The role of specialist parasites in structuring host communities

Natural enemies can be a powerful force when structuring natural communities, and in facilitating or preventing species coexistence depending on the nature of the trophic interaction. In particular, “keystone” predators can promote species coexistence, provided they preferentially attack the competitively dominant species. However, it is not clear whether parasites can play a similar structuring role; parasites typically form chronic associations with their victims, reducing their fitness (i.e., fecundity) rather than survival, and allowing infected hosts to remain viable competitors within the community. Therefore the density-dependent suppression of the host is likely to be more subtle than that due to predation. Using a series of simple population-dynamic models we show that specialist parasites can facilitate species coexistence, although possibly less so than predators. These results contrast with those typically found with models of generalist parasites, which can reduce the likelihood of species coexistence through apparent competition. In addition, we show that the likelihood of parasite-facilitated species coexistence depends greatly on the specific type of parasite. In particular, macroparasites (e.g., parasitic helminths) may be less likely to facilitate species coexistence than microparasites (e.g., viruses or bacteria) due to their typically highly aggregated distribution amongst their hosts. Furthermore, species coexistence is more likely if the parasite is relatively benign to its host. Parasitism by apparently “harmless” specialist parasites may provide an important but overlooked factor in the maintenance of species diversity, facilitating species invasions into new communities and the emergence of novel infectious diseases.     

How parasites affect interactions between competitors and predators

We present a synthesis of empirical and theoretical work investigating how parasites influence competitive and predatory interactions between other species. We examine the direct and indirect effects of parasitism and discuss examples of density and parasite-induced trait-mediated effects. Recent work reveals previously unrecognized complexity in parasite-mediated interactions. In addition to parasite-modified and apparent competition leading to species exclusion or enabling coexistence, parasites and predators interact in different ways to regulate or destablize the population dynamics of their joint prey. An emerging area is the impact of parasites on intraguild predation (IGP). Parasites can increase vulnerability of infected individuals to cannibalism or predation resulting in reversed species dominance in IGP hierarchies. We discuss the potential significance of parasites for community structure and biodiversity, in particular their role in promoting species exclusion or coexistence and the impact of emerging diseases. Ongoing invasions provide examples where parasites mediate native/invader interactions and play a key role in determining the outcome of invasions. We highlight the need for more quantitative data to assess the impact of parasites on communities, and the combination of theoretical and empirical studies to examine how the effects of parasitism scale up to community-level processes.     

Helminths as heirlooms and souvenirs: a review of new world paleoparasitology

Evidence from studies on ancient human feces, intestinal contents and organs of preserved bodies has established that Enterobius vermicularis, Trichuris trichiura, Diphyllobothrium spp and probably Trichinella spiralis infected humans in the pre-Columbian New World. These species, and perhaps other common human helminths for which there is not yet convincing evidence, probably accompanied transberingeal immigrants and their dogs, and thus can be seen as heirloom parasites. Early humans on the American continents were affected by helminths of native animals such as Paragonimus and Cryptocotyle, and these have also been found in precontact human remains. Michael Kliks considers that the indigenous parasites infecting early Americans may be viewed as zoonotic souvenirs of some 50 millennia of migrations from Alaska to Patagonia. Among the most serious zoonoses would have been infection by cystic hydatid larvae of echinococcid tapeworms, the many enzootic filarial worms, and a variety of larval trematodes and nematodes.     

Parasites of Aquatic Exotic Invertebrates: Identification of Potential Risks Posed to the Great Lakes

Exotic species typically lose most of their associated parasites during long-distance spread. However, the few parasites that are co-introduced may have considerable adverse impacts on their novel hosts, including mass mortalities. We present a comprehensive inventory of parasites known to infect 38 species of exotic invertebrates established in the Great Lakes, as well as 16 invertebrate species predicted to arrive in the near future, all of them crustaceans. Based on a literature analysis, we identified a total of 277 parasite taxa associated with the examined invertebrates in their native ranges and/or invaded areas. Of these parasites, 56 species have been documented to cause various pathologies in their intermediate or final hosts, with humans and fishes being the most frequently affected host categories. Potentially harmful parasites were identified in 61% of the invaders for which published information was retrieved (in their ranges outside of the Great Lakes), with molluscs and crustaceans hosting the highest numbers of such parasites. The results of our study provide a baseline for further assessment and management of the parasitological risks posed by exotic species to the Great Lakes.     

Effects of a hurricane on fish parasites

Hurricanes, also called tropical cyclones, can dramatically affect life along their paths, including a temporary losing or reducing in number of parasites of fishes. Hurricane Katrina in the northern Gulf of Mexico in August 2005 provides many examples involving humans and both terrestrial and aquatic animals and plants. Fishes do not provide much of an indicator of hurricane activity because most species quickly repopulate the area. Fish parasites, however, serve as a good indicator of the overall biodiversity and environmental health. The reasons for the noted absence or reduction of parasites in fishes are many, and specific parasites provide indications of different processes. The powerful winds can produce perturbations of the sediments harboring intermediate hosts. The surge of high salinity water can kill or otherwise affect low salinity intermediate hosts or free-living stages. Both can introduce toxicants into the habitat and also interfere with the timing and processes involved with host-parasite interrelationships. All these have had a major influence on fish parasite populations of fishes in coastal Mississippi, especially for those parasites incorporating intermediate hosts in their life cycles. The length of time for a parasite to become re-established can vary considerably, depending on its life cycle as well as the associated biota, habitat, and environmental conditions, and each parasite provides a special indicator of environmental health.     

Host immune function and sexual selection in birds

Parasites have been hypothesized to affect sexual selection of their hosts, if secondary sexual characters reliably signal absence of infectious parasites, superior parenting ability caused by the absence of parasites, or heritable resistance to parasites, for which there is some intraspecific and interspecific evidence. Measures of immune defence of hosts provide reliable information on the current infection status of individuals of the chosen sex, usually males, and correlations between immune defence and development of secondary sexual characters thus provide a novel critical test of parasite-mediated sexual selection. In a comparative study of birds, sexually dichromatic species had higher immune defences, measured in terms of leukocyte concentration and the size of spleen and bursa of Fabricius, respectively, than closely related, monochromatic species. Male plumage brightness was consistently negatively related to the size of the spleen in males of sexually dichromatic species, but not in males of monochromatic species. Hence, the brightest males, which frequently are preferred as mates by choosy females, had low levels of immune defence, suggesting that such males were healthy. This provides evidence for a general role of parasites in sexual selection among their bird hosts.     

From micro- to macroevolution: brood parasitism as a driver of phenotypic diversity in birds

A fundamental question in biology is how diversity evolves and why some clades are more diverse than others. Phenotypic diversity has often been shown to result from morphological adaptation to different habitats. The role of behavioral interactions as a driver of broadscale phenotypic diversity has received comparatively less attention. Behavioral interactions, however, are a key agent of natural selection. Antagonistic behavioral interactions with predators or with parasites can have significant fitness consequences, and hence act as strong evolutionary forces on the phenotype of species, ultimately generating diversity between species of both victims and exploiters. Avian obligate brood parasites lay their eggs in the nests of other species, their hosts, and this behavioral interaction between hosts and parasites is often considered one of the best examples of coevolution in the natural world. In this review, we use the coevolution between brood parasites and their hosts to illustrate the potential of behavioral interactions to drive evolution of phenotypic diversity at different taxonomic scales. We provide a bridge between behavioral ecology and macroevolution by describing how this interaction has increased avian phenotypic diversity not only in the brood parasitic clades but also in their hosts.     

Fossils of parasites: what can the fossil record tell us about the evolution of parasitism?

Parasites are common in many ecosystems, yet because of their nature, they do not fossilise readily and are very rare in the geological record. This makes it challenging to study the evolutionary transition that led to the evolution of parasitism in different taxa. Most studies on the evolution of parasites are based on phylogenies of extant species that were constructed based on morphological and molecular data, but they give us an incomplete picture and offer little information on many important details of parasite–host interactions. The lack of fossil parasites also means we know very little about the roles that parasites played in ecosystems of the past even though it is known that parasites have significant influences on many ecosystems. The goal of this review is to bring attention to known fossils of parasites and parasitism, and provide a conceptual framework for how research on fossil parasites can develop in the future. Despite their rarity, there are some fossil parasites which have been described from different geological eras. These fossils include the free‐living stage of parasites, parasites which became fossilised with their hosts, parasite eggs and propagules in coprolites, and traces of pathology inflicted by parasites on the host's body. Judging from the fossil record, while there were some parasite–host relationships which no longer exist in the present day, many parasite taxa which are known from the fossil record seem to have remained relatively unchanged in their general morphology and their patterns of host association over tens or even hundreds of millions of years. It also appears that major evolutionary and ecological transitions throughout the history of life on Earth coincided with the appearance of certain parasite taxa, as the appearance of new host groups also provided new niches for potential parasites. As such, fossil parasites can provide additional data regarding the ecology of their extinct hosts, since many parasites have specific life cycles and transmission modes which reflect certain aspects of the host's ecology. The study of fossil parasites can be conducted using existing techniques in palaeontology and palaeoecology, and microscopic examination of potential material such as coprolites may uncover more fossil evidence of parasitism. However, I also urge caution when interpreting fossils as examples of parasites or parasitism‐induced traces. I point out a number of cases where parasitism has been spuriously attributed to some fossil specimens which, upon re‐examination, display traits which are just as (if not more) likely to be found in free‐living taxa. The study of parasite fossils can provide a more complete picture of the ecosystems and evolution of life throughout Earth's history.     

Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.     

The role of seabirds of the Iles Eparses as reservoirs and disseminators of parasites and pathogens

The role of birds as reservoirs and disseminators of parasites and pathogens has received much attention over the past several years due to their high vagility. Seabirds are particularly interesting hosts in this respect. In addition to incredible long-distance movements during migration, foraging and prospecting, these birds are long-lived, site faithful and breed in dense aggregations in specific colony locations. These different characteristics can favor both the local maintenance and large-scale dissemination of parasites and pathogens. The Iles Eparses provide breeding and feeding grounds for more than 3 million breeding pairs of seabirds including at least 13 species. Breeding colonies on these islands are relatively undisturbed by human activities and represent natural metapopulations in which seabird population dynamics, movement and dispersal can be studied in relation to that of circulating parasites and pathogens. In this review, we summarize previous knowledge and recently-acquired data on the parasites and pathogens found in association with seabirds of the Iles Eparses. These studies have revealed the presence of a rich diversity of infectious agents (viruses, bacteria and parasites) carried by the birds and/or their local ectoparasites (ticks and louse flies). Many of these agents are widespread and found in other ecosystems confirming a role for seabirds in their large scale dissemination and maintenance. The heterogeneous distribution of parasites and infectious agents among islands and seabird species suggests that relatively independent metacommunities of interacting species may exist within the western Indian Ocean. In this context, we discuss how the patterns and determinants of seabird movements may alter parasite and pathogen circulation. We conclude by outlining key aspects for future research given the baseline data now available and current concerns in eco-epidemiology and biodiversity conservation.     

Evolution of pathogens in a man-made world.

Human activities have resulted in substantial, large-scale environmental modifications, especially in the past century. Ecologists and evolutionary biologists are increasingly coming to realize that parasites and pathogens, like free-living organisms, evolve as the consequence of these anthropogenic changes. Although this area now commands the attention of a variety of researchers, a broad predictive framework is lacking, mainly because the links between human activities, the environment and parasite evolution are complex. From empirical and theoretical examples chosen in the literature, we give an overview of the ways in which humans can directly or indirectly influence the evolution of different traits in parasites (e.g. specificity, virulence, polymorphism). We discuss the role of direct and indirect factors as diverse as habitat fragmentation, pollution, biodiversity loss, climate change, introduction of species, use of vaccines and antibiotics, ageing of the population, etc. We also present challenging questions for further research. Understanding the links between anthropogenic changes and parasite evolution needs to become a cornerstone of public health planning, economic development and conservation biology.     

Coevolution is linked with phenotypic diversification but not speciation in avian brood parasites

Coevolution is often invoked as an engine of biological diversity. Avian brood parasites and their hosts provide one of the best-known examples of coevolution. Brood parasites lay their eggs in the nests of other species, selecting for host defences and reciprocal counteradaptations in parasites. In theory, this arms race should promote increased rates of speciation and phenotypic evolution. Here, we use recently developed methods to test whether the three largest avian brood parasitic lineages show changes in rates of phenotypic diversity and speciation relative to non-parasitic lineages. Our results challenge the accepted paradigm, and show that there is little consistent evidence that lineages of brood parasites have higher speciation or extinction rates than non-parasitic species. However, we provide the first evidence that the evolution of brood parasitic behaviour may affect rates of evolution in morphological traits associated with parasitism. Specifically, egg size and the colour and pattern of plumage have evolved up to nine times faster in parasitic than in non-parasitic cuckoos. Moreover, cuckoo clades of parasitic species that are sympatric (and share similar host genera) exhibit higher rates of phenotypic evolution. This supports the idea that competition for hosts may be linked to the high phenotypic diversity found in parasitic cuckoos.     

Phylogenetic systematics and evolution of primate-derived Pneumocystis based on mitochondrial or nuclear DNA sequence comparison

Previous studies have demonstrated that the agent of Pneumocystis pneumonia (PcP), Pneumocystis carinii, is actually a complex of eukaryotic organisms, and cophylogeny could explain the distribution of the hosts and parasites. In the present work, we tested the hypothesis of cophylogeny between the primate-derived Pneumocystis group and their hosts. Specific strains isolated from 20 primate species, including humans, were used to produce a phylogeny of the parasites. Aligned sequences corresponding to DNA sequences of three genes (DHPS, mtSSU-rRNA, and mtLSU-rRNA) were separately analyzed and then combined in a single data set. The resulting parasite phylogeny was compared with different controversial phylogenies for the hosts. This comparison demonstrated that, depending upon which topology is accepted for the hosts, at least 61% and perhaps 77% of the homologous nodes of the respective cladograms of the hosts and parasites may be interpreted as resulting from codivergence events. This finding and the high specificity of these parasites suggests that cophylogeny may be considered the dominant pattern of evolution for Pneumocystis organisms, representing a new example of parallel evolution between primates and their specific parasites. Because the phylogeny of Pneumocystis followed very closely the differentiation of their hosts at the species level, the study of the parasites could provide valuable information on the phylogeny of their hosts. We used this information to explore controversial hypotheses of the phylogeny of the Platyrrhini by comparison with the phylogeny of their specific Pneumocystis parasites. If these organisms were closely associated as lung parasites with primates through the ages, the hypothesis of the Pneumocystis spp. being new pathogenic agents could be refuted. However, these organisms are opportunistic symbionts, becoming pathogenic whenever the immunological defences of their hosts decline. This study also provides support for the hypothesis that the different Pneumocystis species are genetically independent organisms, helping to clarify their taxonomic status.     

Costs to host defence and the persistence of parasitic cuckoos.

Raising genetically unrelated young is maladaptive, yet brood parasitism is widespread in birds. In several systems, hosts can evolve near-perfect defences against the parasite (discrimination and rejection of unlike eggs), making it difficult to understand how the parasite continues to exist. This study demonstrates costs to host defences (e.g. rejection of one's own eggs) such that once the parasite goes extinct on a particular host species, defence mechanisms are selectively disadvantageous. The consequent loss of host defences, and potential for re-exploitation of the host by the parasite, can explain the continued persistence of avian brood parasites. The results provide one general explanation for coexistence of parasites and their hosts.     

The functional importance of parasites in animal communities: many roles at many levels?

Past research on parasites and community ecology has focussed on two distinct levels of the overall community. First, it has been shown that parasites can have a role in structuring host communities. They can have differential effects on the different hosts that they exploit, they can directly debilitate a host that itself is a key structuring force in the community, or they can indirectly alter the phenotype of their host and change the importance of the host for the community. Second, certain parasite species can be important in shaping parasite communities. Dominant parasite species can directly compete with other parasite species inside the host and reduce their abundance to some extent, and parasites that alter host phenotype can indirectly make the host more or less suitable for other parasite species. The possibility that a parasite species simultaneously affects the structure of all levels of the overall community, i.e. the parasite community and the community of free-living animals, is never considered. Given the many direct and indirect ways in which a parasite species can modulate the abundance of other species, it is conceivable that some parasite species have functionally important roles in a community, and that their removal would change the relative composition of the whole community. An example from a soft-sediment intertidal community is used to illustrate how the subtle, indirect effects of a parasite species on non-host species can be very important to the structure of the overall community. Future community studies addressing the many potential influences of parasites will no doubt identify other functionally important parasite species that serve to maintain biodiversity.     

Spread of parasites and diseases of aquatic organisms by acclimatization: a short review

The influence of transportation and acclimatization of fishes and shellfishes on their parasites and pathogens is discussed. It has been shown that aquatic organisms lose most of their parasites during the period of establishment, but some species may remain. In most instances these are parasites with direct development (Myxosporea, Monogenea, Crustacea). Species with intermediate hosts, but which utilize many species of invertebrates, establish more easily than those which have specific invertebrate intermediate hosts. If there are closely related host species to those introduced into the water body, parasites brought to it can transfer to these related species. This may result in a high infection of the native species and significant mortality.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

Food webs: a plea for parasites

Parasites have the capacity to regulate host populations and may be important determinants of community structure, yet they are usually neglected in studies of food webs. Parasites can provide much of the information on host biology, such as diet and migration, that is necessary to construct accurate webs. Because many parasites have complex life cycles that involve several different hosts, and often depend on trophic interactions for transmission, parasites provide complementary views of web structure and dynamics. Incorporation of parasites in food webs can substantially after baste web properties, Including connectance, chain length and proportions of top and basal species, and can allow the testing of specific hypotheses related to food-web dynamics.     

Component communities of the parasites of gudgeon (Gobio gobio) from the basins of Northern Dvina and Mezen rivers

Component communities of parasites of gudgeon from the ecologically sustainable reservoirs are studied. The general principle of their organization is established. The material had been collected in the basins of Northern Dvina (41 specimens of gudgeon were dissected) and Mezen (55 specimens of gudgeon were dissected) rivers using generally accepted methods. Errors of regression equations for all individual species groups with their subsequent summation were calculate in order to estimate the state of the component community structure. In different seasons of a year the component community of the parasites of gudgeon from the Ertom river has the same structure, which is determined by the ratio of the biomasses of its comprising species, while it is differs in its species composition, biomasses of the species, leading groups of parasites, and in the dominating species. Thus, several stable seasonal states of the communities of fish parasites can be supposed. Three groups of species distinguished by the ratio of their biomasses are the general for the component communities of the parasites of gudgeon from the basins of Northern Dvina and Mezen rivers. The generalist species is more frequently the dominating species. The group of autogenic species always leads in the community. When methods of parasites collection are violated, the decrease in the number of species groups down to two is recorded. When the materials collected in different periods of a year from an ecologically sustainable reservoir are mixed, the sum of the errors of regression equations become higher than 0.250.     

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.