Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia

Understanding how pathogens and parasites diversify through time and space is fundamental to predicting emerging infectious diseases. Here, we use biogeographic, coevolutionary and phylogenetic analyses to describe the origin, diversity, and distribution of avian malaria parasites in the most diverse avifauna on Earth. We first performed phylogenetic analyses using the mitochondrial cytochrome b (cyt b) gene to determine relationships among parasite lineages. Then, we estimated divergence times and reconstructed ancestral areas to uncover how landscape evolution has shaped the diversification of Parahaemoproteus and Plasmodium in Amazonia. Finally, we assessed the coevolutionary patterns of diversification in this host–parasite system to determine how coevolution may have influenced the contemporary diversity of avian malaria parasites and their distribution among Amazonian birds. Biogeographic analysis of 324 haemosporidian parasite lineages recovered from 4178 individual birds provided strong evidence that these parasites readily disperse across major Amazonian rivers and this has occurred with increasing frequency over the last five million years. We also recovered many duplication events within areas of endemism in Amazonia. Cophylogenetic analyses of these blood parasites and their avian hosts support a diversification history dominated by host switching. The ability of avian malaria parasites to disperse geographically and shift among avian hosts has played a major role in their radiation and has shaped the current distribution and diversity of these parasites across Amazonia.     

A new Perkinsus species (Apicomplexa,Perkinsea) from the abalone Haliotis ruber

A new protozoan of the genus Perkinsus is described from the muscle and hemolymph of the blacklip abalone, Haliotis ruber, from South Australia. It occurs in the muscle of the adductor and mantle, and free and in brownish masses in the hemolymph. Cells cultured in thioglycollate medium produced a prezoosporangium which stained blue-black with iodine. The parasite differs from Perkinsus marinus, the only other member of the class, in having a much larger trophozoite, an eosinophilic vacuoplast when present, a short discharge tube, and appears to be uninfective to oysters.     

Genetically resistant sheep avoid parasites to a greater extent than do susceptible sheep

Livestock breeding programmes have created resistant (R) and susceptible (S) sheep that differ in their ability to control parasites through their immune function but potentially also their grazing behaviour (i.e. parasite avoidance). Using the Perendale genetic lines, we tested the hypothesis that R-sheep avoid parasites more effectively, reducing their parasite exposure/challenge, compared with S-sheep. However, in grazing systems, parasite-rich areas are also forage rich, suggesting that parasite avoidance behaviours are associated with nutritional penalties. We first created a naturally heterogeneous sward structure of gaps and tussocks and then used focal behavioural observations to quantify the sward selection of R- and S-sheep. Tussock swards were more nitrogen rich (41%), offered increased forage intake rates (32%) and contained 17 times more parasite larvae than gap swards. All the animals avoided grazing the tussock swards. However, the R-sheep grazed the tussock swards to a lesser degree than the S-sheep. We conclude that selection for genetic resistance has resulted in animals that, despite being well armed to fight parasitism through improved immune function, adopt parasite avoidance strategies with associated nutritional disadvantages. This experiment highlights the role of host behaviour in the control of parasitism and suggests that animals can be bred to avoid disease.     

Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Babesia rodhaini: A study of the effects of immune serum

The effect of passively administered immune serum against B. rodhaini has been studied quantitatively. The curve relating the proportion of parasites surviving, to the dose of serum, is sigmoid with a steep middle region. Parasites are killed at a rate proportional to the dose of serum in the early stages of infection, but after about 24 h a residual population of parasites multiplies at a rate only slightly less than that of normal parasites in normal hosts. The slight reduction is attributed to a residual effect of immune serum, and to the induction of an active immune response inadequate to prevent continuing multiplication of parasites.

The relationship between log₁₀ (parasite dose) and ST₅₀ for groups of mice is used to measure the dose of infective parasites.     

Effects of the swimbladder parasite Anguillicola crassus on the migration of European silver eels Anguilla anguilla in the Baltic Sea

In a mark–recapture study in 2006, migrating European Anguilla anguilla silver eels were caught, tagged and released in the Baltic Sea and recaptures in commercial pound nets examined for possible effects on migration of infection with the swimbladder parasite Anguillicola crassus . The overall recapture rate was 36%. The prevalence of infection was lowest at the northernmost sampling site. There were no significant differences between infected and uninfected A. anguilla in condition indices, body fat content and estimated migration speeds. Parasite infection intensity levels were significantly negatively correlated with times and distances covered between release and recapture, but did not correlate with migration speed. It appears that more heavily infected A. anguilla were relatively more vulnerable to recapture in pound nets. It is hypothesized that parasite-induced damage to the swimbladder inhibited vertical migrations and infected A. anguilla tended to migrate in shallower coastal waters, relatively close to the shore.     

Helminth parasite diversity discloses age and sex differences in the foraging behaviour of southern lapwings (Vanellus chilensis)

Parasites with heteroxen cycles are important sources of information on the trophic relations of hosts. This is particularly instructive for species whose age‐based or sex‐based differences are hardly detected by behavioural observations. Here, we describe the helminth community of the omnivorous southern lapwing (Vanellus chilensis) and evaluate whether it is affected by the host's sex, age and body size. The species is sexually monomorphic in body length, but males are slightly heavier than females. We analysed 112 individuals collected in Curitiba, Brazil, in March 2010. All hosts were parasitized. The helminth community was composed of 10 species (the digeneans Leucochloridium parcum and Athesmia sp., the cestode Infula macrophallus, the acantocephalans Plagiorhynchus sp., Centrorhynchus sp., Mediorhynchus sp., and an unidentified Gigantorhynchida, and the nematodes Heterakis psophiae, Dispharynx nasuta and an unidentified Capillariidae), seven of which were novel reports for this host species. Prevalence ranged from <1% to 99%. Whereas I. macrophallus was the most prevalent species, D. nasuta showed the highest mean intensity and abundance of infection. The former was found in most hosts as single male–female pairs, suggesting the occurrence of intrasexual competition. The infracommunities of juvenile birds showed a higher parasite species richness than those of adult males and females, suggesting the exploitation of a wider array of prey. However, the three classes harboured seven parasite species. Differences in parasite diversity (lower in juveniles, intermediate in adult males and higher in adult females) reflect the evenness in the distribution of parasite specimens among taxa in each age–sex class and are compatible with differences in their foraging strategy. Finally, we conclude based on the cycles of the heteroxen species that southern lapwings preyed upon molluscs, coleopterans, woodlice and earthworms.     

Infectivity of Neoaplectana carpocapsae and Heterorhabditis heliothidis to pupae of the parasite Apanteles militaris

The infectivity of Neoaplectana carpocapsae and Heterorhabditis heliothidis to Apanteles militaris, a gregarious parasite of the armyworm, was deterntined at 100. 1,000, 5,000, and 10,000 nematodes per petri dish. For both nematode species, the percentage of infected A. militaris within a cocoon cluster decreased as inoculum levels decreased. At the highest inoculum level, N. carpocapsae infected an average of 32% of the parasite pupae within a cocoon cluster, whereas H. heliothidis infected an average of 22%. Covariance analysis indicated, however, that N. carpocapsae had significantly greater infectivity than did H. heliothidis. Some of the dauer juveniles of N. carpocapsae on the body of the armyworm contacted the emerging parasites and eventually became enveloped within the silken cocoons. Dauer juveniles produced by N. carpocapsae in parasite pupae could not penetrate and escape from silken cocoons even when the cocoons were placed in a moist environment.     

Microcalorimetric characterization of seasonal metabolic trends in marine microcosms

A microcalorimetric and oximetric circulation system has been used to describe the emergence of seasonal adaptative changes occurring in marine microcosms at the water-sediment interface. The microcosms were prepared from three stations: one estuarine and two lagoonal. They were submitted to the same acute eutrophication, using peptone, and the evolutions shown by power-time and oxygen-time curves were compared over a 2-yr period. The metabolic heat productions and their oxidative counterparts are well correlated with seasonal trends. In summer, the microcalorimetric curves are typically unimodal, with very low dispersion, and a low thermodynamic steady state is attained in a few hours (40–50 μW), indicating an efficient, integrated regulatory mechanism; oxygen conditions evolute towards anoxia within 6 to 8 h. In winter, the power-time curves are typically sigmoid, with low dispersion; the thermodynamic steady state attained indicates a high maintenance energy requirement (140–150 μW), probably due to microbial populations less adapted to eutrophication stress. In winter, oxygen depletion is only partial and a plateau is attained within limits of 80 to 40% of initial saturation, and lasts 1 wk at least. Spring and autumn responses are very heterogeneous, varying from summer to winter types and displaying evolutive bimodal patterns. The sea-water-sediment interfaces from different estuarine and lagoonal habitats with distinct physical and chemical characteristics, but subjected to similar environmental and seasonal perturbations, show similar energetic patterns according to the seasons. It is proposed, as a working hypothesis, that the seasonal variations of the microcalorimetric response to experimental eutrophication are the expression of a global homeostatic adaptative memory, determined by natural environmental perturbations. Spring and autumn can be considered as intermediate periods within which a seasonal “adaptative memory” is replaced gradually by another one. The heterogeneity of the microcalorimetric response in spring and autumn microcosms could be related to an asynchronous maturation for the different components of the benthic ecosystem.     

Is there a fixed number of niches for endoparasites of fish?

Kennedy and Guégan, based on Cornell and Lawton (J Anim Ecol 1992;61:1–12), found a curvilinear relationship (the fundamental form of the relationship for parasite communities) between infracommunity and component community richness, and interpreted this as meaning that only processes acting within the infracommunities can explain the limitation in the number of parasite species in a given host. The research described here shows that an asymptotic relationship is the consequence of the differential likelihoods of parasite species to appear in an infracommunity as determined by transmission rates and intrinsic lifespans. Processes operating at the infracommunity level are not necessary to explain the curvilinear relationship. Even communities much richer than those found in European freshwater fishes cannot be assumed to be saturated in the sense that further species cannot be added over evolutionary time.     

Progress in parasitic plant biology: host selection and nutrient transfer

Host range varies widely among species of parasitic plants. Parasitic plants realize host selection through induction by chemical molecular signals, including germination stimulants and haustoria-inducing factors (HIFs). Research on parasitic plant biology has provided information on germination, haustorium induction, invasion, and haustorial structures and functions. To date, some molecular mechanisms have been suggested to explain how germination stimulants work, involving a chemical change caused by addition of a nucleophilic protein receptor, and direct or indirect stimulation of ethylene generation. Haustorium initiation is induced by HIFs that are generated by HIF-releasing enzymes from the parasite or triggered by redox cycling between electrochemical states of the inducers. Haustorium attachment is non-specific, however, the attachment to a host is facilitated by mucilaginous substances produced by haustorial hairs. Following the attachment, the intrusive cells of parasites penetrate host cells or push their way through the host epidermis and cortex between host cells, and some types of cell wall-degrading enzymes may assist in the penetration process. After the establishment of host-parasite associations, parasitic plants develop special morphological structures (haustoria) and physiological characteristics, such as high transpiration rates, high leaf conductance, and low water potentials in hemiparasites, for nutrient transfer and resource acquisition from their hosts. Therefore, they negatively affect the growth and development and even cause death of their hosts.     

The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata)

Dietary carotenoids have been shown to confer immunological benefits to some species of animals in which males also use these pigments to attract mates. Thus, the potential exists for an allocation trade-off between the sexual and immunological functions of carotenoids. Food availability may also influence immune system function. The present study examined the effects of carotenoid and food availability on the resistance of male guppies ( Poecilia reticulata Peters) from four wild populations to the parasite Gyrodactylus turnbulli Harris. Intermediate levels of carotenoid ingestion resulted in the lowest parasite loads, which suggests that carotenoids strengthen parasite resistance at low levels but either benefit parasites or suppress host immunity at high levels. Males raised on the high-food level initially had fewer parasites, suggesting heightened innate immunity relative to males raised on the low-food level. Over the course of the experiment, however, the high-food males supported higher parasite population growth rates than the low-food males. The results obtained emphasize the importance of evaluating the effects of diet on multiple aspects of immune system function, and caution against assuming that positive effects of carotenoids on immunity in one context will automatically translate to other contexts.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 301–309.     

Parasites of native and exotic freshwater fishes in south‐western Australia

In this study, 1429 fishes of 18 different species (12 native and six exotic) were sampled from 29 localities to compare the levels of parasitism between native and exotic fish species and to examine the relationship between environmental degradation and parasite diversity. Forty‐four putative species of parasites were found and most of these appear to be native parasites, which have not previously been described. Two parasite species, Lernaea cyprinacea and Ligula intestinalis, are probably introduced. Both were found on or in a range of native fish species, where they may cause severe disease. Levels of parasitism and parasite diversity were significantly greater in native fishes than in exotic species, and this may contribute to an enhanced demographic performance and competitive ability in invading exotics. Levels of parasitism and parasite diversity in native fishes were negatively related to habitat disturbance, in particular to a suite of factors that indicate increased human use of the river and surrounding environment. This was due principally to the absence in more disturbed habitats of a number of species of endoparasites with complex life cycles, involving transmission between different host species.     

Direct non-insect-vector transmission of Leishmania parasites in mice

Animal to animal non-vector transmission of Leishmania major was investigated in Balb/c mice, a strain known for its susceptibility to this parasite. Both overt or inapparent infection (documented by positive spleen cultures) was possible after prolonged contact with infected animals. Similarly transmission of infection from infected mothers to their offspring was documented.     

Social networks and the spread of Salmonella in a sleepy lizard population

Although theoretical models consider social networks as pathways for disease transmission, strong empirical support, particularly for indirectly transmitted parasites, is lacking for many wildlife populations. We found multiple genetic strains of the enteric bacterium Salmonella enterica within a population of Australian sleepy lizards (Tiliqua rugosa), and we found that pairs of lizards that shared bacterial genotypes were more strongly connected in the social network than were pairs of lizards that did not. In contrast, there was no significant association between spatial proximity of lizard pairs and shared bacterial genotypes. These results provide strong correlative evidence that these bacteria are transmitted from host to host around the social network, rather than that adjacent lizards are picking up the same bacterial genotype from some common source.     

Inhibition of Dirofilaria immitis in gregarine-infected Aedes aegypti: preliminary observations.

This study examined some of the effects of Ascocystis culicis infections in Aedes aegypti mosquitoes and on the development of dog heartworm, Dirofilaria immitis, in A. culicis-infected A. aegypti. Infections of 100 or more gregarines had an adverse effect on mosquito larvae and the resulting pupae weighed 1 to 2 mg less than the gregarine-free stock mosquitoes. Intensity of gregarine-induced pathology of adult mosquitoes was best estimated by counting the cells of the Malpighian tubules. Larvae infected with approximately 100 gregarines per larva had at least half the number of cells in their tubules destroyed, and development of D. immitis was greatly reduced. Thus, gregarine infections may be useful in reducing populations of aedine mosquitoes and, in areas endemic for heartworm, may interrupt transmission of D. immitis.     

Characterization of Host Cell Mutants Significantly Resistant to Cryptosporidium parvum Infection

Cryptosporidium parvum is a parasitic protist and a causative agent of mild‐to‐severe diarrheal diseases in humans and animals. Despite its globally recognized importance, knowledge on the mechanism of parasite invasion and molecular interactions between host cells and the parasite is limited. Here, we report the establishment of 43 mutant cell lines derived from HCT‐8 cells by UV‐induced mutagenesis and the characterization of three mutants with significantly reduced susceptibility to cryptosporidial infection. Based on qRT‐PCR assay performed at 18 h postinfection time, the parasite loads could be reduced by ~45%, ~35%, and ~20% in mutants A05, B08, and B12, respectively (p < 0.001 in all three mutants vs. HCT‐8 cells). The mutagenesis mainly affected the attachment of parasite in A05 (i.e. ~30% reduction, p < 0.001 vs. HCT‐8), and intracellular development in B08 and B12. The three cell mutants may serve as valuable reagents to further investigate the mechanism of parasite invasion and intracellular development by identifying the gene mutations associated with the parasite attachment (A05) and intracellular development (B08 and B12).