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.     

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.     

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.     

Distribution and abundance of the tick Ixodes uriae in a diverse subantarctic seabird community

At Bird Island, South Georgia, we surveyed the distribution and abundance of ticks on the vertebrate fauna and found only 1 species Ixodes uriae. We classified all seabird species into 3 groups: (1) seabirds nesting on the surface of the ground solitarily, in dispersed groups of a few nests, or in colonies with well-spaced nests; (2) seabirds nesting on the surface of the ground in dense colonies; and (3) seabirds nesting in dense colonies in burrows or rock crevices. We detected I. uriae only on 3 species of the second group that nested in large, dense, persistent colonies, i.e., black-browed albatross (Diomedea melanophrys), gray-headed albatross (Diomedea chrysostoma), and macaroni penguin (Eudyptes chrysolophus). Ticks were found on the undersides of the feet on albatrosses but not on the undersides of the feet on penguins. We hypothesize that the coarse pebble nests of penguins, combined with the fact that their young walk around more than albatross young, make the environment on the underside of penguin feet more harsh and hostile for ticks than the underside of albatross feet. Despite the great abundance of Antarctic fur seals (Arctocephalus gazella) on the island, we found no ticks on them.     

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.     

Population trends in Kittiwake Rissa tridactyla colonies in relation to tick infestation

Parasite and disease transmission has long been considered one of the main costs of group living, but there is still little empirical evidence. Most seabird species breed in dense colonies and occupy the same breeding sites for many years and thus could be exposed to deleterious levels of haematophagous ectoparasite infestations. The aims of this study were to provide information on the epidemiology of the tick Ixodes uriae and to investigate the relationship between Kittiwake Rissa tridactyla colony population trends and local levels of tick infestation in chicks. It is based on a cross-sectional survey of a large sample of British Kittiwake colonies (22 colonies more than 30 years old and situated on natural cliffs). Ixodes uriae was by far the most common ectoparasite detected and was found in all colonies examined. Ticks were aggregated between nests, but not between siblings. Very young and old chicks were far less parasitized than chicks of intermediate age and were excluded from the analysis. Among colonies for which we had good data on population trends in Kittiwakes, those decreasing in number had a higher prevalence and density of ticks than those which were increasing. We suggest that this correlation reveals a cause-and-effect relationship. By influencing the local reproductive success, ectoparasites can affect the recruitment of new breeders and the breeders' site fidelity in the following year, thus influencing the local trend of numbers. This causal link highlights the potential effect of parasites on their host population and thus needs to be investigated further.     

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.     

The life cycle of the tick Amblyomma loculosum in a sooty tern Sterna fuscata colony in the Seychelles

An infestation of a sooty tern colony on Bird Island, Seychelles, with the ixodid tick Amblovomma loculosum was studied during visits to the colony in 1993 to 1995. During the infestation, adult ticks were numerous during the birds' incubation, larvae were abundant when young chicks were present, and there was some evidence that nymphs were found when older chicks were present. The life cycle of the tick appeared closely synchronized with that of its host. Following a breeding failure of the sooty terns, caused by adverse weather in August-September 1994, few adult ticks were found during the birds' breeding season of 1995, suggesting that the absence of chicks late in the 1994 breeding season led to starvation of the ticks and their failure to survive their diapause until the onset of the birds' next breeding season.     

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.     

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.     

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.     

Feeding territoriality and the reproductive consequences in brown skuas<Emphasis Type="Italic"> Catharacta antarctica lonnbergi</Emphasis>

In the maritime Antarctic, brown skuas (Catharacta antarctica lonnbergi) show two foraging strategies: some pairs occupy feeding territories in penguin colonies, while others can only feed in unoccupied areas of a penguin colony without defending a feeding territory. One-third of the studied breeding skua population in the South Shetlands occupied territories of varying size (48 to >3,000 penguin nests) and monopolised 93% of all penguin nests in sub-colonies. Skuas without feeding territories foraged in only 7% of penguin sub-colonies and in part of the main colony. Females owning feeding territories were larger in body size than females without feeding territories; no differences in size were found in males. Territory holders permanently controlled their resources but defence power diminished towards the end of the reproductive season. Territory ownership guaranteed sufficient food supply and led to a 5.5 days earlier egg-laying and chick-hatching. Short distances between nest and foraging site allowed territorial pairs a higher nest-attendance rate such that their chicks survived better (71%) than chicks from skua pairs without feeding territories (45%). Due to lower hatching success in territorial pairs, no difference in breeding success of pairs with and without feeding territories was found in 3 years. We conclude that skuas owning feeding territories in penguin colonies benefit from the predictable and stable food resource by an earlier termination of the annual breeding cycle and higher offspring survivorship.Research licence: Umweltbundesamt Bonn 13.4-94003-1/5-7.     

The seabird tick, <Emphasis Type="Italic">Ixodes</Emphasis><Emphasis Type="Italic">uriae</Emphasis>, uses uric acid in penguin guano as a kairomone and guanine in tick feces as an assembly pheromone on the Antarctic Peninsula

In the vicinity of Palmer Station, Antarctica, the seabird tick, Ixodes uriae, forms large aggregations under rocks at the periphery of Adelie penguin rookeries. When the adult penguins return to the rookeries at the beginning of the nesting season the ticks leave their off-host aggregation site, attach to the penguins for a period of feeding, and then subsequently return to the aggregation site. In this study, we searched for chemical cues that may be used by the ticks to locate their aggregation sites as well as cues involved in finding penguins. Tick excreta and soil extracts from beneath tick aggregations contained a pheromone that elicited assembly behavior in unfed larvae, non-fed nymphs and non-fed adults. Guanine, the major excretory product of ticks, elicited assembly behavior, thus, guanine is likely an active component involved in assembly. Non-fed stages also responded positively to penguin guano and uric acid, the primary excretory product of penguins, suggesting that uric acid and other components of penguin guano function as a kairomone used by the non-fed ticks to locate their host. After feeding, the immature ticks’ response to both the assembly and kairomones is switched off for several days, and the ticks regain responsiveness only after they have molted. Fed adult females lay eggs and die without ever regaining responsiveness. Thus, I. uriae relies on two closely related chemicals to regulate two critical aspects of its life: assembly and host-finding. Guanine and other components of tick excreta function as an assembly pheromone in promoting the formation of off-host aggregations, while uric acid and other components of penguin guano function as a kairomone used by the tick to locate its host.     

A comprehensive multiple matrix model representing the life cycle of the tick that transmits the agent of Lyme disease.

An extension of Leslie matrix methodology was developed to describe the life cycle of Ixodes dammini, the tick that transmits the agent of Lyme disease in eastern North America. Thereby, we described the seasonally changing pattern of interactions of the tick with its various hosts in a well-studied site on Nantucket Island, Massachusetts. Particular numerical values representing the site were estimated mainly on the basis of published values and interpreted on the basis of experience. The model was used to predict seasonal abundance and annual rate of increase of this vector tick. Although these ticks quest for hosts during two consecutive feeding seasons, all but a few feed during the first such season. The relative distribution of developmental stages of the tick stabilized after 35 years. Abundance of the simulated population increased exponentially and doubled every 6 years. The simulations produced realistic seasonal feeding distributions of the ticks in its various developmental stages.     

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.     

Colony sound facilitates sexual and agonistic activities in royal penguins

A unique playback system was used to exaggerate continuously the number of calls heard in royal penguin, Eudyptes schlegeli, colonies to determine whether social facilitation increases a female's exposure to both sexual and agonistic activities, a process that could influence the timing of reproduction in colonies. We also determined whether the source of colony sound or the phase of the breeding cycle influenced the facilitation of sexual or agonistic activities. The system recorded and then played a new 12-min colony sound sample every 24 min throughout the first four phases of the breeding cycle. Because each broadcast was unique, this playback system avoids the possibility of habituation and can modify the acoustic environment in social groups for extended periods of time. The activities of penguins in control colonies (with no playback) were compared with those in colonies that heard samples derived from either their own or a different colony. Colony sound facilitated both sexual and agonistic activities from male and female royal penguins during all four phases of the cycle that we examined. Playbacks from the perceiver's own colony facilitated a greater response than sound originating from a different colony. Studies comparing egg-laying dates in colonies exposed continuously to the sounds of agonistic activities with those in control colonies, or colonies exposed continuously to the sounds of sexual activities are now needed to determine whether the facilitation of agonistic activities opposes the effects of social stimulation on the hormonal changes leading to ovulation in colony-dwelling birds. Copyright 2000 The Association for the Study of Animal Behaviour.     

The impact of avian predator-scavengers on King Penguin Aptenodytes patagonicus chicks at Marion Island

While ashore King Penguins Aptenodytes patagonicus are fed upon by a guild of five predator-scavenger seabirds. During the winter (April-October) male Southern Giant Petrels Macronectes giganteus killed an estimated 6430 (11.2%) of Marion Island's King Penguin chicks, although most birds only scavenged in the colonies. The rate of predation varied, with peaks in April-May and in September. The proportion of successful attacks was 22.7%. There was a strong correlation between colony size and the rate of accumulation of chick corpses. Kelp Gulls Larus dominicanus and Lesser Sheathbills Chionis minor also scavenged penguin corpses but Northern Giant Petrels M. halli and female Southern Giant Petrels rarely entered the colonies. During the summer predation was mainly by Sub-Antarctic Skuas Catharacta lonnbergi which took eggs and small chicks.     

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.     

Experimental evaluation of birds as disseminators of the cosmopolitan tick Rhipicephalus sanguineus (Acari: Ixodidae)

Rhipicephalus sanguineus is believed to be the most widespread tick species of the world and its dissemination seems to rely on the diffusion of its main host, the dog. Empirical observations indicate that several bird species in urban areas regularly steal dog food. Such circumstances create a chance for R. sanguineus ticks to climb on birds and carry ticks to another site. In this work we evaluated experimentally the likelihood of birds (chicks) to either feed and/or carry R. sanguineus ticks from an infested site to another and to infest a host (rabbit) in the new location. Chicks were not suitable hosts for R. sanguineus ticks. Not a single adult tick engorged on chicks, yield as well as weight of engorged larvae and nymphs were very low and feeding period of these ticks was very long. However, a few larvae and, chiefly, nymphs were delivered to a new location either mechanically or after attachment and engorging total or partially on chicks. A few of these ticks fed successfully on rabbits. Further evidence on the capacity of birds to introduce R. sanguineus into non-infested dog settings should be provided by systematic examination of birds from urban areas, close to tick infested households.