Host diet as a determinant of parasite growth, reproduction and survival

Changes have been observed in the biology of protozoan and helminth parasites of small mammals during a variety of experimental nutritional manipulations ranging from deficiency in a specific nutrient to the general withholding of food from the host. Commonly observed effects include retardations in parasite growth rate, gametogenesis, fecundity, and asexual multiplication. The duration of patency and of the association of a parasite with its host have also been observed to be curtailed. The nutritional responses of parasites during host hibernation require investigation and much research will be needed to explain how perturbations in host dietary composition and intake may lead to the observed effects. Care should be exercised over applying the results from experimental studies to naturally occurring infections, but the experiments are justified because they indicate potential effects, if not their biological significance, and because causation can be determined.     

A kin selection model for the evolution of virulence.

The costs and benefits of parasite virulence are analysed in an evolutionarily stable strategy (ESS) model. Increased host mortality caused by disease (virulence) reduces a parasite's fitness by damaging its food supply. The fitness costs of high virulence may be offset by the benefits of increased transmission or ability to withstand the host's defences. It has been suggested that multiple infections lead to higher virulence because of competition among parasite strains within a host. A quantitative prediction is given for the ESS virulence rate as a function of the coefficient of relatedness among co-infecting strains. The prediction depends on the quantitative relation between the costs of virulence and the benefits of transmission or avoidance of host defences. The particular mechanisms by which parasites can increase their transmission or avoid host defences also have a key role in the evolution of virulence when there are multiple infections.     

Modulation of host cell intracellular Ca2+

During the course of evolution, protozoan parasites have developed strategies to subvert the immune response of their host in order to multiply, reproduce and survive. One of these inherited strategies is their capacity to modulate the host cell transductional mechanisms in their favor. Alteration of host cells Ca(2-) homeostasis following interaction and/or invasion by protozoan parasites such as Leishmania donovani, Trypanosoma cruzi, Plasmodium falciparum or Entamoeba histolytica has been reported. There is direct evidence that such disturbances are responsible for pathogenesis observed during parasitic infections. This homeostatic imbalance of Ca(2+) in the host cell is an early inducible event whose underlying mechanisms needs further investigation, as discussed here by Martin Olivier.     

Host resistance and tolerance of parasitic gut worms depend on resource availability

Resource availability can significantly alter host–parasite dynamics. Abundant food can provide more resources for hosts to resist infections, but also increase host tolerance of infections by reducing competition between hosts and parasites for food. Whether abundant food favors host resistance or tolerance (or both) might depend on the type of resource that the parasite exploits (e.g., host tissue vs. food), which can vary based on the stage of infection. In our study, we evaluated how low and high resource diets affect Cuban tree frog (Osteopilus septentrionalis) resistance and tolerance of a skin-penetrating, gut nematode Aplectana sp. at each stage of the infection. Compared to a low resource diet, a high resource diet enhanced frog resistance to worm penetration and tolerance while worms traveled to the gut. In contrast, a low resource diet increased resistance to establishment of the infection. After the infection established and worms could access food resources in the gut, a high resource diet enhanced host tolerance of parasites. On a high resource diet, parasitized frogs consumed significantly more food than non-parasitized frogs; when food was then restricted, mass of non-parasitized frogs did not change, whereas mass of parasitized frogs decreased significantly. Thus, a high resource diet increased frog tolerance of established worms because frogs could fully compensate for energy lost to the parasites. Our study shows that host–parasite dynamics are influenced by the effect of resource availability on host resistance and tolerance, which depends on when parasites have access to food and the stage of infection.     

Parasite effects on host’s trophic and isotopic niches

Wild animals are usually infected with parasites that can alter their hosts’ trophic niches in food webs as can be seen from stable isotope analyses of infected versus uninfected individuals. The mechanisms influencing these effects of parasites on host isotopic values are not fully understood. Here, we develop a conceptual model to describe how the alteration of the resource intake or the internal resource use of hosts by parasites can lead to differences of trophic and isotopic niches of infected versus uninfected individuals and ultimately alter resource flows through food webs. We therefore highlight that stable isotope studies inferring trophic positions of wild organisms in food webs would benefit from routine identification of their infection status.     

Multiple infections by the anther smut pathogen are frequent and involve related strains

Population models of host-parasite interactions predict that when different parasite genotypes compete within a host for limited resources, those that exploit the host faster will be selected, leading to an increase in parasite virulence. When parasites sharing a host are related, however, kin selection should lead to more cooperative host exploitation that may involve slower rates of parasite reproduction. Despite their potential importance, studies that assess the prevalence of multiple genotype infections in natural populations remain rare, and studies quantifying the relatedness of parasites occurring together as natural multiple infections are particularly scarce. We investigated multiple infections in natural populations of the systemic fungal plant parasite Microbotryum violaceum, the anther smut of Caryophyllaceae, on its host, Silene latifolia. We found that multiple infections can be extremely frequent, with different fungal genotypes found in different stems of single plants. Multiple infections involved parasite genotypes more closely related than would be expected based upon their genetic diversity or due to spatial substructuring within the parasite populations. Together with previous sequential inoculation experiments, our results suggest that M. violaceum actively excludes divergent competitors while tolerating closely related genotypes. Such an exclusion mechanism might explain why multiple infections were less frequent in populations with the highest genetic diversity, which is at odds with intuitive expectations. Thus, these results demonstrate that genetic diversity can influence the prevalence of multiple infections in nature, which will have important consequences for their optimal levels of virulence. Measuring the occurrence of multiple infections and the relatedness among parasites within hosts in natural populations may be important for understanding the evolutionary dynamics of disease, the consequences of vaccine use, and forces driving the population genetic structure of parasites.     

Horizontal transmission of Wolbachia in a Drosophila community

Abstract.  1.  Wolbachia bacteria are reproductive parasites of arthropods and infect an estimated 20% of all insect species worldwide. In order to understand patterns of Wolbachia infection, it is necessary to determine how infections are gained or lost. Wolbachia transmission is mainly vertical, but horizontal transmission between different host species can result in new infections, although its ecological context is poorly understood. Horizontal transmission is often inferred from molecular phylogenies, but could be confounded by recombination between different Wolbachia strains.
2. This study addressed these issues by using three genes: wsp , ftsZ , and groE , to study Wolbachia infections in fruit- and fungus-feeding Drosophila communities in Berkshire, U.K.
3. Identical sequences were found for all three genes in Drosophila ambigua and Drosophila tristis. This suggests horizontal transmission of Wolbachia between these two previously unstudied Drosophila species, which may be the result of the two host species sharing the same food substrates or parasites.
4.  Wolbachia infections might be lost from species due to curing by naturally occurring antibiotics and the presence of these is likely to vary between larval food substrates.
5. It was investigated whether Wolbachia incidence was lower in fungus-feeding than in fruit-feeding Drosophila species, but no significant difference based on food substrate was found.     

Impact of intestinal parasites on digestive function in humans

In humans as well as in animals, intestinal parasites can affect key stages of alimentation, digestion, and absorption. Selected examples of the effects of parasitic infection on food intake, intestinal propulsion and motility, organ function, epithelial structure and function, and intestinal circulation are presented. Malabsorption and nutrient loss can result from many of these common infections. Additional data are needed to determine the extent to which alterations in gastrointestinal structure and function vs. effects on appetite mediate the effects of parasites on host nutrition in humans.     

Arctic parasitology: why should we care?

The significant impact on human and animal health from parasitic infections in tropical regions is well known, but parasites of medical and veterinary importance are also found in the Arctic. Subsistence hunting and inadequate food inspection can expose people of the Arctic to foodborne parasites. Parasitic infections can influence the health of wildlife populations and thereby food security. The low ecological diversity that characterizes the Arctic imparts vulnerability. In addition, parasitic invasions and altered transmission of endemic parasites are evident and anticipated to continue under current climate changes, manifesting as pathogen range expansion, host switching, and/or disease emergence or reduction. However, Arctic ecosystems can provide useful models for understanding climate-induced shifts in host-parasite ecology in other regions.     

Energetic costs of parasitism in the Cape ground squirrel Xerus inauris

Parasites have been suggested to influence many aspects of host behaviour. Some of these effects may be mediated via their impact on host energy budgets. This impact may include effects on both energy intake and absorption as well as components of expenditure, including resting metabolic rate (RMR) and activity (e.g. grooming). Despite their potential importance, the energy costs of parasitism have seldom been directly quantified in a field setting. Here we pharmacologically treated female Cape ground squirrels (Xerus inauris) with anti-parasite drugs and measured the change in body composition, the daily energy expenditure (DEE) using doubly labelled water, the RMR by respirometry and the proportions of time spent looking for food, feeding, moving and grooming. Post-treatment animals gained an average 19g of fat or approximately 25kJd-1. DEE averaged 382kJd-1 prior to and 375kJd-1 post treatment (p>0.05). RMR averaged 174kJd-1 prior to and 217kJd-1 post treatment (p<0.009). Post-treatment animals spent less time looking for food and grooming, but more time on feeding. A primary impact of infection by parasites could be suppression of feeding behaviour and, hence, total available energy resources. The significant elevation of RMR after treatment was unexpected. One explanation might be that parasites produce metabolic by-products that suppress RMR. Overall, these findings suggest that impacts of parasites on host energy budgets are complex and are not easily explained by simple effects such as stimulation of a costly immune response. There is currently no broadly generalizable framework available for predicting the energetic consequences of parasitic infection.     

Co-occurrences of parasite clones and altered host phenotype in a snail-trematode system

The frequent co-occurrence of two or more genotypes of the same parasite species in the same individual hosts has often been predicted to select for higher levels of virulence. Thus, if parasites can adjust their level of host exploitation in response to competition for resources, mixed-clone infections should have more profound impacts on the host. Trematode parasites are known to induce a wide range of modifications in the morphology (size, shell shape or ornamentation) of their snail intermediate host. Still, whether mixed-clone trematode infections have additive effects on the phenotypic alterations of the host remains to be tested. Here, we used the snail Potamopyrgus antipodarum-infected by the trematode Coitocaecum parvum to test for both the general effect of the parasite on host phenotype and possible increased host exploitation in multi-clone infections. Significant differences in size, shell shape and spinosity were found between infected and uninfected snails, and we determined that one quarter of naturally infected snails supported mixed-clone infections of C. parvum. From the parasite perspective, this meant that almost half of the clones identified in this study shared their snail host with at least one other clone. Intra-host competition may be intense, with each clone in a mixed-clone infection experiencing major reductions in volume and number of sporocysts (and consequently multiplication rate and cercarial production) compared with single-clone infections. However, there was no significant difference in the intensity of host phenotype modifications between single and multiple-clone infections. These results demonstrate that competition between parasite genotypes may be strong, and suggest that the frequency of mixed-clone infections in this system may have selected for an increased level of host exploitation in the parasite population, such that a single-clone is associated with a high degree of host phenotypic alteration.     

The effect of Schistocephalus solidus infection on meal size of three‐spined stickleback

The effect of infection with the pseudophyllidean cestode Schistocephalus solidus on the meal size of individually housed three‐spined stickleback Gasterosteus aculeatus was quantified. Infected fish harboured plerocercoid loads that contributed from 1·1 to 33·9% of their total mass. Across this range of infection levels, the presence of S. solidus infection had no significant directional effect on standard length ( L _S) corrected meal size of host three‐spined sticklebacks. Amongst multiply infected fish there was a significant negative relationship between L _S‐corrected meal size and the proportion of host mass contributed by S. solidus parasites. This relationship, however, did not hold for singly‐infected fish. Furthermore, the data suggest that multiply‐infected fish that harbour a combined mass of parasites contributing < c . 15% to host body mass might exhibit meal sizes that exceed those of length‐matched uninfected fish. The results suggest that although heavy infections can significantly reduce the meal size of heavily infected three‐spined sticklebacks, in the early stages of multiple S. solidus infections host food intake may increase. The probable causes of these differential effects on meal size and their consequences for the host‐parasite system are discussed.     

Fluctuating asymmetry in an insect host: a big role for big parasites?

Parasites are expected to be associated with host developmental instability because developmentally unstable hosts may be more susceptible to, or more frequently exposed to, parasitic infections compared with developmentally stable ones, or because parasites may directly disrupt host development. In this study, we analysed the relationship between developmental stability in the weta Pleioplectron simplex (Orthoptera) and infections by hairworm and mermithid parasites. These parasites have a long development in their host and the size of adult worms exceeds the length of the host by a considerable amount (15–20 cm). For one character (femora) we found that fluctuating asymmetry was significantly higher in parasitized individuals compared with unparasitized ones, in each of two samples collected in different years. Because no relationship was observed between the level of fluctuating asymmetry and the parasite size or number, however, infection by hairworm and mermithid parasites could be more a consequence of developmental instability than a cause. For other characters (tibia, external and internal spines of femora), the level of fluctuating asymmetry between parasitized and unparasitized individuals was not significantly different. Our results are discussed in relation to ecological constraints met by hairworm and mermithid parasites to complete their life cycle.     

Interactions between the parasitic protozoa of small mammals

In the wild, small mammals are frequently infected with more than one parasite. Laboratory studies have revealed complex interactions between parasites and also between parasitic protozoa and viruses or bacteria. In general, infection with many parasites is accompanied by a period of immunodepression during which superimposed infections are favoured, giving rise to more intense and prolonged secondary infections while the original infection is unaffected. On the other hand, organisms that activate macrophages may protect die host against a subsequent infection. These kinds of interactions have been investigated in the laboratory using Trypanosoma musculi, T. lewisi, Giardia muris, Spironucleus muris, Babesia microti and Heligmosomoides polygyrus , all of which occur in British small mammals, suggesting that such interactions occur in the field, are worth investigating and should be considered in epidemiological studies.     

Effects of parasites on fish behaviour: a review and evolutionary perspective

Fish serve as hosts to a range of parasites that are taxonomically diverse and that exhibit a wide variety of life cycle strategies. Whereas many of these parasites are passed directly between ultimate hosts, others need to navigate through a series of intermediate hosts before reaching a host in (or on) which they can attain sexual maturity. The realisation that parasites need not have evolved to minimise their impact on hosts to be successful, and in many cases may even have a requirement for their hosts to be eaten by specific predators to ensure transmission, has renewed interest in the evolutionary basis of infection-associated host behaviour. Fishes have proved popular models for the experimental examination of such hypotheses, and parasitic infections have been demonstrated to have consequences for almost every aspect of fish behaviour. Despite a scarcity of knowledge regarding the mechanistic basis of such behaviour changes in most cases, and an even lower understanding of their ecological consequences, there can be little doubt that infection-associated behaviour changes have the potential to impact severely on the ecology of infected fishes. Changes in foraging efficiency, time budget, habitat selection, competitive ability, predator-prey relationships, swimming performance and sexual behaviour and mate choice have all been associated with – and in some cases been shown to be a result of – parasite infections, and are reviewed here in some detail. Since the behavioural consequences of infections are exposed to evolutionary selection pressures in the same way as are other phenotypic traits, few behavioural changes will be evolutionarily neutral and host behaviour changes that facilitate transmission should be expected. Despite this expectation, we have found little conclusive evidence for the Parasite Increased Trophic Transmission (PITT) hypothesis in fishes, though recent studies suggest it is likely to be an important mechanism. Additionally, since the fitness consequences of the many behavioural changes described have rarely been quantified, their evolutionary and ecological significance is effectively unknown.Potential hosts may also change their behaviour in the presence of infective parasite stages, if they adopt tactics to reduce exposure risk. Such `behavioural resistance', which may take the form of habitat avoidance, prey selectivity or avoidance of infected individuals, can be viewed as behavioural change associated with the threat of being parasitised, and so is included here. Actually harbouring infections may also stimulate fishes to perform certain types of simple or complex behaviours aimed at removing parasites, such as substrate scraping or the visitation of cleaning stations, although the efficacy of the latter as a parasite removal strategy is currently subject to a good deal of debate.The effects parasites have on shoaling behaviour of host fish have attracted a good deal of attention from researchers, and we have provided a case study to summarise the current state of knowledge. Parasites have been shown to affect most of the antipredator effects of shoaling (such as vigilance, co-ordinated evasion and predator confusion) and can also impair an individual's foraging ability. It therefore seems unsurprising that, in a number of species avoidance of parasitised individuals has evolved which may explain the occurrence of parasite-assorted shoals in the field. Parasitised fish are found more often in peripheral shoal positions and show a reduced tendency for shoaling in some fish species. Given the array of host behaviours that may be changed, the fitness consequences of shoal membership for parasitised hosts and their parasites are not always easy to predict, yet an understanding of these is important before we can make predictions regarding the ecological impact of infections on host fish populations.Clearly, there remain many gaps in our knowledge regarding the effects of parasites on the behaviour of host fish. We believe that a much greater understanding of the importance of infection-associated behaviour changes in fish could be gained from high quality research in comparatively few areas. We have completed our review by highlighting the key research topics that we believe should attract new research in this field.     

Parasites and phytoplankton, with special emphasis on dinoflagellate infections

Planktonic members of most algal groups are known to harbor intracellular symbionts, including viruses, bacteria, fungi, and protozoa. Among the dinoflagellates, viral and bacterial associations were recognized a quarter century ago, yet their impact on host populations remains largely unresolved. By contrast, fungal and protozoan infections of dinoflagellates are well documented and generally viewed as playing major roles in host population dynamics. Our understanding of fungal parasites is largely based on studies for freshwater diatoms and dinoflagellates, although fungal infections are known for some marine phytoplankton. In freshwater systems, fungal chytrids have been linked to mass mortalities of host organisms, suppression or retardation of phytoplankton blooms, and selective effects on species composition leading to successional changes in plankton communities. Parasitic dinoflagellates of the genus Amoebophrya and the newly described Perkinsozoa, Parvilucifera infectans, are widely distributed in coastal waters of the world where they commonly infect photosynthetic and heterotrophic dinoflagellates. Recent work indicates that these parasites can have significant impacts on host physiology, behavior, and bloom dynamics. Thus, parasitism needs to be carefully considered in developing concepts about plankton dynamics and the flow of material in marine food webs.     

Parasite-induced alteration of plastic response to predation threat: increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis

Larvae of many trophically-transmitted parasites alter the behaviour of their intermediate host in ways that increase their probability of transmission to the next host in their life cycle. Before reaching a stage that is infective to the next host, parasite larvae may develop through several larval stages in the intermediate host that are not infective to the definitive host. Early predation at these stages results in parasite death, and it has recently been shown that non-infective larvae of some helminths decrease such risk by enhancing the anti-predator defences of the host, including decreased activity and increased sheltering. However, these behavioural changes may divert infected hosts from an optimal balance between survival and foraging (either seeking food or a mate). In this study, this hypothesis was tested using the intermediate host of the acanthocephalan parasite Pomphorhynchus laevis, the freshwater amphipod Gammarus pulex. We compared activity, refuge use, food foraging and food intake of hosts experimentally infected with the non-infective stage (acanthella), with that of uninfected gammarids. Behavioural assays were conducted in four situations varying in predation risk and in food accessibility. Acanthella-infected amphipods showed an increase in refuge use and a general reduction in activity and food intake. There was no effect of parasite intensity on these traits. Uninfected individuals showed plastic responses to water-borne cues from fish by adjusting refuge use, activity and food intake. They also foraged more when the food was placed outside the refuge. At the intra-individual level, refuge use and food intake were positively correlated in infected gammarids only. Overall, our findings suggest that uninfected gammarids exhibit risk-sensitive behaviour including increased food intake under predation risk, whereas gammarids infected with the non-infective larvae of P. laevis exhibit a lower motivation to feed, irrespective of predation risk and food accessibility.     

Association between haematozoan infections and reproduction in the Pied Flycatcher

1. Parasites may affect breeding success of their host since they compete for the same resources as their hosts. Reproduction may also increase the susceptibility of a host to parasite infections owing to lowered resistance to parasites during breeding.
2. We studied the association between breeding performance and haematozoan parasite infection in the Pied Flycatcher ( Ficedula hypoleuca ) by using both natural data on reproduction and data from clutch size manipulations.
3. The most frequent blood parasites of the Pied Flycatcher in central Finland were Haemoproteus pallidus , Haemoproteus balmorali and Trypanosoma avium complex.
4. We did not find evidence that these haematozoan parasites have any debilitating effects on either reproduction or survival. The variation in reproductive effort did not seem to influence susceptibility to new blood parasite infections.
5. The intensity of Haemoproteus balmorali tended to increase in infected males as the brood size was artificially enlarged. Also, in females intensity of H. pallidus infection tended to increase with the level of clutch size manipulation. Thus, increased reproductive effort seems to debilitate the ability of Pied Flycatcher to control chronic infections.
6. Individuals with enlarged clutches/broods increased their reproductive effort at the expense of defence towards parasites. The cost of current reproduction may then be at least partly mediated by haematozoan infections.     

Predicting effects of naturally acquired abomasal nematode infections on growth rate and food intake in reindeer using serum pepsinogen levels

An experiment was performed on semiwild reindeer with naturally acquired parasite infections to assess whether measures of serum pepsinogen concentration and fecal egg counts can be used to predict effects of abomasal nematodes on reindeer weight gain and food intake. Food intake and weight gains were lower in infected calves compared with calves where parasites had been removed by anthelmintic treatment. Among the infected animals, concentration of pepsinogen in serum was correlated with food intake and weight gains. Concentration of abomasal nematode eggs in feces was not. Our results suggest that measures of pepsinogen levels in serum, but not fecal egg counts, may be used to predict the effects of abomasal nematodes on food intake and weight gain of reindeer.     

Frequency-dependent host selection by parasitic mites: a model and a case study

Previous studies on frequency-dependent food selection (changing food preferences in response to changes in relative food abundance) have focused on predators and parasitoids. These organisms utilize several victims during their lifetime. We introduce the case of parasites which, having accepted a host, do not change it. We propose two alternative models to explain the biased occurrence of parasites on different host types: (1) through the option of rejecting less-preferred hosts prior to accepting one of them; (2) by differential parasite survival on different host types. These models predict that host rejection, but not differential survival, can create frequency-dependent parasitism (FDP). Unlike previously described factors responsible for frequency dependence of food selection, which act through changing the foraging behaviour of individual predators or parasitoids, FDP involves no adjustment of parasite foraging strategy according to previous feeding experience. The mite Hemisarcoptes coccophagus is an obligate parasite of armoured scale insects (Homptera: Diaspididae). Our field data show that H. coccophagus is found more frequently on ovipositing than on young host females. Our model, combining the effects of host rejection and differential survival, is used to estimate the relative contribution of these factors to parasite biased occurrence on different hosts. The contribution of differential survival was dominant in H. coccophagus, and overode any effect of host rejection. Nevertheless, our prediction that FDP may be found in parasites is supported by literature data about a parasitic water mite.