Resistance and tolerance: A hierarchical framework to compare individual versus family-level host contributions in an experimental amphibian-trematode system.

Hosts have two general strategies for mitigating the fitness costs of parasite exposure and infection: resistance and tolerance. The resistance-tolerance framework has been well developed in plant systems, but only recently has it been applied to animal-parasite interactions. However, difficulties associated with estimating fitness, controlling parasite exposure, and quantifying parasite burden have limited application of this framework to animal systems. Here, we used an experimental approach to quantify the relative influence of variation among host individuals and genetic families in determining resistance and tolerance within an amphibian-trematode system. Importantly, we used multiple, alternative metrics to assess each strategy, and employed a Bayesian analytical framework to compare among responses while incorporating uncertainty. Relative to unexposed hosts, exposure to the pathogenic trematode (Ribeiroia ondatrae) reduced the survival and growth of California newts (Taricha torosa) (survival: 93% vs. 74%; growth: 0.29 vs. -0.5 vs mm day -1). Similarly, parasite infection success (the inverse of resistance) ranged from 8% to 100%. Yet despite this broad variation in host resistance and tolerance among individual newts, we found no evidence for transmissable, among-family variation in any of the resistance or tolerance metrics. This suggests that opportunities for evolution of these traits is limited, likely requiring significant increases in mutation, gene flow, or environmental heterogeneity. Our study provides a quantitative framework for evaluating the importance of alternative metrics of resistance and tolerance across multiple time points in the study of host-parasite interactions in animal systems.

Acanthoparyphium sp. and other metazoan symbionts of the American oyster, Crassostrea virginica, from South Texas.

In this study, we investigated oysters, Crassostrea virginica , from Laguna Madre in South Texas, where a 45-yr old study recorded metacercarial infections of the echinostomatid trematode, Acanthoparyphium spinulosum , an Asian relative of which, Acanthoparyphium tyosenense, has been associated with human infections via the ingestion of raw mollusks. In an effort to examine the base-line infection parameters of Acanthoparyphium sp. in oysters, we examined the effect of distance from the shoreline, which is the habitat of the first intermediate host snail, Cerithidea pliculosa, as well as temporal changes in oyster infection levels, by conducting quarterly collections of oysters during a year. We found that almost all oysters (prevalence = 97.8-100%) were infected regardless of distance to the shoreline and season. However, the abundance of metacercariae was significantly higher close to the shoreline, while no significant temporal changes could be detected. In addition to the echinostomatid, we found a high abundance of the metacestode Tylocephalum sp. and the presence of 4 other metazoan parasites. None of the infections seemed to incur significant tissue damage to the oysters. Our study shows that at least locally, recreational harvesters of oysters may be exposed to Acanthoparyphium sp. Future studies should examine oysters from snail host habitats in the Gulf of Mexico, and the potential zoonotic risk of Acanthoparyphium sp. should be evaluated using experimental infections of animal models.

Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk.

Parasite infections often lead to dramatically different outcomes among host species. Although an emerging body of ecoimmunological research proposes that hosts experience a fundamental trade-off between pathogen defences and life-history activities, this line of inquiry has rarely been extended to the most essential outcomes of host-pathogen interactions: namely, infection and disease pathology. Using a comparative experimental approach involving 13 amphibian host species and a virulent parasite, we test the hypothesis that 'pace-of-life' predicts parasite infection and host pathology. Trematode exposure increased mortality and malformations in nine host species. After accounting for evolutionary history, species that developed quickly and metamorphosed smaller ('fast-species') were particularly prone to infection and pathology. This pattern likely resulted from both weaker host defences and greater adaptation by parasites to infect common hosts. Broader integration between life history theory and disease ecology can aid in identifying both reservoir hosts and species at risk of disease-driven declines.

Intra-host competition between co-infecting digeneans within a bivalve second intermediate host: dominance by priority-effect or taking advantage of others?

We experimentally investigated the interactions between two parasites known to manipulate their host's phenotype, the trematodes Acanthoparyphium sp. and Curtuteria australis, which infect the cockle Austrovenus stutchburyi. The larval stages of both species encyst within the tissue of the bivalve's muscular foot, with a preference for the tip of the foot. As more individuals accumulate at that site, they impair the burrowing behaviour of cockles and increase the probability of the parasites' transmission to a bird definitive host. However, individuals at the foot tip are also vulnerable to non-host predators in the form of foot-cropping fish which selectively bite off the foot tip of exposed cockles. Parasites encysted at the foot base are safe from such predators although they do not contribute to altering host behaviour, but nevertheless benefit from host manipulation as all parasites within the cockle are transmitted if it is ingested by a bird. Experimental infection revealed that Acanthoparyphium sp. and C. australis have different encystment patterns within the host, with proportionally fewer Acanthoparyphium metacercariae encysting at the foot tip than C. australis. This indicates that Acanthoparyphium may benefit indirectly from C. australis and incur a lower risk of non-host predation. However, in co-infections, not only did C. australis have higher infectivity than Acanthoparyphium, it also severely affected the latter's infection success. The asymmetrical strategies and interactions between the two species suggest that the advantages obtained from exploiting the host manipulation efforts of another parasite might be offset by traits such as reduced competitiveness in co-infections.

Mercury in parasitic nematodes and trematodes and their double-crested cormorant hosts: bioaccumulation in the face of sequestration by nematodes.

Endoparasites can alter their host's heavy metal concentrations by sequestering metals in their own tissues. Contracaecum spp. (a nematode), but not Drepanocephalus spathans (a trematode), were bioaccumulating mercury to concentrations 1.5 times above cormorant hosts. Nematodes did not have significantly greater stable nitrogen isotope values (δ(15)N) than their hosts, which is contradictory to prey-predator trophic enrichment studies, but is in agreement with other endoparasite-host relationships. However, Contracaecum spp. δ(13)C values were significantly greater than their hosts, which suggest that nematodes were consuming host tissues. Nematodes were accumulating and thus sequestering some of their cormorant hosts' body burden of methyl mercury; however, they were not dramatically reducing their hosts' accumulation of methyl mercury.

Sympatric and allopatric experimental infections of the planorbid snail Gyraulus chinensis with miracidia of Euparyphium albuferensis (Trematoda: Echinostomatidae).

An experimental infection with echinostomatid miracidia in sympatric or 'local' vs. allopatric or 'away' snail combinations, as a model to examine parasite compatibility, was carried out. We employed Euparyphium albuferensis miracidia to infect Gyraulus chinensis snails, from three different natural parks: Albufera (Valencia, Spain); the Ebro Delta (Tarragona, Spain) and Coto de Doñana (Huelva, Spain). Insignificant differences between the three snail strains were noted for the infection rate and the rhythm of daily cercarial production. However, a significantly higher total cercarial production per snail, patent period and life span were observed in local snails. The different infection characteristics in the three G. chinensis strains considered reveal that E. albuferensis miracidia demonstrate local adaptation.

The effects of temperature on the distribution and establishment of Echinoparyphium recurvatum metacercariae in Lymnaea peregra.

The establishment and distribution of Echinoparyphium recurvatum metacercariae in the second intermediate host, Lymnaea peregra, were investigated at a temperature range of 5-29 degrees C. Preliminary studies on the survival and infectivity of E. recurvatum cercariae showed that both parameters were temperature dependent. No cercarial transmission occurred at 5 or 10 degrees C. Nevertheless, the transmission efficiency (1/H0) indicated that transmission was temperature independent in the temperature range 17-25 degrees C and was much lower than in previous studies using this host-parasite system. These differences were attributed to low cercarial densities used in this study. The effect of temperature on encystment site choice (mantle cavity, kidney, pericardium) by metacercariae showed that the mantle cavity was the prime site of encystment, followed by the pericardium and the kidney. Temperatures at the lower and upper ranges (14 and 29 degrees C), however, caused a significant reduction in encystment in the mantle cavity but not in the pericardium or kidney. The importance of cercarial densities, the physiological mechanisms influencing metacercarial distribution and their implications for parasite transmission to the definitive host are discussed.

Infection patterns in white sea blue mussels Mytilus edulis of different age and size with metacercariae of Himasthla elongata (Echinostomatidae) and Cercaria parvicaudata (Renicolidae).

Infection of mussels Mytilus edulis L. by 2 trematode species was studied in a natural intertidal population in the Chupa inlet of the White Sea. The prevalence of metacercariae of Himasthla elongata (Mehlis, 1831) and Cercaria parvicaudata (Stunkard & Shaw, 1931) in mussels reached 100% in 3 to 4 yr old molluscs and remained at this level in older individuals. Infection intensity increased evenly with the age of the molluscan host, showing a tendency to decrease only in the oldest (9 yr old) mussels. These patterns of age dynamics of prevalence and infection intensity were associated with accumulation of trematode larvae in the course of the molluscs' lives. Ability of metacercariae to exist in mussels for long periods (at least 2.5 yr) was verified in the course of an experiment, during which infected molluscs were kept in a subtidal net cage. Decrease of infection intensity in the oldest individuals may reflect selective mortality of the most severely infected molluscs. Among mussels of the same age, higher infection intensity values occurred in larger individuals. This may be due to an enhanced pumping rate in large molluscs, which increases the probability of cercariae, free-living trematode larvae, infecting them via water currents.

Food-borne intestinal trematodiases in humans.

Food-borne trematodiases still remain a public health problem world-wide, despite changes in eating habits, alterations in social and agricultural practices, health education, industrialization, environmental alteration, and broad-spectrum anthelmintics. Food-borne trematodiases usually occur focally, are still persistently endemic in some parts of the world, and are most prevalent in remote rural places among school-age children, low-wage earners, and women of child-bearing age. Intestinal fluke diseases are aggravated by socio-economic factors such as poverty, malnutrition, an explosively growing free-food market, a lack of sufficient food inspection and sanitation, other helminthiases, and declining economic conditions. Control programs implemented for food-borne zoonoses and sustained in endemic areas are not fully successful for intestinal food-borne trematodiases because of centuries-old traditions of eating raw or insufficiently cooked food, widespread zoonotic reservoirs, promiscuous defecation, and the use of "night soil" (human excrement collected from latrines) as fertilizer. This review examines food-borne intestinal trematodiases associated with species in families of the Digenea: Brachylaimidae, Diplostomidae, Echinostomatidae, Fasciolidae, Gastrodiscidae, Gymnophallidae, Heterophyidae, Lecithodendriidae, Microphallidae, Nanophyetidae, Paramphistomatidae, Plagiorchiidae, and Strigeidae. Because most of the implicated species are in the Echinostomatidae and Heterophyidae, emphasis in the review is placed on species in these families.

The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms.

The New Zealand cockle Austrovenus stutchburyi, whose foot is commonly infected by the digenean trematode Curtuteria australis (Echinostomatidae), is often found heavily infected and unable to burrow on the sediment surface of tidal flats. This has been interpreted as a Curtuteria-manipulation with the purpose of increasing the transmission of the parasite to shorebirds acting as final hosts. Using a field-experimental approach the alternative hypothesis was tested, that surface-dwelling cockles, caught on the surface for other reasons than parasites, accumulate larval C. australis at a higher rate than buried cockles. During the 3-month experiment, larval trematodes accumulated with a rate of approximately 0.5 metacercariae/day in both surface and buried cockles. The result strengthens the manipulation hypothesis indirectly by rejecting the alternative hypothesis. The metacercariae were unevenly distributed along the cockle-foot, with about 4 times as many cysts being found in the tip than in either the mid or hind part of the foot. In light of existing knowledge of the burrowing behaviour and apparatus in bivalves, and a negative relationship between foot mobility and infection intensity, it is suggested that C. australis manipulates its host through a mechanical obstruction of foot muscles and the dynamic hydrostatic skeleton, both necessary for successful burrowing.

Toxic effects of cadmium and zinc on the transmission of Echinoparyphium recurvatum cercariae.

The toxicity of cadmium, zinc and Cd/Zn mixtures to the transmission of Echinoparyphium recurvatum (Digenea: Echinostomatidae) cercariae into the snail second intermediate hosts was investigated at concentrations ranging from 100 microg l-1 to 10 000 microg l-1 in both soft and hard water. A differential response in the infectivity of metal-exposed cercariae into Lymnaea peregra and Physa fontinalis was demonstrated which was dependent on the snail species being infected. Exposure of L. peregra, P. fontinalis, and L. stagnalis to heavy metals caused a differing susceptibility to E. recurvatum cercariae depending on the snail species being exposed. The mechanism and effects of metal toxicity, together with the importance of the parasite/host strain on cercarial transmission are discussed.

The life cycle and transmission dynamics of the larval stages of Hypoderaeum conoideum.

The morphology of the different larval stages and life cycle of Hypoderaeum conoideum (Trematoda: Echinostomatidae) are described. The freshwater snail species Lymnaea peregra (Gastropoda: Lymnaeidae) serves as the natural first intermediate host and this and L. corvus serve as experimental first intermediate hosts. These and other freshwater snails, such as Physella acuta and Gyraulus chinensis, in turn serve as second intermediate hosts. Adult worms were obtained from chicks and ducks, but not from rats, mice and golden hamsters. The morphology of the larval stages is compared with previous work on H. conoideum. Several aspects of the biology of the life history stages are described with emphasis on the transmission dynamics of the free-living stages. Differential suitability of the snail species that may act as first and/or second intermediate hosts is studied and discussed.

Survival and infectivity of Hypoderaeum conoideum and Euparyphium albuferensis cercariae under laboratory conditions.

The survival characteristics of the cercariae of Hypoderaeum conoideum and Euparyphium albuferensis (Trematoda: Echinostomatidae) at 20 degrees C and 30 degrees C are described, and the age dependency of their infectivity at 20 degrees C is studied to determine their respective transmission efficiencies. Cercarial survival was found to be age-dependent and was higher at 20 degrees C. For both cercariae, the maximum life-span was 26 h at 20 degrees C and 16 h at 30 degrees C, and their respective times to 50% mortality were similar at each temperature. Both cercariae seem to be well adapted to transmission in their natural habitat, though cercarial infectivity of H. conoideum was higher than that of E. albuferensis, this being correlated with their prevalences in nature. The age-dependency of cercarial survival may be related to steadily diminishing endogenous energy levels, though the delay in attaining maximum infectivity suggests that other factors not related to energy considerations are involved in the delimitation of the cercarial infective period. However, this latter observation may constitute an adaptative mechanism allowing cercarial dissemination.

The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae).

Survival and infectivity characteristics are described for cercariae of the echinostome Echinoparyphium recurvatum at 10, 15, 20, 25 and 30 degrees C. Cercarial survival was markedly age- and temperature-dependent, maximum survival time being reduced from 68 h at 10 degrees C to 12 h at 30 degrees C, 50% survival times falling from 47.9 h at 10 degrees C to 8.4 h at 30 degrees C. The mean instantaneous per capita death rate of cercariae increased exponentially with temperature. Cercarial infectivity was also temperature dependent, the main effect of temperature being upon the rate at which infectivity diminished with increasing age of cercariae. Infectivity increased from zero at 10 degrees C to a maximum at 25 degrees C after which it declined to a low level at 30 degrees C. Overall transmission efficiency of cercariae at each experimental temperature was calculated as the ratio of the mean instantaneous per capita death rate (mu) to the mean instantaneous per capita rate of infection (beta). Transmission efficiency of cercariae was found to be maximal at 20 degrees C and at a relatively high level between 10 and 25 degrees C. Transmission efficiency was zero at 10 degrees C and at a very low level at 30 degrees C. These results suggest that the cercariae of E. recurvatum show transmission optima at water temperatures likely to be encountered in natural habitats in Britain and Europe.