Health of Antarctic birds: a review of their parasites,pathogens and diseases

Antarctic birds are not beyond the effects of parasites or pathogens. However, potential ecological consequences of wide-spread infections for bird populations in Antarctica have received little attention. In this paper, we review the information published about disease and parasites, and their effects on Antarctic birds. The information on host species, parasites and pathogens, and geographic regions is incomplete and data on ecological effects on the populations, including how birds respond to pathogens and parasites, are almost inexistent. We conclude that more research is needed to establish general patterns of spatial and temporal variation in pathogens and parasites, and to determine how such patterns could influence hosts. This information is crucial to limit the spread of outbreaks and may aid in the decision-making process should they occur.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

Abundance-variance and abundance-occupancy relationships in a marine host-parasite system: the importance of taxonomy and ecology of transmission

Abundance-occupancy and abundance-variance relationships are two of the most general macroecological patterns capturing essential fundamentals of the structuring of species distributions and are widely documented for free-living animal and plant species populations at different spatial scales. However, empirical data for parasites have been gathered using appropriate sampling designs only recently. We performed analyses across species of the variation in infection parameters and patterns of aggregation of the most widespread parasites in the marine sparid fish Boops boops across seven localities of two marine biogeographical regions, the North East Atlantic and the Mediterranean. We used a large dataset of multiple population samples replicated over time for 20 parasite species and carried out assessments both intraspecifically and interspecifically, across taxonomic and ecological groupings. This taxonomically diverse complex of species representing five major metazoan higher taxa with differing transmission ecologies allowed us to assess the effect of taxonomic and ecological determinants on the abundance-occupancy and abundance-variance relationships in the model marine host-parasite system. The results revealed that: (i) a power function, relating spatial variance to mean abundance, represents a suitable model for the spatial distribution of the species; (ii) prevalence, abundance and the degree of spatial heterogeneity are true species characteristics and differ consistently between higher level taxonomic groupings; (iii) infection parameters and abundance-variance relationship are dependent on host specificity and regional distribution patterns of the parasites; and (iv) the observed infection parameters agree well with predictions from the epidemiological negative binomial abundance-occupancy model built on parameters of Taylor's power law both within and across species.     

Spatial heterogeneity of daphniid parasitism within lakes

Spatially explicit models show that local interactions of hosts and parasites can strongly influence invasion and persistence of parasites and can create lasting spatial patchiness of parasite distributions. These predictions have been supported by experiments conducted in two-dimensional landscapes. Yet, three-dimensional systems, such as lakes, ponds, and oceans, have received comparatively little attention from epidemiologists. Freshwater zooplankton hosts often aggregate horizontally and vertically in lakes, potentially leading to local host–parasite interactions in one-, two-, or three-dimensions. To evaluate the potential spatial component of daphniid parasitism driven by these local interactions (patchiness), we surveyed vertical and horizontal heterogeneity of pelagic Daphnia infected with multiple microparasites in several north temperate lakes. These surveys uncovered little evidence for persistent vertical patchiness of parasitism, since the prevalence of two parasites showed little consistent trend with depth in four lakes (but more heterogeneity during day than at night). On a horizontal scale of tens of meters, we found little systematic evidence of strong aggregation and spatial patterning of daphniid hosts and parasites. Yet, we observed broad-scale, basin-wide patterns of parasite prevalence. These patterns suggest that nearshore offshore gradients, rather than local-scale interactions, could play a role in governing epidemiology of this open water host–parasite system. Electronic Supplementary Material Supplementary material is available for this article at     

Spatial patterns,ecological niches,and interspecific competition of avian brood parasites: inferring from a case study of Korea

Since obligate avian brood parasites depend completely on the effort of other host species for rearing their progeny, the availability of hosts will be a critical resource for their life history. Circumstantial evidence suggests that intense competition for host species may exist not only within but also between species. So far, however, few studies have demonstrated whether the interspecific competition really occurs in the system of avian brood parasitism and how the nature of brood parasitism is related to their niche evolution. Using the occurrence data of five avian brood parasites from two sources of nationwide bird surveys in South Korea and publically available environmental/climatic data, we identified their distribution patterns and ecological niches, and applied species distribution modeling to infer the effect of interspecific competition on their spatial distribution. We found that the distribution patterns of five avian brood parasites could be characterized by altitude and climatic conditions, but overall their spatial ranges and ecological niches extensively overlapped with each other. We also found that the predicted distribution areas of each species were generally comparable to the realized distribution areas, and the numbers of individuals in areas where multiple species were predicted to coexist showed positive relationships among species. In conclusion, despite following different coevolutionary trajectories to adapt to their respect host species, five species of avian brood parasites breeding in South Korea occupied broadly similar ecological niches, implying that they tend to conserve ancestral preferences for ecological conditions. Furthermore, our results indicated that contrary to expectation interspecific competition for host availability between avian brood parasites seemed to be trivial, and thus, play little role in shaping their spatial distributions and ecological niches. Future studies, including the complete ranges of avian brood parasites and ecological niches of host species, will be worthwhile to further elucidate these issues.     

Spatiotemporal patterns of avian host–parasite interactions in the face of biogeographical range expansions

Exploration of interactions between hosts and parasitic symbionts is important for our understanding of the temporal and spatial distribution of organisms. For example, host colonization of new geographical regions may alter levels of infections and parasite specificity, and even allow hosts to escape from co‐evolved parasites, consequently shaping spatial distributions and community structure of both host and parasite. Here we investigate the effect of host colonization of new regions and the elevational distribution of host–parasite associations between birds and their vector‐transmitted haemosporidian blood parasites in two geological and geographical settings: mountains of New Guinea and the Canary Islands. Our results demonstrate that bird communities in younger regions have significantly lower levels of parasitism compared to those of older regions. Furthermore, host–parasite network analyses demonstrate that blood parasites may respond differently after arriving to a new region, through adaptations that allow for either expanding (Canary Islands) or retaining (New Guinea) their host niches. The spatial prevalence patterns along elevational gradients differed in the two regions, suggesting that region‐specific biotic (e.g., host community) and abiotic factors (e.g., temperature) govern prevalence patterns. Our findings suggest that the spatiotemporal range dynamics in host–parasite systems are driven by multiple factors, but that host and parasite community compositions and colonization histories are of particular importance.     

Host diversity drives parasite diversity: meta‐analytical insights into patterns and causal mechanisms

Statistical correlations of biodiversity patterns across multiple trophic levels have received considerable attention in various types of interacting assemblages, forging a universal understanding of patterns and processes in free‐living communities. Host–parasite interactions present an ideal model system for studying congruence of species richness among taxa as obligate parasites are strongly dependent upon the availability of their hosts for survival and reproduction while also having a tight coevolutionary relationship with their hosts. The present meta‐analysis examined 38 case studies on the relationship between species richness of hosts and parasites, and is the first attempt to provide insights into the patterns and causal mechanisms of parasite biodiversity at the community level using meta‐regression models. We tested the distinct role of resource (i.e. host) availability and evolutionary co‐variation on the association between biodiversity of hosts and parasites, while spatial scale of studies was expected to influence the extent of this association. Our results demonstrate that species richness of parasites is tightly correlated with that of their hosts with a strong average effect size (r= 0.55) through both host availability and evolutionary co‐variation. However, we found no effect of the spatial scale of studies, nor of any of the other predictor variables considered, on the correlation. Our findings highlight the tight ecological and evolutionary association between host and parasite species richness and reinforce the fact that host–parasite interactions provide an ideal system to explore congruence of biodiversity patterns across multiple trophic levels.     

Host and parasite recruitment correlated at a regional scale

Drivers of large-scale variability in parasite prevalence are not well understood. For logistical reasons, explorations of spatial patterns in parasites are often performed as observational studies. However, to understand the mechanisms that underlie these spatial patterns, standardized and controlled comparisons are needed. Here, we examined spatial variability in infection of an important fishery species and ecosystem engineer, the oyster (Crassostrea virginica) by its pea crab parasite (Zaops ostreus) across 700 km of the southeastern USA coastline. To minimize the influence of host genetics on infection patterns, we obtained juvenile oysters from a homogeneous source stock and raised them in situ for 3 months at multiple sites with similar environmental characteristics. We found that prevalence of pea crab infection varied between 24 and 73 % across sites, but not systematically across latitude. Of all measured environmental variables, oyster recruitment correlated most strongly (and positively) with pea crab infection, explaining 92 % of the variability in infection across sites. Our data ostensibly suggest that regional processes driving variation in oyster recruitment similarly affect the recruitment of one of its common parasites.     

Host resistance and coevolution in spatially structured populations

Natural, agricultural and human populations are structured, with a proportion of interactions occurring locally or within social groups rather than at random. This within-population spatial and social structure is important to the evolution of parasites but little attention has been paid to how spatial structure affects the evolution of host resistance, and as a consequence the coevolutionary outcome. We examine the evolution of resistance across a range of mixing patterns using an approximate mathematical model and stochastic simulations. As reproduction becomes increasingly local, hosts are always selected to increase resistance. More localized transmission also selects for higher resistance, but only if reproduction is also predominantly local. If the hosts disperse, lower resistance evolves as transmission becomes more local. These effects can be understood as a combination of genetic (kin) and ecological structuring on individual fitness. When hosts and parasites coevolve, local interactions select for hosts with high defence and parasites with low transmissibility and virulence. Crucially, this means that more population mixing may lead to the evolution of both fast-transmitting highly virulent parasites and reduced resistance in the host.     

Dispersal and natural enemies interact to drive spatial synchrony and decrease stability in patchy populations

Spatial synchrony is widespread in natural populations but the mechanisms that underpin it are not yet fully understood. Two key biotic drivers of spatial synchrony have been identified: dispersal and trophic interactions (e.g. natural enemies). We used spatially structured, patchy bacterial populations to show that although increased dispersal always enhanced spatial synchrony of fluctuations in bacterial abundance, this effect was far stronger in the presence of a bacteriophage parasite. Bacteriophages drove strong within patch fluctuations in bacterial abundance that became phase locked through dispersal. Furthermore, the way in which stability, measured as constancy, responded to increasing dispersal was qualitatively different depending on whether parasites were present or not. Patch-level constancy decreased with dispersal in the presence of parasites, whereas dispersal increased patch-level constancy in the absence of parasites. Population-level constancy also decreased with dispersal in the presence of parasites, but was unaffected by dispersal in the absence of parasites. These contrasting patterns were likely due to the different role played by dispersal in the presence and absence of parasites, synchronizing dynamics in the former case and averaging stochastic fluctuations in the latter. Taken together, our findings suggest that dispersal and natural enemies can interact to drive spatially synchronous population fluctuations that decrease stability at both the patch and population level.     

Host species,and not environment,predicts variation in blood parasite prevalence,distribution, and diversity along a humidity gradient in northern South America

Environmental factors strongly influence the ecology and evolution of vector‐borne infectious diseases. However, our understanding of the influence of climatic variation on host–parasite interactions in tropical systems is rudimentary. We studied five species of birds and their haemosporidian parasites (Plasmodium and Haemoproteus) at 16 sampling sites to understand how environmental heterogeneity influences patterns of parasite prevalence, distribution, and diversity across a marked gradient in water availability in northern South America. We used molecular methods to screen for parasite infections and to identify parasite lineages. To characterize spatial heterogeneity in water availability, we used weather‐station and remotely sensed climate data. We estimated parasite prevalence while accounting for spatial autocorrelation, and used a model selection approach to determine the effect of variables related to water availability and host species on prevalence. The prevalence, distribution, and lineage diversity of haemosporidian parasites varied among localities and host species, but we found no support for the hypothesis that the prevalence and diversity of parasites increase with increasing water availability. Host species and host × climate interactions had stronger effects on infection prevalence, and parasite lineages were strongly associated with particular host species. Because climatic variables had little effect on the overall prevalence and lineage diversity of haemosporidian parasites across study sites, our results suggest that independent host–parasite dynamics may influence patterns in parasitism in environmentally heterogeneous landscapes.     

Scaling up from epidemiology to biogeography: local infection patterns predict geographical distribution in fish parasites

Aim We investigated how the spatial distribution of parasites, measured as either their geographical range size or their frequency of occurrence among localities, relates to either their average local abundance or the variance in their abundance among localities where they occur. Location We used data on the abundance of 46 metazoan parasite species in 66 populations of threespine sticklebacks, Gasterosteus aculeatus, from Europe and North America. Methods For each parasite species, frequency of occurrence was calculated as the proportion of stickleback populations in which it occurred, and geographical range size as the area within the smallest possible polygon delimited using the coordinates of the localities where it occurred. Generalized linear models were used to assess how these two measures of spatial distribution were influenced by several predictor variables: geographical region (North America or Europe), life cycle (simple or complex), average local abundance, the coefficient of variation in abundance across localities, and median prevalence (proportion of infected hosts within a locality). Results Our analyses uncovered four patterns. First, parasites in North America tend to have higher frequencies of occurrence among surveyed localities, but not broader geographical ranges, than those in Europe. Second, parasite species with simple life cycles have wider geographical ranges than those with complex cycles. Third, there was a positive relationship between average abundance of the different parasite species and their frequency of occurrence, but not between average abundance and geographical range size. Fourth, the coefficient of variation in abundance covaried positively with both the frequency of occurrence and geographical range size across the different parasite species. Thus, all else being equal, parasites showing greater site‐to‐site variability in abundance occur in a greater proportion of localities and over a broader geographical area than those with a more stable abundance among sites. Main conclusions Local infection patterns are linked with large‐scale distributional patterns in fish parasites, independently of host effects, such that local commonness translates into regional commonness. The mechanisms linking parasite success at both scales remain unclear, but may include those that maintain the continuum between specialist and generalist parasites. Regardless, the observed patterns have implications for the predicted changes in the geographical distributions of many parasites in response to climate change.     

Patterns of association, nestedness, and species co-occurrence of helminth parasites in the greater kudu, Tragelaphus strepsiceros, in the Kruger National Park, South Africa, and the Etosha National Park, Namibia

The helminth parasites of the greater kudu from the Kruger National Park (KNP), South Africa, and the Etosha National Park (ENP), Namibia, were examined to determine the major patterns of spatial and demographic variation in community structure and to evaluate nonrandomness in parasite community assembly. Nonmetric multidimensional scaling ordination procedures were used to test for differences in parasite community composition between hosts of the 2 parks and between hosts of different demographic groups within KNP. Infracommunities within KNP were also examined for patterns of nonrandomness using 2 null models, i.e., nestedness and species co-occurrence. Infracommunities of KNP and ENP were significantly different from each other, as were infracommunities of different host demographic groups within KNP. Parasite species in the greater kudu from KNP displayed significant levels of nestedness and were found to co-occur less frequently than expected by chance; however, this lack of co-occurrence was significant only when all demographic groups were considered. When restricted to any particular age class, co-occurrence patterns could not be distinguished from random. Overall, these data suggest that biogeography and host demographics are important factors in determining community organization of helminth parasites in the greater kudu.     

The Role of Complex Formation and Deleterious Mutations for the Stability of RNA-Like Replicator Systems

In the RNA world hypothesis, RNA(-like) self-replicators are suggested as the central player of prebiotic evolution. However, there is a serious problem in the evolution of complexity in such replicators, i.e., the problem of parasites. Parasites, which are replicated by catalytic replicators (catalysts), but do not replicate the others, can destroy a whole replicator system by exploitation. Recently, a theoretical study underlined complex formation between replicators--an often neglected but realistic process--as a stabilizing factor in a replicator system by demonstrating that complex formation can shift the viable range of diffusion intensity to higher values. In the current study, we extend the previous study of complex formation. Firstly, by investigating a well-mixed replicator system, we establish that complex formation gives parasites an implicit advantage over catalysts, which makes the system significantly more vulnerable to parasites. Secondly, by investigating a spatially extended replicator system, we show that the formation of traveling wave patterns plays a crucial role in the stability of the system against parasites, and that because of this the effect of complex formation is not straightforward; i.e., whether complex formation stabilizes or destabilizes the spatial system is a complex function of other parameters. We give a detailed analysis of the spatial system by considering the pattern dynamics of waves. Furthermore, we investigate the effect of deleterious mutations. Surprisingly, high mutation rates can weaken the exploitation of the catalyst by the parasite.     

Roosting behaviour is related to reproductive strategy in brood parasitic cowbirds

Shiny Cowbirds Molothrus bonariensis and Screaming Cowbirds Molothrus rufoaxillaris are closely related brood parasites but the former is socially polygynous or promiscuous and an extreme host generalist, whereas the latter is socially monogamous and parasitizes almost exclusively one host. Females of both species lay in relative darkness, before dawn, relying for host nest location on previous days’ prospecting activity, or possibly on following better‐informed roost associates. We studied the temporal and spatial patterns of roosting behaviour in these species to test the hypothesis that roosting behaviour of cowbirds is related to their breeding strategy (brood parasitism) and reflects differences in strategies between species. We recorded fidelity to a roost, location fidelity within a roost, inter‐individual spatial associations and timing of roost departures and parasitic events, using tagged individuals. Female Shiny Cowbirds and both sexes of Screaming Cowbirds showed marked fidelity in roosting location, and roost departures occurred both during and after the known time window for parasitism, with earlier departures probably corresponding to laying days. Screaming Cowbird females and males that were trapped together and showed high levels of association during the day, also showed high levels of association in the roost. We describe the spatial and temporal patterns of a relatively poorly known aspect of avian ecology in general and the behaviour of brood parasites in particular.     

Birds are islands for parasites

Understanding the mechanisms driving the extraordinary diversification of parasites is a major challenge in evolutionary biology. Co-speciation, one proposed mechanism that could contribute to this diversity is hypothesized to result from allopatric co-divergence of host–parasite populations. We found that island populations of the Galápagos hawk (Buteo galapagoensis) and a parasitic feather louse species (Degeeriella regalis) exhibit patterns of co-divergence across variable temporal and spatial scales. Hawks and lice showed nearly identical population genetic structure across the Galápagos Islands. Hawk population genetic structure is explained by isolation by distance among islands. Louse population structure is best explained by hawk population structure, rather than isolation by distance per se, suggesting that lice tightly track the recent population histories of their hosts. Among hawk individuals, louse populations were also highly structured, suggesting that hosts serve as islands for parasites from an evolutionary perspective. Altogether, we found that host and parasite populations may have responded in the same manner to geographical isolation across spatial scales. Allopatric co-divergence is likely one important mechanism driving the diversification of parasites.     

Describing the current status of Plasmodium falciparum population structure and drug resistance within mainland Tanzania using molecular inversion probes

High‐throughput Plasmodium genomic data is increasingly useful in assessing prevalence of clinically important mutations and malaria transmission patterns. Understanding parasite diversity is important for identification of specific human or parasite populations that can be targeted by control programmes, and to monitor the spread of mutations associated with drug resistance. An up‐to‐date understanding of regional parasite population dynamics is also critical to monitor the impact of control efforts. However, this data is largely absent from high‐burden nations in Africa, and to date, no such analysis has been conducted for malaria parasites in Tanzania countrywide. To this end, over 1,000 P. falciparum clinical isolates were collected in 2017 from 13 sites in seven administrative regions across Tanzania, and parasites were genotyped at 1,800 variable positions genome‐wide using molecular inversion probes. Population structure was detectable among Tanzanian P. falciparum parasites, approximately separating parasites from the northern and southern districts and identifying genetically admixed populations in the north. Isolates from nearby districts were more likely to be genetically related compared to parasites sampled from more distant districts. Known drug resistance mutations were seen at increased frequency in northern districts (including two infections carrying pfk13‐R561H), and additional variants with undetermined significance for antimalarial resistance also varied by geography. Malaria Indicator Survey (2017) data corresponded with genetic findings, including average region‐level complexity‐of‐infection and malaria prevalence estimates. The parasite populations identified here provide important information on extant spatial patterns of genetic diversity of Tanzanian parasites, to which future surveys of genetic relatedness can be compared.     

On the relevance of abundance and spatial pattern for interpretations of host-parasite association data

The quantification of host-parasite associations from field data is a fundamental step towards understanding host-parasite and host-parasite-pathogen dynamics. For parasites that are not rigid host specialists, exemplified in this paper by ticks, the interpretation of host-parasite association data is difficult. Interpretations of tick collection records have largely assumed that off-host collection records offer a valid basis from which to make claims about the host specificity or generality of tick species. A simple simulation analysis of rudimentary tick-host interactions in a hypothetical 50 x 50-cell habitat demonstrates that perceptions of tick-host relationships can be strongly biased by spatial patterns. Regardless of their true level of host specificity or generality, it seems that: (i) more abundant ticks will be perceived as generalists, while rarer species will be considered specialists; and (ii) tick species that have patchy, strongly aggregated distributions will be more likely to be perceived as host specialists than species that have more dispersed or uniform distributions. Since all available evidence suggests that abundances and spatial patterns vary between tick species, there is no way of assessing the true validity of claims about host specificity without first undertaking detailed research on the relative abundances and spatial and temporal patterns of both tick and host distributions.     

Parasites as indicators of movement and population connectivity of a non-diadromous, tropical estuarine teleost: king threadfin Polydactylus macrochir

Temporal and spatial patterns in parasite assemblages were examined to evaluate the degree of movement and connectivity of post-recruitment life-history stages of a large, non-diadromous tropical estuarine teleost, king threadfin Polydactylus macrochir, collected from 18 locations across northern Australia. Ten parasites types (juvenile stages of two nematodes and seven cestodes, and adults of an acanthocephalan) were deemed to be suitable for use as biological tags, in that they were considered to have a long residence time in the fish, were relatively easy to find and were morphologically very different to each other which aided discrimination. Univariate and discriminant function analysis of these parasites revealed little difference in temporal replicates collected from five locations, suggesting that the parasite communities were stable over the timeframes explored. Univariate, discriminant function, and Bray-Curtis similarity analyses indicated significant spatial heterogeneity, with Bray-Curtis classification accuracies ranging from 55 to 100% for locations in north-western and northern Australia, 24 to 88% in the Gulf of Carpentaria, and 39 to 88% on the east coast of Queensland. Few differences were observed among locations separated by <200 km. The observed patterns of parasite infection are in agreement with concurrent studies of movement and connectivity of P. macrochir in that they indicate a complex population structure across northern Australia. These results should be considered when reviewing the management arrangements for this species.     

Parasitism ofAphis gossypii (Homoptera: Aphididae) byAllothrombium pulvinum larvae (Acari: Trombidiidae) in cotton fields: spatial dispersion and density dependence

Spatial aspects of the interaction between the aphid host,Aphis gossypii, and its parasite,Allo-thrombium pulvinum larvae, on cotton plants were examined in seven fields in China. For both the host and the parasite, sample variance increased with the mean according to Taylor's power law, which explained a substantial proportion (84–97%) of the variation in the data. Although both the host and parasite showed aggregated distribution on cotton plants, the host aphids aggregated more strongly than the parasites. The host dispersion pattern was not significantly affected by the presence of parasites. Increasing the spatial scales of observation from individual plot to the entire field also had no significant effects on host and parasite dispersion patterns. Parasites aggregated in cotton plants with higher aphid densities in five out of the seventeen samples. Spatial patterns of parasitism were mostly host density-independent (71% of the samples) and sometimes inversely density-dependent (29% of the sample). The processes underlying these patterns were discussed.