Environmental parasitology: stressor effects on aquatic parasites

Anthropogenic stressors are causing fundamental changes in aquatic habitats and to the organisms inhabiting these ecosystems. Yet, we are still far from understanding the diverse responses of parasites and their hosts to these environmental stressors and predicting how these stressors will affect host–parasite communities. Here, we provide an overview of the impacts of major stressors affecting aquatic ecosystems in the Anthropocene (habitat alteration, global warming, and pollution) and highlight their consequences for aquatic parasites at multiple levels of organisation, from the individual to the community level. We provide directions and ideas for future research to better understand responses to stressors in aquatic host–parasite systems.     

Physiological stress links parasites to carotenoid‐based colour signals

Vertebrates commonly use carotenoid‐based traits as social signals. These can reliably advertise current nutritional status and health because carotenoids must be acquired through the diet and their allocation to ornaments is traded‐off against other self‐maintenance needs. We propose that the coloration more generally reveals an individual’s ability to cope with stressful conditions. We tested this idea by manipulating the nematode parasite infection in free‐living red grouse (Lagopus lagopus scoticus) and examining the effects on body mass, carotenoid‐based coloration of a main social signal and the amount of corticosterone deposited in feathers grown during the experiment. We show that parasites increase stress and reduce carotenoid‐based coloration, and that the impact of parasites on coloration was associated with changes in corticosterone, more than changes in body mass. Carotenoid‐based coloration appears linked to physiological stress and could therefore reveal an individual’s ability to cope with stressors.     

Epidemiology of honey bee parasites

The epidemiology of honey bee parasites has been somewhat neglected, but Lynn Royce and Philippe Rossignol describe their unique characteristics. Indeed, it appears that a parasite of social insects has in essence to adapt to two hosts: first, the individual worker within a colony, the numbers of which grow linearly and second, to the colony itself, the actual reproductive 'organism'. Transmission also has vertical and horizontal components. Analysis of tracheal mite populations in particular suggests that intracolony parasite levels are regulated by the swarming behavior of their hosts. Ironically, current and highly productive methods of honey bee management with movable hives curb swarming and may contribute to increasing the spread and the impact of some parasites. This insight may result in changing management practices to reduce the detrimental effects of bee parasites.     

Multiple zoosporic parasites pose a significant threat to amphibian populations

There is substantial evidence for the dominant role of Batrachochytrium dendrobatidis in amphibian population dynamics. However, a wide range of other pathogens could also be important in precipitating amphibian population declines, particularly in the face of climate change or other stressors. Here we discuss some examples of zoosporic parasites in the Chytridiomycota, Mesomycetozoa, Perkinsozoa and Oomycota, all of which infect amphibians in freshwater habitats. The pathosystem model provides an excellent basis for understanding host–parasite interactions. Chemotactic zoopores and several families of proteases facilitate infection. Introduction of non-native host may accelerate the dispersal of these parasites. Unlike B. dendrobatidis some of the other zoosporic parasites grow well at or slightly above 25 °C, and their growth rates are likely to increase with global warming. The interactions of parasites with each other and the combined effect of simultaneous infection with multiple species in amphibian populations remain to be carefully studied.     

Maternally transmitted parasite defence can be beneficial in the absence of parasites

Newborn animals do not have a fully functional immune system and are thus impaired in their ability to fight parasites. Mothers can therefore increase the survival probability of their young by providing them with passive immunity, e.g. in the form of maternal antibodies transferred via the placenta or the eggs. The maternal responses are only induced when parasites are present, and have been observed not only in vertebrates but also in invertebrates. However, while these parasite-induced maternal effects are known to reduce the harmful effects of common parasites, they may also impose costs for the young, either because the maternal response impairs parental performance, or because maternally transmitted products moderate offspring development. We experimentally tested these two hypotheses in a wild great tit population. We exposed birds to a common ectoparasite before egg-laying to induce the maternal response, and thereafter separated egg-mediated maternal effects from effects on post-laying parental performance by cross-fostering whole clutches. To assess the costs of this response without its confounding benefits, we kept nests free of parasites after hatching. Since the costs of maternal effects can be expressed differently under relaxed and harsh rearing conditions, we simultaneously manipulated clutch size. First, parasite-exposed parents raised lighter young, suggesting that parasite defence or the induced maternal response are costly to the parents and reduce their capacity to raise young. Second, under relaxed but not under harsh rearing conditions, young with the flea-induced maternal effect were heavier and were in better body condition than controls, suggesting that the maternally transferred products can be allocated to physiological functions beyond parasite defence.     

Effects of parasites on fish populations: practical considerations

Fish populations are subject to numerous natural and anthropogenic factors which reduce abundance. In wild populations it is difficult to isolate and quantify the effects of any single factor, such as prédation, or starvation, or disease, on fish stock size. Evidence is accumulating, however, which supports the notion that some of the animal parasites, and particularly the Protozoa, can act as severe pathogens, causing direct mortality or rendering the hosts more vulnerable to other environmental or biotic Stressors. Lethal effects of parasites can be determined statistically or by experiment, but actual observation of mortalities is rare—especially in the sea—principally because of prédation or scavenging. Sublethal effects (a partial misnomer since many such effects lead indirectly to mortality) include muscle degeneration, liver dysfunction, interference with nutrition, cardiac disruption, nervous system involvement, castration or mechanical interference with spawning, weight loss, and gross distortion of the body.Study of fish in captivity or under culture conditions has provided much information about the effects of animal parasites on survival. Epizootics occur, mortalities ensue, immunity may or may not develop, and parasites considered inocuous may prove to be not so under added Stressors such as crowding and poor water quality found in the culture environment.     

Ecosystem consequences of fish parasites*

In most aquatic ecosystems, fishes are hosts to parasites and, sometimes, these parasites can affect fish biology. Some of the most dramatic cases occur when fishes are intermediate hosts for larval parasites. For example, fishes in southern California estuaries are host to many parasites. The most common of these parasites, Euhaplorchis californiensis, infects the brain of the killifish Fundulus parvipinnis and alters its behaviour, making the fish 10–30 times more susceptible to predation by the birds that serve as its definitive host. Parasites like E. californiensis are embedded in food webs because they require trophic transmission. In the Carpinteria Salt Marsh estuarine food web, parasites dominate the links and comprise substantial amount of biomass. Adding parasites to food webs alters important network statistics such as connectance and nestedness. Furthermore, some free‐living stages of parasites are food items for free‐living species. For instance, fishes feed on trematode cercariae. Being embedded in food webs makes parasites sensitive to changes in the environment. In particular, fishing and environmental disturbance, by reducing fish populations, may reduce parasite populations. Indirect evidence suggests a decrease in parasites in commercially fished species over the past three decades. In addition, environmental degradation can affect fish parasites. For these reasons, parasites in fishes may serve as indicators of environmental impacts.     

Ecology of marine parasites

Important ecological aspects of marine parasites are discussed. Whereas effects of parasites on host individuals sometimes leading to death are known from many groups of parasites, effects on host populations have been studied much less. Mass mortalities have been observed mainly among hosts occurring in abnormally dense populations or after introduction of parasites by man. As a result of large-scale human activities, it becomes more and more difficult to observe effects of parasites on host populations under natural conditions. Particular emphasis is laid on ecological characteristics of parasites, such as host range and specificity, microhabitats, macrohabitats, food, life span, aggregated distribution, numbers and kinds of parasites, pathogenicity and mechanisms of reproduction and infection and on how such characteristics are affected by environment and hosts. It is stressed that host specificity indices which take frequency and/or intensity of infection into account, are a better measure of restriction of parasites to certain hosts than host range which simply is the number of host species found to be infected.     

Co‐infections by malaria parasites decrease feather growth but not feather quality in house martin

During moult, stressors such as malaria and related haemosporidian parasites (e.g. Plasmodium and Haemoproteus) could affect the growth rate and quality of feathers, which in turn may compromise future reproduction and survival. Recent advances in molecular methods to study parasites have revealed that co‐infections with multiple parasites are frequent in bird–malaria parasite systems. However, there is no study of the consequences of co‐infections on the moult of birds. In house martins Delichon urbica captured and studied at a breeding site in Europe during 11 yr, we measured the quality and the growth rate of tail feathers moulted in the African winter quarters in parallel with the infection status of blood parasites that are also transmitted on the wintering ground. Here we tested if the infection with two haemosporidian parasite lineages has more negative effects than a single lineage infection. We found that birds with haemosporidian infection had lower body condition. We also found that birds co‐infected with two haemosporidian lineages had the lowest inferred growth rate of their tail feathers as compared with uninfected and single infected individuals, but co‐infections had no effect on feather quality. In addition, feather quality was negatively correlated with feather growth rate, suggesting that these two traits are traded‐off against each other. We encourage the study of haemosporidian parasite infection as potential mechanism driving this trade‐off in wild populations of birds.     

Roles of parasites in animal invasions

Biological invasions are global threats to biodiversity and parasites might play a role in determining invasion outcomes. Transmission of parasites from invading to native species can occur, aiding the invasion process, whilst the 'release' of invaders from parasites can also facilitate invasions. Parasites might also have indirect effects on the outcomes of invasions by mediating a range of competitive and predatory interactions among native and invading species. Although pathogen outbreaks can cause catastrophic species loss with knock-on effects for community structure, it is less clear what impact persistent, sub-lethal parasitism has on native-invader interactions and community structure. Here, we show that the influence of parasitism on the outcomes of animal invasions is more subtle and wide ranging than has been previously realized.     

Protozoan parasites of British small rodents

Thirty-five species of protozoan parasites belonging to thirteen genera have now been recorded for British small rodents. These include species of Entamoeba, Giardia, Spironucleus, Trichomonas, Chilomastix, Eimeria and Cryptosporidium in the gut; Trypanosoma, Hepatozoon and Babesia in the blood; and Toxoplasma, Frenkelia and Sarcocystis in the tissues. Recent advances have progressed along two lines, the elucidation of the life-cycles of the species of Frenkelia and Sarcocystis , which are now known to involve a carnivore as the final host, and laboratory studies on those parasites that can be maintained in laboratory animals. It is now possible to draw up a definitive list of hosts and parasites and this should serve as a basis for studies on the epidemiology of these parasites and their possible effects on their hosts.     

Marine parasites: an Australian perspective

A review is given of major studies in marine parasitology in Australia. Aspects discussed include: geographical distribution of parasites in Australian coastal waters and their affinities to parasites of other zoogeographical regions; species diversity in Australian coastal surface and deep waters; use of marine parasites for stock discrimination; use of marine parasites as ecological models; ultrastructural and phylogenetic studies of marine parasites; and effects of marine parasites on their hosts.     

Sex, parasites and resistance--an evolutionary approach

Immune systems are among the most diverse biological systems. An evolutionary arms race between hosts and rapidly evolving pathogens is supposed to be a reason for this diversity, and might explain why most eukaryotic hosts and parasites reproduce sexually. In this review, I will focus on possible benefits of sexual reproduction in hosts and parasites, using a model system consisting of a tapeworm and its two intermediate hosts, copepods and sticklebacks. We found that the hermaphroditic tapeworms can increase their infection success by reproducing sexually with a partner (outcrossing), instead of reproducing alone. The defence system of the copepods provides highly specific discrimination of antigenic characteristics of the tapeworms. This supports the finding that tapeworms benefit from outcrossing, but contradicts the conventional notion that the immune system of invertebrates, in contrast to vertebrates, is not able to react with specificity. Finally, sticklebacks seem to benefit from optimal diversity in their specific immune system. Previous studies showed that female sticklebacks prefer mates, which sire offspring with an optimal diversity in the MHC (genes involved in antigen presentation). We now found that these individuals suffer less from tapeworm infection. Furthermore, they are able to reduce the expression of an unspecific immune trait, thereby possibly avoiding harmful side effects of a highly activated, unspecific immune system.     

The topoisomerases of protozoan parasites

Protozoan parasites are responsible for a wide range of debilitating and fatal diseases that are proving notoriously difficult to treat. Many of the standard chemotherapies in use today are expensive, have toxic side effects and, in some cases have marginal efficacy because of the emergence of drug-resistant parasites. In the search for more effective treatments, protozoan topoisomerases are now being considered as potential drug targets, building on the clinical success of anticancer and antibacterial agents that target human and bacterial topoisomerases. In this review, Sandra Cheesman explores progress in this relatively new but potentially important field of research.     

Cryopreservation of protozoan parasites

Conventional methods for the propagation and preservation of parasites in vivo or in vitro have some limitations, including the need for labor, initial isolation and loss of strains, bacterial, and fungal contamination, and changes in the original biological and metabolic characteristics. All these disadvantages are considerably reduced by cryopreservation. In this study, we examined the effects of various freezing conditions on the survival of several protozoan parasites after cryopreservation. The viability of Entamoeba histolytica was improved by seeding (p < 0.05, chi2 test), while this was not so effective for Trichomonas vaginalis. Of six cryoprotectants examined, dimethyl sulfoxide (Me(2)SO), and glycerol showed the strongest cryoprotective effects. The optimum conditions for using Me(2)SO were a concentration of 10% with no equilibration, and those for glycerol were a concentration of 15% with equilibration for 2h. The optimum cooling rate depended on the parasite species. Trypanosoma brucei gambiense and Leishmania amazonensis were successfully cryopreserved over a wide range of cooling rates, whereas the survival rates of E. histolytica, T. vaginalis, Pentatrichomonas hominis, and Blastocystis hominis were remarkably decreased when frozen at improper rates. Unlike the cooling rate, exposure of the protozoans to a rapid thawing method produced better motility for all parasites.     

Intraerythrocytic parasites and red cell deformability: Plasmodium berghei and Babesia microti

In the studies reported here, we examined the effects of two intraerythrocytic parasites (Plasmodium berghei and Babesia microti) on the deformability of their host red cells. Red cell deformability was assessed by three criteria: 1) the prevalence of tank-treading (the tank-tread-like movement of the red cell membrane around its cytoplasmic contents), 2) elongation under fluid shear stress (the steady-state length: width ratio), and 3) the time required for the red cell to reduce its steady-state elongation by 63.2% after the abrupt release of the shear stress (the characteristic shape-recovery time). Trophozoite-stage parasites of both species reduced the prevalence of tank-treading. Ring- and trophozoite-stage parasites of both species reduced steady-state elongation, and ring-stage P. berghei prolonged the shape-recovery time. These results suggest that altered red cell deformability is a common feature of infection with intraerythrocytic parasites.     

The effect of parasites on sex differences in selection

The life history strategies of males and females are often divergent, creating the potential for sex differences in selection. Deleterious mutations may be subject to stronger selection in males, owing to sexual selection, which can improve the mean fitness of females and reduce mutation load in sexual populations. However, sex differences in selection might also maintain sexually antagonistic genetic variation, creating a sexual conflict load. The overall impact of separate sexes on fitness is unclear, but the net effect is likely to be positive when there is a large sex difference in selection against deleterious mutations. Parasites can also have sex-specific effects on fitness, and there is evidence that parasites can intensify the fitness consequences of deleterious mutations. Using lines that accumulated mutations for over 60 generations, we studied the effect of the pathogenic bacterium Pseudomonas aeruginosa on sex differences in selection in the fruit fly Drosophila melanogaster. Pseudomonas infection increased the sex difference in selection, but may also have weakened the intersexual correlation for fitness. Our results suggest that parasites may increase the benefits of sexual selection.     

Effects of blood parasites on sexual and natural selection in the pied flycather

The occurrence of the blood parasites Haemoproteus and Trypanosoma in the pied flycatcher, Ficedula hypoleuca , was examined to test current hypotheses that parasites reduce the expression of secondary sexual traits, mating success, breeding success, and survival of infected individuals. The results showed that there was no significant relationship between male plumage brightness and Trypanosoma infection, but males infected with Haemoproteus tended to be brighter than uninfected males, partly because first-year males were less often infected than older males. Polygynous males did not have fewer parasites than monogamous males. Females did not choose uninfected males among those they had sampled. Clutch size and laying date were not related to female infection status, and the number and quality of nestlings was not related to parasite infections of either male or female parent. The ability of males to provide parental care was not related to their infection status. The return rate from one breeding season to the next of infected males was not lower than that of uninfected males. The lack of correlations between parasites and male plumage colour and female mate choice apparently do not support the Hamilton-Zuk hypothesis of sexual selection. However, the absence of demonstration of any negative effects of parasites suggests that infection status may not be a direct measure of parasite resistance, or the degree to which the host suffers. Instead, the results support the alternative view that infected individuals have demonstrated their ability to survive and to cope with the parasites, while uninfected individuals are probably not yet tested for their resistance. This points to problems in using parasite prevalences and distributions, at least of some protozoan blood parasites, for tests of Hamilton-Zuk hypothesis, even though this was done in the first test by Hamilton and Zuk and by many later researchers     

Coevolving parasites enhance the diversity-decreasing effect of dispersal

High dispersal rates between patches in spatially structured populations can impede diversification and homogenize diversity. These homogenizing effects of dispersal are likely to be enhanced by coevolving parasites that impose strong selection on hosts for resistance. However, the interactive effects of dispersal and parasites on host diversification have never been tested. We used spatially structured, experimental populations of the bacterium Pseudomonas fluorescens, cultured with or without the phage SBW25Ф2 under three levels of dispersal (none, localized or global), and quantified diversity in terms of evolved bacterial colony morphologies after approximately 100 bacterial generations. We demonstrate that higher levels of colony morphology richness evolved in the presence of phage, and that dispersal reduced diversity most strongly in the presence of phage. Thus, our results suggest that, while parasites can drive host diversification, host populations coevolving with parasites are more prone to homogenization through dispersal.