present a major problem for food production and security in equatorial regions where fish and shellfish provide a major source of dietary protein. As the incidences of some infectious diseases may increase with climate change, adaptation strategies must consider global patterns in disease vulnerability of aquaculture and develop options to minimize impacts on food production.

Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes

Abstract Parasites, in particular trematodes (Platyhelminthes: Digenea), play major roles in the population dynamics and community structure of invertebrates on soft‐sediment mudflats. Here, we provide a list of the 20 trematode species currently known to infect molluscs, crustaceans and polychaetes from Otago Harbour (New Zealand) soft‐sediment intertidal areas, as well as information on their transmission modes, life cycles, andknown ecological impacts. Several of the host‐parasite species combinations recorded here are reported for the first time. We also provide DNA barcodes, based on sequences of the cytochrome oxidase subunit l (CO1) gene, for 19 of the 20 trematode species, to facilitate future identification of these parasites in marine ecological studies.

The true cost of host manipulation by parasites.

If there is one thing that the past three decades of research in behavioural and evolutionary ecology have taught us, it is that there are no free lunches. Adaptive traits provide net fitness benefits to the animals bearing them, but the gains would be even greater if there were no concurrent costs associated with the expression of those traits. The ability of many parasites to enhance their transmission success by manipulating t 2 r a n m m T c e p I c F

Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae)

Abstract The cercariae and sporocysts (or rediae) of four trematode species are described from the intertidal snail Zeacumantus subcarinatus: a distome xiphidiocercaria assigned to the genus Renicola (family Renicolidae); a monostome xiphidiocercaria belonging either to the genus Microphallus or Megalophallus (family Microphallidae); a magnacercous cercaria of the genus Galactosomum (family Hetero‐phyidae); and a cercaria of the genus Philophthalmus (family Philophthalmidae). The morphological features of these cercariae are compared to previously described cercariae of the same genera. In addition, since the philophthalmid cercaria encysts readily on artificial substrates in the laboratory, the metacercaria of this species is also described. These cercariae are part of a diverse community of at least six digenean species parasitising the snail Z. subcarinatus that, together, have a major impact on the ecology and evolution of this snail.

Cryptic species complexes in manipulative echinostomatid trematodes : when two become six

SUMMARY Recent studies have shown that some digenean trematodes previously identified as single species due to the lack of distinguishing morphological characteristics actually consist of a number of genetically distinct cryptic species. We obtained mitochondrial 16S and nuclear ITS1 sequences for the redial stages of Acanthoparyphium sp. and Curtuteria australis collected from snails and whelks at various locations around Otago Peninsula, New Zealand. These two echinostomes are well-known host manipulators whose impact extends to the entire intertidal community. Using phylogenetic analyses, we found that Acanthoparyphium sp. is actually composed of at least 4 genetically distinct species, and that a cryptic species of Curtuteria occurs in addition to C. australis. Molecular data obtained for metacercariae dissected from cockle second intermediate hosts matched sequences obtained for Acanthoparyphium sp. A and C. australis rediae, respectively, but no other species. The various cryptic species of both Acanthoparyphium and Curtuteria also showed an extremely localized pattern of distribution: some species were either absent or very rare in Otago Harbour, but reached far higher prevalence in nearby sheltered inlets. This small-scale spatial segregation is unexpected as shorebird definitive hosts can disperse trematode eggs across wide geographical areas, which should result in a homogeneous mixing of the species on small geographical scales. Possible explanations for this spatial segregation of the species include sampling artefacts, local adaptation by first intermediate hosts, environmental conditions, and site fidelity of the definitive hosts.

Taxonomic resolution in parasite community studies: are things getting worse?

Species identification is crucial for studies of parasite diversity, yet most surveys include taxa identified only to genus or family level. Using a large dataset comprising 950 surveys of helminth communities from 650 different species of fish, bird and mammal hosts, we investigated what determines the level of taxonomic resolution achieved. Identification of all helminths down to species level was achieved in only one-third of surveys, whereas all taxa were identified at least to genus level in two-thirds of surveys. The species richness of a parasite community and past study effort on the host species did not correlate with taxonomic resolution. However, the higher the proportion of parasite taxa occurring as larvae in a community, the lower the resolution achieved. Also, taxonomic resolution was better overall for communities in birds or mammals than for those in fish, and better for trematodes and acanthocephalans than for cestodes and nematodes. Perhaps the most intriguing result was a clear significant effect of year of publication on the taxonomic resolution achieved in parasite surveys: the proportion of helminth taxa identified at least to genus level has remained high until the year 2000, but has dropped in studies published since then. The loss of expertize in parasite taxonomy happening worldwide is one possible explanation. This downward trend needs to be reversed if we are to monitor new parasite occurrences in the face of environmental changes.

Interactions between parasites of the cockle Austrovenus stutchburyi : hitch-hikers, resident-cleaners, and habitat-facilitators

The patterns of association between parasites within a particular host are determined by a number of factors. One of these factors is whether or not infection by one parasite influences the probability of acquiring other parasite species. This study investigates the pattern of association between various parasites of the New Zealand cockle Austrovenus stutchburyi. Hundreds of cockles were collected from one locality within Otago Harbour, New Zealand and examined for trematode metacercariae and other symbionts. Two interspecific associations emerged from the study. First, the presence of the myicolid copepod Pseudomyicola spinosus was positively associated with higher infection intensity by echinostomes. The side-effect of the copepods activities within the cockle is suggested as the proximate mechanism that facilitates infection by echinostome cercariae, leading to a greater rate of accumulation of metacercariae in cockles harbouring the copepod. Second, a positive association was also found between infection intensity of the metacercariae of foot-encysting echinostomes and that of gymnophallid metacercariae. This supports earlier findings and suggests that the gymnophallid is a hitch-hiker parasite because, in addition to the pattern of positive association, it (a) shares the same transmission route as the echinostomes, and (b) unlike the echinostomes, it is not capable of increasing the hosts susceptibility to avian predation. Thus, both active hitch-hiking and incidental facilitation lead to non-random infection patterns in this parasite community.

Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophallus sp.

The complex life cycle of digenean trematodes with alternating stages of asexual multiplication and sexual reproduction can generate interesting within-host population genetic patterns. Metacercarial stages found in the second intermediate host are generally accumulated from the environment. Highly mobile second intermediate hosts can sample a broad range of cercarial genotypes and accumulate genetically diverse packets of metacercariae, but it is unclear whether the same would occur in systems where the second intermediate host is relatively immobile and cercarial dispersal is the sole mechanism that can maintain genetic homogeneity at the population level. Here, using polymorphic microsatellite markers, we addressed this issue by genotyping metacercariae of the trematode Gymnophallus sp. from the New Zealand cockle Austrovenus stutchburyi. Despite the relatively sessile nature of the second intermediate host of Gymnophallus, very high genotypic diversity of metacercariae was found within cockles, with only two cockles harbouring multiple copies of a single clonal lineage. There was no evidence of population structuring at the scale of our study, suggesting the existence of a well-mixed population. Our results indicate that (i) even relatively sessile second intermediate hosts can accumulate a high diversity of genotypes and (ii) the dispersal ability of cercariae, whether passive or not, is much greater than expected for such small and short-lived organisms. The results also support the role of the second intermediate host as an accumulator of genetic diversity in the trematode life cycle.

The use of fluorescent fatty acid analogs as labels in trematode experimental infections

We examined the utility of fluorescent fatty acid analog dyes for labeling larval trematodes to use in experimental infections. Our goals were to identify two dyes that label larval trematodes belonging to the species Maritrema novaezealandensis and Coitocaecum parvum, determine if the dyes influence survival and infectivity of larval trematodes and/or host mortality, and if larval trematodes labeled with alternative dyes could be distinguished post-infection. The two dyes tested, BODIPY FL C(12) and BODIPY 558/568 C(12), successfully labeled all treated larval trematodes, did not influence cercariae survival or infectivity, and did not influence host mortality in either host-parasite system. All larval parasites were fluorescent and distinguishable after 5 days in amphipod intermediate hosts. In addition, larval Acanthoparyphium sp. were strongly fluorescent with both dyes after 5 weeks within cockle hosts. This method should be extremely useful for experimental studies using trematode-host systems as models for addressing a range of ecological and evolutionary questions.

Effects of interspecific competition on asexual proliferation and clonal genetic diversity in larval trematode infections of snails

Interactions among different parasite species within hosts can be important factors shaping the evolution of parasite and host populations. Within snail hosts, antagonistic interactions among trematode species, such as competition and predation, can influence parasite abundance and diversity. In the present study we examined the strength of antagonistic interactions between 2 marine trematodes (Maritrema novaezealandensis and Philophthalmus sp.) in naturally infected Zeacumantus subcarinatus snails. We found approximately the same number of snails harbouring both species as would be expected by chance given the prevalence of each. However, snails infected with only M. novaezealandensis and snails with M. novaezealandensis and Philophthalmus sp. co-occurring were smaller than snails harbouring only Philophthalmus sp. In addition, the number of Philophthalmus sp. rediae was not affected by the presence of M. novaezealandensis sporocysts and the within-host clonal diversity of M. novaezealandensis was not influenced by the presence of Philophthalmus sp. Our results suggest that antagonistic interactions may not be a major force influencing the evolution of these trematodes and that characteristics such as host size and parasite infection longevity are shaping their abundance and population dynamics.