The incidence of the tick parasite Ixodes uriae in Kittiwake Rissa tridactyla colonies in relation to the age of the colony, and a mechanism of infecting new colonies

Kittiwakes Rissa tridactyla (683 chicks and 64 adults) were examined for ectoparasites in three breeding areas: Isle of May (Firth of Forth, Scotland; eight colonies of approximately known age of occupation on natural sites), North Shields and Gateshead (Tyne and Wear, England; well established colonies of known age on buildings). All the 208 ticks collected were Ixodes uriae. On the Isle of May, a colony which had only been established for 7 years was already infested by ticks. Tick incidence increased significantly with the length of colonization of the area during the first 30 years. Age of colonization did not have an effect after 30 years. In Gateshead only a single adult among the 127 birds examined had a tick. No ticks were found on the 106 chicks born at North Shields checked in 1987 or in 1988. However, among nine visiting newly-fledged chicks from neighbouring colonies caught at the North Shields colony, six had either ticks or scars of previous infestation. Some visiting chicks remained for several days in the host colony and were even fed by the owners of visited nests. Ixodes uriae may thus spread from one colony to another during visits of newly-fledged infested chicks to neighbouring colonies. The absence of any infestation in old colonies (38 years in North Shields and 17 years in Gateshead) on buildings that are regularly visited by newly fledged infested chicks, suggests that buildings may lack the rock refuges necessary for tick survival from one year to the next. In this respect Kittiwake colonies on buildings are rather atypical.     

Increased mortality of black-browed albatross chicks at a colony heavily-infested with the tick Ixodes uriae

At Bird Island, South Georgia, we studied the effects of the tick Ixodes uriae on survival of chicks at two colonies of the black-browed albatross Diomedea melanophrys, one where most chicks were infested with ticks, the other where most chicks were tick-free. When the two colonies were compared, it was found that the colony heavily-infested with ticks had significantly greater chick mortality than the colony lightly-infested with ticks. However, within each of the two colonies, there was no significant difference in survival between chicks with ticks and those without ticks.     

Spatial genetic structure of the ectoparasite Ixodes uriae within breeding cliffs of its colonial seabird host

To examine the potential importance of the spatial subdivision of hosts for the functioning of parasite populations, we analysed patterns of local genetic structure within natural populations of the seabird ectoparasite, Ixodes uriae, at the scale of the host breeding cliff. The seabird hosts of this parasite nest in dense colonies with a hierarchical spatial organisation (individual nests-breeding cliffs-colony). Using eight microsatellite markers and samples from three breeding cliffs of the Black-legged kittiwake (Rissa tridactyla), we found that tick populations were indeed genetically structured at this spatial scale. However, the nature of this structuring depended on the characteristics of the cliffs considered. Both the host nest and cliff topography seemed to be important factors in the isolation of tick groups, but their relative roles may depend on the size of the local parasite population. We found no evidence of isolation by distance within a cliff suggesting that independent tick dispersal may not be a significant force influencing population structure in highly infested cliffs. However, genetic structure seemed to decrease with tick life stage, nymphal ticks being more strongly structured than adult ticks. These results may be related to the clustering of tick progeny combined with differential mortality and dispersal probabilities of each life stage. Overall, results indicate that the spatial organisation of hosts can indeed have important consequences for the population genetic structure of their parasites and, thus, may modify parasite dynamics and the scale at which local coevolutionary processes occur.     

Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races

Abstract Despite the fact that parasite dispersal is likely to be one of the most important processes influencing the dynamics and coevolution of host-parasite interactions, little information is available on the factors that affect it. In most cases, opportunities for parasite dispersal should be closely linked to host biology. Here we use microsatellite genetic markers to compare the population structure and dispersal of two host races of the seabird tick Ixodes uriae at the scale of the North Atlantic. Interestingly, tick populations showed high within-population genetic variation and relatively low population differentiation. However, gene flow at different spatial scales seemed to depend on the host species exploited. The black-legged kittiwake ( Rissa tridactyla ) had structured tick populations showing patterns of isolation by distance, whereas tick populations of the Atlantic puffin ( Fratercula arctica ) were only weakly structured at the largest scale considered. Host-dependent rates of tick dispersal between colonies will alter infestation probabilities and local dynamics and may thus modify the adaptation potential of ticks to local hosts. Moreover, as I. uriae is a vector of the Lyme disease agent Borrelia burgdorferi sensu lato in both hemispheres, the large-scale movements of birds and the subsequent dispersal of ticks will have important consequences for the dynamics and coevolutionary interactions of this microparasite with its different vertebrate and invertebrate hosts.     

Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla

Although much insight is to be gained through the comparison of the population genetic structures of parasites and hosts, there are, at present, few studies that take advantage of the information on vertebrate life histories available through the consideration of their parasites. Here, we examined the genetic structure of a colonial seabird, the black-legged kittiwake (Rissa tridactyla) using seven polymorphic microsatellite markers to make inferences about population functioning and intercolony dispersal. We sampled kittiwakes from 22 colonies across the species' range and, at the same time, collected individuals of one of its common ectoparasites, the tick Ixodes uriae. Parasites were genotyped at eight microsatellite markers and the population genetic structure of host and parasite were compared. Kittiwake populations are only genetically structured at large spatial scales and show weak patterns of isolation by distance. This may be due to long-distance dispersal events that erase local patterns of population subdivision. However, important additional information is gained by comparing results with those of the parasite. In particular, tick populations are strongly structured at regional scales and show a stepping-stone pattern of gene flow. Due to the parasite's life history, its population structure is directly linked to the frequency and spatial extent of within-breeding season movements of kittiwakes. The comparison of host and parasite gene flow therefore helps us to disentangle the intercolony movements of birds from that of true dispersal events (movement followed by reproduction). In addition, such data can provide essential elements for predicting the outcome of local co-evolutionary interactions.     

Dispersal and distribution of the tick Ixodes uriae within and among seabird host populations: the need for a population genetic approach

The aim of this study was to characterize the spatial distribution of the tick Ixodes uriae within and among populations of its seabird hosts and to consider the potential insight that could be gained by a population genetic approach to the issue of dispersal of this tick. Analyses of data collected around the Avalon Peninsula, Newfoundland, indicated that both the prevalence and mean abundance of ticks varied significantly among sample locations. Whereas ticks were found on all 4 host species examined (Rissa tridactyla, Uria aalge, Alca torda, Fratercula arctica), infestation prevalence and mean abundance differed among the species. On R. tridactyla, ticks were significantly aggregated at the among-nest scale and nestling infestation was spatially autocorrelated. Conversely, ticks were not aggregated among chicks within nests. These results enabled us to make a priori predictions regarding tick dispersal and host specificity and suggest there may be spatial structure of Ixodes uriae populations at both macro- and microgeographic scales. Investigating the population genetic structure of ticks within and among populations of hosts with different breeding biologies should provide direct insight into the metapopulation dynamics of such a spatially structured system.     

Reproductive strategies of the seabird tick Ixodes uriae (Acari: Ixodidae)

Ixodes uriae is a common ectoparasite of colonial seabirds in the circumpolar areas of both hemispheres. Despite its potential effects on host population dynamics and its role as a vector of pathogens, little is known about the reproductive strategies of this tick under natural conditions. Multiple mating of engorged females has been recorded in several instances, but the resulting paternity of offspring and its potential evolutionary significance have never been evaluated. Here, the paternity of offspring produced by females collected in the field was determined by using 5 polymorphic microsatellite markers. The results indicate that multiple mating in I. uriae can lead to multiple paternity in broods and, given the life history of this parasite, may be related to the adaptive benefits of producing genetically diverse offspring. Copulations took place both before and after the female's blood meal, but most successful fertilizations seemed to occur before engorgement. This suggests that the mating strategies of this tick may have evolved in response to local environmental constraints and, in particular, to the availability of conspecific ticks.     

Activity periods and questing behavior of the seabird tick Ixodes uriae (Acari: Ixodidae) on Gull Island, Newfoundland: the role of puffin chicks

Questing behavior of Ixodes uriae and their associated seasonal, host-feeding patterns are crucial to our understanding of tick life history strategies and the ecology of diseases that they transmit. Consequently, we quantified questing behavior of nymphs and adult female I. uriae ticks at Gull Island, a seabird colony in Newfoundland, Canada, to examine seasonal variation of off-host and on-host tick activity. We sampled a total of 133 adult Atlantic puffins (Fratercula arctica), 152 puffin chicks, and 145 herring gull (Larus argentatus) chicks for ticks during the breeding seasons of 2004 and 2005. Questing ticks were sampled by dragging a white flannel cloth across the grassy breeding areas during the mo of May, June, July, and August. Nymph questing activity reached a peak during mid-July (79 and 110 individuals/hr in 2004 and 2005, respectively). The prevalence of nymphs and adult female ticks on different seabird hosts varied between years and during the seasons. Puffin chicks had the highest prevalence (above 70% in July) of nymphs in both years and this was correlated with questing activity. Female ticks rarely fed on puffin chicks, but were prevalent on adult puffins and gulls, although prevalence and questing of ticks were not correlated in these hosts. These patterns of off-host and on-host tick activity suggests that I. uriae ticks likely use a combination of questing and passive waiting, e.g., in puffin burrows, to detect hosts, depending on the tick stage and the host species.     

Life cycle of the tick Ixodes uriae in penguin colonies: relationships with host breeding activity.

A survey of the temporal pattern of population structure and feeding activity of the seabird tick Ixodes uriae was conducted for the first time in two host species colonies: King penguin (Aptenodytes patagonicus halli) and Macaroni penguin (Eudyptes chrysolophus chrysolophus). The life cycle of the tick was investigated over 3 years in a King penguin colony and 2 years in a Macaroni penguin colony at Possession Island (Crozet Archipelago). There was a marked seasonal feeding activity pattern of ticks in both host species, connected with the presence of birds during the breeding season. Although the King penguin colonies were occupied throughout the year by birds, the favourable period for engorgement was limited to 3.5-4.5 months, and almost all the ticks overwintered in the unengorged state. Consequently, I. uriae probably completed its life cycle over 3 years in King penguin colonies. In contrast, this life cycle could be shortened to 2 years in Macaroni penguin colonies, as a result of a different timetable of the presence of birds for breeding and moulting. The relationships between such plasticity and the host behaviour and subantarctic climatic conditions are discussed.     

Pasteurella multocida infections in rockhopper penguins (Eudyptes chrysocome) from Campbell Island, New Zealand

During an investigation into the population decline of rockhopper penguins (Eudyptes chrysocome) on Campbell Island, New Zealand, avian cholera (Pasteurella multocida) was found in dead adults and chicks. An RNA enveloped virus was isolated from Ixodes uriae, a tick which commonly parasitizes rockhopper penguins on the island. It is not known whether this virus is virulent for penguins. No evidence was obtained to suggest that avian cholera was the principal cause for the decline in the rockhopper penguin population.     

Inter‐oceanic variation in patterns of host‐associated divergence in a seabird ectoparasite

Aim Parasites with global distributions and wide host spectra provide excellent models for exploring the factors that drive parasite diversification. Here, we tested the relative force of host and geography in shaping population structure of a widely distributed and common ectoparasite of colonial seabirds, the tick Ixodes uriae. Location Two natural geographic replicates of the system: numerous seabird colonies of the North Pacific and North Atlantic Ocean basins. Methods Using eight microsatellite markers and tick samples from a suite of multi‐specific seabird colonies, we examined tick population structure in the North Pacific and compare patterns of diversity and structure to those in the Atlantic basin. Analyses included population genetic estimations of diversity and population differentiation, exploratory multivariate analyses, and Bayesian clustering approaches. These different analyses explicitly took into account both the geographic distance among colonies and host use by the tick. Results Overall, little geographic structure was observed among Pacific tick populations. However, host‐related genetic differentiation was evident, but was variable among host types and lower than in the North Atlantic. Main conclusions Tick population structure is concordant with the genetic structure observed in seabird host species within each ocean basin, where seabird populations tend to be less structured in the North Pacific than in the North Atlantic. Reduced tick genetic structure in the North Pacific suggests that host movement among colonies, and thus tick dispersal, is higher in this region. In addition to information on parasite diversity and gene flow, our findings raise interesting questions about the subtle ways that host behaviour, distribution and phylogeographic history shape the genetics of associated parasites across geographic landscapes.     

Ticks Ixodes uriae and the breeding performance of a colonial seabird, king penguin Aptenodytes patagonicus

High densities of penguins in their colonies and the continuous use of these sites over consecutive reproductive periods increase the risk of development of tick populations. We have studied the effects of tick parasitism by Ixodes uriae in a colony of king penguins Aptenodytes patagonicus at Possession Island during three breeding seasons. We investigated the prevalence and periods of tick infestation during the one-year breeding cycle of penguins. The effects of tick parasitism on penguin breeding performance were assessed from photographs of the colony and with an automatic penguin identification system. We compared two groups of penguins carrying individual subcutaneous electronic tags, one group breeding in an infested area and the other in a non-infested area. Tick feeding activity was coincident with the periods when adult penguins stayed ashore for six days or more, i.e. during the incubating period. This duration corresponds to the duration of a tick meal on the host. The level of infestation varied between years. Penguins showed a lower incubating success in infested areas during a year of high infestation. In an infested area, individuals seen with ticks had a lower breeding success in rearing a one-year old chick than those seen without ticks.     

Recent evolution of host-associated divergence in the seabird tick Ixodes uriae

Ecological interactions are an important source of rapid evolutionary change and thus may generate a significant portion of novel biodiversity. Such changes may be particularly prevalent in parasites, where hosts can induce strong selection for adaptation. To understand the relative frequency at which host-associated divergences occur, it is essential to examine the evolutionary history of the divergence process, particularly when it is occurring over large geographical scales where both geographical and host-associated isolation may playa part. In this study, we use population genetics and phylogeography to study the evolutionary history of host-associated divergence in the seabird tick Ixodes uriae (Acari, Ixodidae). We compare results from microsatellite markers that reflect more ecological timescales with a conserved mitochondrial gene (COIII) that reflects more ancient divergence events. Population structure based on microsatellites showed clear evidence of host-associated divergence in all colonies examined. However, isolated populations of the same host type did not always group together in overall analyses and the genetic differentiation among sympatric host races was highly variable. In contrast, little host or geographical structure was found for the mitochondrial gene fragment. These results suggest that host race formation in I. uriae is a recent phenomenon, that it may have occurred several times and that local interactions are at different points in the divergence process. Rapid divergence in I. uriae implies a strong interaction with its local host species, an interaction that will alter the ecological dynamics of the system and modify the epidemiological landscape of circulating micropathogens.     

Recurrent evolution of host-specialized races in a globally distributed parasite

The outcome of coevolutionary interactions is predicted to vary across landscapes depending on local conditions and levels of gene flow, with some populations evolving more extreme specializations than others. Using a globally distributed parasite of colonial seabirds, the tick Ixodes uriae, we examined how host availability and geographic isolation influences this process. In particular, we sampled ticks from 30 populations of six different seabird host species, three in the Southern Hemisphere and three in the Northern Hemisphere. We show that parasite races have evolved independently on hosts of both hemispheres. Moreover, the degree of differentiation between tick races varied spatially within each region and suggests that the divergence of tick races is an ongoing process that has occurred multiple times across isolated areas. As I. uriae is vector to the bacterium responsible for Lyme disease Borrelia burgdorferi sensu lato, these results may have important consequence for the epidemiology of this disease. With the increased occurrence of novel interspecific interactions due to global change, these results also stress the importance of the combined effects of gene flow and selection for parasite diversification.     

Variable exposure and immunological response to Lyme disease Borrelia among North Atlantic seabird species

Colonial seabirds often breed in large aggregations. These individuals can be exposed to parasitism by the tick Ixodes uriae, but little is known about the circulation of pathogens carried by this ectoparasite, including Lyme disease Borrelia. Here we investigated the prevalence of antibodies (Ab) against Borrelia burgdorferi sensu lato in seabird species sampled at eight locations across the North Atlantic. Using enzyme-linked immunosorbent assay tests, we found that the prevalence of anti-Borrelia Ab in adult seabirds was 39.6% on average (over 444 individuals), but that it varied among colonies and species. Common guillemots showed higher seroprevalence (77.1%+/-5.9) than black-legged kittiwakes (18.6%+/-6.7) and Atlantic puffins (22.6%+/-6.3). Immunoblot-banding patterns of positive individuals, reflecting the variability of Borrelia antigens against which Ab were produced, also differed among locations and species, and did not tightly match the prevalence of Borrelia phylogroups previously identified in ticks collected from the same host individuals. These results represent the first report of the widespread prevalence of Ab against Borrelia within an assemblage of seabird species and demonstrate that Borrelia is an integrated aspect in the interaction between seabirds and ticks. More detailed studies on the dynamics of Borrelia within and among seabird species at different spatial scales will now be required to better understand the implications of this interaction for seabird ecology and the epidemiology of Lyme disease.     

Habitat requirements of the seabird tick, <Emphasis Type="Italic">Ixodes uriae</Emphasis> (Acari: Ixodidae), from the Antarctic Peninsula in relation to water balance characteristics of eggs,nonfed and engorged stages

The seabird tick Ixodes uriae is exposed to extreme environmental conditions during the off-host phase of its life cycle on the Antarctic Peninsula. To investigate how this tick resists desiccation, water requirements of each developmental stage were determined. Features of I. uriae water balance include a high percentage body water content, low dehydration tolerance limit, and a high water loss rate, which are characteristics that classify this tick as hydrophilic. Like other ticks, I. uriae relies on water vapor uptake as an unfed larva and enhanced water retention in the adult, while nymphs are intermediate and exploit both strategies. Stages that do not absorb water vapor, eggs, fed larvae and fed nymphs, rely on water conservation. Other noteworthy features include heat sensitivity that promotes water loss in eggs and unfed larvae, an inability to drink free water from droplets, and behavioral regulation of water loss by formation of clusters. We conclude that I. uriae is adapted for life in a moisture-rich environment, and this requirement is met by clustering in moist, hydrating, microhabitats under rocks and debris that contain moisture levels that are higher than the tick's critical equilibrium activity.     

Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla)

The capacity for mothers to transmit induced resistance against a specific parasite to their young may be an essential maternal effect that determines the fitness of offspring. In a previous study, antibodies against the Lyme disease agent Borrelia burgdorferi sensu lato were detected in kittiwake ( Rissa tridactyla ) eggs in relation to the exposure of birds to the tick vector Ixodes uriae . However, as yet, there has been no demonstration of a direct relationship between antibody concentrations in parents and young in a natural population. Here, we show, using the kittiwake– Borrelia system, the existence of a positive relationship between antibody concentrations in maternal serum and that in eggs and chick serum. No such relationship was found between paternal serum and eggs or young. These results suggest the existence of an adaptive maternal effect, an effect that should have important implications for the ecology and evolution of host–parasite interactions.     

Natural Attachment Duration of Adult Female Ticks Ixodes Uriae (Acari: Ixodidae) on Free-Living Adult Black-Legged Kittiwakes Rissa Tridactyla

An investigation into the attachment duration of the tick Ixodes uriae on free-living adult black-legged kittiwakes Rissa tridactyla was carried out at a colony in southeast Scotland. Adult kittiwakes (n = 14) were caught and searched for ticks. Newly attached ticks (n = 31) were marked as was the bird before its release. These birds were recaptured at intervals of two to seven days and the presence or absence of the tick was recorded. The median attachment duration was estimated as 7.7 days (SE = 0.38) and estimated times for 5% and 95% of ticks to become detached were 5.22 days (SE = 0.67) and 9.51 days (SE = 0.58) respectively. Information on tick attachment duration is essential for the development of accurate models of tick population dynamics and patterns of disease transmission.     

Offspring quality and tick infestation load in brood rearing great tits Parus major

Although the impact of nest-dwelling ectoparasites on nestlings in altricial birds is relatively well documented, little information is available on the fitness consequences of bird–ectoparasite systems with limited ectoparasite transmission between parents and their offspring. In this particular context we tested the hypothesis that parental infestation by a haematophageous field ectoparasite, the sheep tick Ixodes ricinus , in a hole-breeding passerine bird, the great tit Parus major , ultimately leads to the reduction of nestling quality. Observational data of a long-term study show that 15 days after hatching, nestlings' body condition (body mass corrected for body size) was negatively associated with the tick load of the mother, while no association was found with tick load of the father. A field experiment was conducted to test if adult infestation by ticks leads to a reduction in offspring quality. The field experiment consisted of a two by two factorial design: neither, one or both parents were infested with a high tick load (12 nymphs) when nestlings were eight days old. Four days after manipulation of the parents, the effect of the treatment on nestlings' health was assessed by measuring haematological and biochemical parameters. Body condition of nestlings was monitored from three days after hatching, until seven days after tick manipulation of the parents. Although parental tick manipulation resulted in successful tick feeding, nestlings' health parameters were not affected. We therefore suggest that the negative association between nestling condition and parental tick load does not reflect a causal effect of parasites, but either reflects a common environmental factor affecting parental infestation levels and offspring condition, or reflects parental quality. We propose different explanations why this association is expressed in female parents only.     

Phylogeographic relationships of Ixodes uriae (Acari: Ixodidae) and their significance to transequatorial dispersal of Borrelia garinii

The seabird tick Ixodes uriae (Acari: Ixodidae) has a bi- and circumpolar distribution and is commonly infected with Lyme disease Borrelia. Identical Borrelia flagellin gene sequences have been detected in I. uriae from both the Northern and Southern Hemispheres, suggesting a transequatorial transport of Borrelia. Parsimony analysis of the internal transcribed spacer 2 (ITS2) and a part of 16S rDNA of I. uriae from the Northern and Southern Hemispheres indicated that northern and southern I. uriae might be reproductively separated. We hypothesize that Borrelia is probably not dispersed from one hemisphere to the other by ticks attached to seabirds.