Relatedness and spatial proximity as determinants of host–parasite interactions in the brood parasitic Barrow's goldeneye (Bucephala islandica)

Recent studies, which have found evidence for kin-biased egg donation, have sparked interest in re-assessing the parasitic nature of conspecific brood parasitism (CBP). Since host–parasite kinship is essential for mutual benefits to arise from CBP, we explored the role of relatedness in determining the behaviour of conspecific nest parasites and their hosts in nesting female Barrow's goldeneyes ( Bucephala islandica ), a duck in which CBP is common. The results revealed that the amount of parasitism increased with host–parasite relatedness, the effect of which was independent of geographical proximity of host and parasite nests. Proximity per se was also positively associated with the amount of parasitism. Furthermore, while hosts appeared to reduce their clutch size as a response to the presence of parasitic eggs, the magnitude of host clutch reduction also tended to increase with increasing relatedness to the parasite. Hence, our results indicate that both relatedness and spatial proximity are important determinants of CBP, and that host clutch reduction may be an adaptation to nest parasitism, modulated by host–parasite relatedness. Taken together, the results provide a demonstration that relatedness influences host and parasite behaviour in Barrow's goldeneyes, resulting in kin-biased egg donation.     

Host-parasite relatedness in wood ducks: patterns of kinship and parasite success

We investigated the role of kinship in intraspecific nest parasitismof wood ducks (Aix sponsa). Among waterfowl, female philopatrycreates the potential for female relatives to nest in proximity.Costs of intraspecific nest parasitism to host females may bereduced if parasites lay eggs with kin. However, previous observationsof marked wood ducks indicated that females avoided parasitizingclutch mates or the female that incubated them. To further examinethe role of kinship, we determined the genotypes of 27 host-parasitepairs at five microsatellite loci. Average relatedness betweenhosts and all females laying parasitic eggs was only 0.04 ±0.03. Parasites appeared to choose hosts randomly with respectto kinship from among females with nests in the neighborhoodand those within the entire study area. However, host relatednessto the parasite with the greatest number of young leaving thenest was 0.11 ± 0.03, which was greater than expectedif eggs were accepted randomly from neighboring females or fromfemales present on the entire study area (p = .03 and p = .02,respectively). These patterns may reflect parasitism of randomlyselected nests followed by differential acceptance by hosts,differential hatching success of related parasites (e.g., dueto greater laying synchrony), or a mixture of parasitic strategies,one with a focus on related hosts and the other on unrelatedhosts. Genetic data revealed that social relationships did notalways reflect true relatedness and that success of primaryparasites was associated with kinship to hosts.     

Host-parasite kinship in a female-philopatric bird population: evidence from relatedness trend analysis

Conspecific brood parasitism (CBP), an alternative reproductive tactic where some females lay eggs in the nests of other females of the same species, occurs in many animals with egg care. It is particularly common in waterfowl, for reasons that are debated. Many waterfowl females nest near their birthplace, making it likely that some local females are relatives. We analyse brood parasitism in a Hudson Bay population of common eiders, testing predictions from two alternative hypotheses on the role of relatedness in CBP. Some models predict host-parasite relatedness, others predict that parasites avoid close relatives as hosts. To distinguish between the alternatives, we use a novel approach, where the relatedness of host-parasite pairs is tested against the spatial population trend in pairwise relatedness. We estimate parasitism, nest take-over and relatedness with protein fingerprinting and bandsharing analysis of egg albumen, nondestructively sampled from each new egg in the nest throughout the laying period. The results refute the hypothesis that parasites avoid laying eggs in the nests of related hosts, and corroborate the alternative of host-parasite relatedness. With an estimated r of 0.12-0.14, females laying eggs in the same nest are on average closer kin than nesting neighbour females. Absence of a population trend in female pairwise relatedness vs. distance implies that host-parasite relatedness is not only an effect of strong natal philopatry: some additional form of kin bias is also involved.     

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     

Conspecific nest parasitism is associated with inequality in nest predation risk in the common goldeneye (Bucephala clangula)

Previous studies of the role of nest predation in conspecificnest parasitism have not taken into account the possibilitythat predation risk may not be randomly distributed among nestsites and that breeding individuals may use different cues toassess the risk and adjust their reproductive tactic betweenyears accordingly. Especially in cavity-nesting species, therole of nest predation in conspecific nest parasitism has beendownplayed, while the role of nest site limitation has beenhighlighted. Using both observational and experimental data,I show that in the common goldeneye (Bucephala clangula), acavity-nesting species in which conspecific nest parasitism iscommon, predation risk varies considerably between nest sitesand does not follow a random expectation. The inequality inpredation risk between nest sites also showed up in the occurrenceof parasitized nests in an experimental setup. Nests parasitizedin year t were more frequent in those nest sites that were notdepredated during the previous nesting attempt in year t - nthan in nest sites that were depredated and in control nestsites that had not been used for nesting before. A nest siteaddition experiment revealed that conspecific nest parasitismwas not associated with nest site limitation. My findings givesupport for the hypothesis that nest predation is an importantecological factor explaining conspecific nest parasitism ingoldeneyes.     

Ectoparasites and age-dependent survival in a desert rodent

Host age is one of the key factors in host–parasite relationships as it possibly affects infestation levels, parasite-induced mortality of a host, and parasite distribution among host individuals. We tested two alternative hypotheses about infestation pattern and survival under parasitism in relation to host age. The first hypothesis assumes that parasites are recruited faster than they die and, thus, suggests that adult hosts will show higher infestation levels than juveniles because the former have more time to accumulate parasites. The second hypothesis assumes that parasites die faster than they are recruited and, thus, suggests that adults will show lower infestation levels because of acquired immune response and/or the mortality of heavily infested juveniles and, thus, selection for less infested adults. As the negative effects of parasites on host are often intensity-dependent, we expected that the age-related differences in infestation may be translated to lower or higher survival under parasitism of adults, in the cases of the first and the second hypotheses, respectively. We manipulated ectoparasite numbers using insecticide and assessed the infestation pattern in adult and juvenile gerbils (Gerbillus andersoni) in the Negev Desert. We found only a partial support for age-dependent parasitism. No age-related differences in infestation and distribution among host individuals were found after adjusting the ectoparasite numbers to the host’s surface area. However, age-related differences in survival under parasitism were revealed. The survival probability of parasitized juveniles decreased in about 48% compared to unparasitized hosts while the survival probability of adults was not affected by ectoparasites. Our results suggest that the effect of host age on host–parasite dynamics may not explicitly be determined by age-dependent differences in ectoparasite recruitment or mortality processes but may also be affected by other host-related and parasite-related traits.     

Population genetic structure of the tree-hole tick Ixodes arboricola (Acari: Ixodidae) at different spatial scales

The endophilic tick Ixodes arboricola infests cavity-nesting birds, and its dispersal strongly depends on the movements of its host. Population genetic structure of I. arboricola was studied with seven polymorphic microsatellite markers. We collected 268 ticks from 76 nest boxes in four woodlots near Antwerp, Belgium. These nest boxes are mainly used by the principal hosts of I. arboricola, the great tit Parus major and the blue tit Cyanistes caeruleus. As these birds typically return to the same cavity for roosting or breeding, ticks within nest boxes were expected to be highly related, and tick populations were expected to be spatially structured among woodlots and among nest boxes within woodlots. In line with the expectations, genetic population structure was found among woodlots and among nest boxes within woodlots. Surprisingly, there was considerable genetic variation among ticks within nest boxes. This could be explained by continuous gene flow from ticks from nearby tree holes, yet this remains to be tested. A pairwise relatedness analysis conducted for all pairs of ticks within nest boxes showed that relatedness among larvae was much higher than among later instars, which suggests that larvae are the most important instar for tick dispersal. Overall, tick populations at the studied spatial scale are not as differentiated as predicted, which may influence the scale at which host–parasite evolution occurs.     

Kin grouping is insufficient to explain the inclusive fitness gains of conspecific brood parasitism in the common eider

Conspecific brood parasitism allows females to exploit other females' nests and enhance their reproductive output. Here, we test a recent theoretical model of how host females gain inclusive fitness from brood parasitism. High levels of relatedness between host and parasitizer can be maintained either by: (a) kin recognizing and parasitizing each other as a form of cooperative breeding or (b) natal philopatry and nest site fidelity facilitating the formation of kin groups, thereby increasing the probability of parasitism between relatives nesting in close proximity. To address these two hypotheses we genotyped feathers and hatch membranes of common eiders (Somateria mollissima) from western Hudson Bay, Canada, using a noninvasive sampling methodology. We found that most instances of brood parasitism do result in inclusive fitness gains. Furthermore, females with failed nests moved an average of 492 m from their previous year's nest site, while successful females only moved an average of 13 m. Therefore, we observed host–parasite relatedness can occur at levels higher than would be expected by chance even in the absence of kin grouping, suggesting that closely related females nesting near one another is not essential to maintain high host–parasitizer relatedness. In addition, kin grouping is only a transient phenomenon that cannot occur every year due to the propensity for females of failed nests to nest farther away from their nest site in subsequent years than females with successful nests, which provides support for kin recognition as a more likely mechanism to maintain high host–parasitizer relatedness over time.     

The effect of landscape heterogeneity on host–parasite dynamics

Environmental heterogeneity has been shown to have a profound effect on population dynamics and biological invasions, yet the effect of its spatial structure on the dynamics of disease invasion in a spatial host–parasite system has received little attention. Here we explore the effect of environment heterogeneity using the pair approximation and the stochastic spatially explicit simulation in which the lost patches are clustered in a fragmented landscape. The intensity of fragmentation is defined by the amount and spatial autocorrelation of the lost habitat. More fragmented landscape (high amount of habitat loss, low clustering of lost patches) was shown to be detrimental to the parasitic disease invasion and transmission, which implies that the potential of using artificial disturbances as a disease-control agency in biological conservation and management. Two components of the spatial heterogeneity (the amount and spatial autocorrelation of the lost habitat) formed a trade-off in determining the host–parasite dynamics. An extremely high degree of habitat loss was, counter-intuitively, harmful to the host. These results enrich our understanding of eco-epidemiological, host–parasite systems, and suggest the possibility of using the spatial arrangement of habitat patches as a conservation tool for guarding focal species against parasitic infection and transmission.     

Perspective of practical biological control and population theories

We have not yet had sufficient theoretical explanation for successful biological control in which a key pest is controlled after an introduction of natural enemies. I compare here real features of successful biological control and theoretical host–parasitoid population models to reduce the gap between theory and practice. I first review the historical interaction between classical biological control projects and theoretical population models. Second, I consider the importance of host refuges in host–parasitoid population dynamics as concerns the mechanisms of low and stable host density. The importance of density–dependent parasitism through parasitoid reproduction in multivoltine host–parasitoid systems and supplemental generalist natural enemies are also discussed. Finally, I consider the difference in tactics for classical biological control and for augmentation of natural enemies in annual crop systems. Received: December 20, 1998 / Accepted: January 15, 1999     

Survival and anti-parasite defense in a host metapopulation under heavy brood parasitism: a source–sink dynamic model

The obligate brood parasite common cuckoo Cuculus canorus, widespread in Eurasia, occasionally reaches a high parasitism rate (over 20%), which usually exists only for a short period of time and in cases of new parasitism. Recent results from Hungary proved that a remarkably high parasitism rate (50–66%) can also be maintained constantly for several decades. In this paradoxical situation the reproductive success of the strongly exploited host population is lower than would be necessary for self-reproduction. We developed a model for a hypothetical host–brood parasite system that demonstrated that immigration of naive individuals from a highly reproductive (source) host population might explain the survival of the highly parasitized (sink) population. Our results also showed the possibility of maintaining the high parasitism rate and the imperfection of the hosts counter-adaptation against the brood parasite over a longer period. Gene flow was necessary to maintain both the acceptor genes and the non-mimetic cuckoo eggs in heavy parasitism. When the immigration rate was low (1–2%), an early expansion of the mimetic cuckoos was followed by a spread of anti-parasite defense, and consequently, the parasitism rate stabilized at a lower, but still relatively high level of about 45–60%.     

Persistent host–parasitoid interaction caused by host maturation variability

The heterogeneity of parasitism risk among host individuals is a key factor for stabilizing or sustaining host–parasitoid interactions. Host maturation variability, or the variation in the maturation times among host individuals, is the simplest source of such heterogeneity, but it has often been neglected in previous theoretical studies. We developed a configuration individual-based model (cIBM) of host–parasitoid interaction to investigate to what degree of host maturation variability promotes the persistence of host–parasitoid interactions. We ran simulations with various degrees of host maturation variability for different lengths of unsusceptible period. The result showed that low host maturation variability could sustain host–parasitoid dynamics when the host-unsusceptible period was short. Conversely, high levels of variability could sustain host–parasitoid dynamics when the host-unsusceptible period was about half of the total larval period. This suggests that the balance between variability and unsusceptible period is important for the persistence of host–parasitoid interaction. We conclude that maturation variability is a factor that can contribute to the sustainment of host–parasitoid interactions.     

The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis)

Host–parasite systems are characterised by coevolutionary arms races between host and parasite. Parasites are often the driving force, as they replicate much faster than their hosts and have shorter generation times and larger population sizes, resulting in higher mutation rates per time interval. This scenario does not fit all host–parasite systems. Socially parasitic cuckoo bumblebees (Bombus (Psithyrus) vestalis) parasitise colonies of Bombus terrestris share most life history characteristics with their hosts. As they parasitise only a subset of all available colonies, their population size should be lower than that of their hosts. This might have strong negative effects on the genetic diversity of B. vestalis and their adaptability. Here, we study for the first time the population structure of a Bombus/Bombus (Psithyrus) system. Highly polymorphic DNA markers were used to reconstruct sibships from individuals collected in the wild. The analysis of the host and parasite populations revealed a rate of parasitism of about 42% (range 33–50%). The population size of B. vestalis was lower compared to their hosts, which was also reflected in low within-group genetic distance. An analysis of the reconstructed queen genotypes revealed more supersisters amongst the B. vestalis queens when compared to the B. terrestris host. The data suggest that B. vestalis females and males do not disperse over long distances. This shows a potential for local adaptation to their hosts.     

Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts

Obligate avian brood parasitism typically involves one of 2strategies: parasite chicks are either 1) virulent and evictall other eggs and nest mates to be raised alone or 2) moretolerant and share foster parental care with host chicks forsome or the entirety of the nestling period. We studied theconsequences of experimentally forced mixed broods of age-matchedone common cuckoo (Cuculus canorus) and 2 great reed warbler(Acrocephalus arundinaceus) chicks. In these broods, both cuckooand host chicks grew slower than did either individual cuckoosor great reed warblers in broods of 1 parasite or 3 host chicks,respectively. Video records showed that in mixed broods, cuckoochicks received feedings less frequently than the 33% predictedby chance at 4 days of age but parental food allocations increasedto chance levels at 8 days of age. The consistent patterns oflower growth rates arose even though chicks in broods of 1 parasiteand 2 hosts received the largest prey items per feeding. Inaddition, several other measures of parental provisioning alsodid not predict species and brood-specific differences in nestlinggrowth rates across the different treatments. However, variationin begging displays and its specific costs on host and parasitechicks in the different nest treatments were not quantifiedin this study. We conclude that young of nest mate–evictorcommon cuckoos benefit from the sole occupancy of host nestsin part owing to an initial competitive disadvantage for parentalcare in broods with age-matched great reed warbler chicks.     

The role of breeding system on ant ecological dominance: genetic analysis of Ectatomma tuberculatum

Social insects exhibit a great variability in their social organization,and this affects colony kin structure, relatedness among nestmates, and population genetic structure. In the mosaic of arborealants of neotropical habitats, mutually exclusive dominant antspecies occupy different territories, and their nest distributionis spatially aggregated in patches influencing patterns of populationgenetic structure. In this study, we performed an analysis ofthe population and colony genetic structure of the facultativepolygynous ant Ectatomma tuberculatum to investigate how theparticular breeding and social system of this species can explainits ecological dominance in the mosaic. Within-nest geneticanalysis revealed that relatedness between nest mate workerswas significantly greater than zero (r = 0.30) with an effectivenumber of queens per nest of Ne = 2.5–3, indicating thatpolygyny is functional in this species. Moreover, we found thatqueen number was highly variable, probably due to queen adoptionevents, leading to the prevalence of polygyny over monogyny.Finally, the strong population genetic structure and the significantisolation by distance suggested that both budding and polydomytake place in this species. The respective role of secondarypolygyny, budding, and polydomy are then discussed in the contextof the mosaic of arboreal ants, and we propose that this particularsocial organization ensures the ecological dominance of E. tuberculatumby optimizing the colonization of new available nesting sitesand by increasing territory size.     

Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent

Parasites often confront conflicting demands when evaluating and distributing themselves among host individuals, in order to attain maximum reproductive success. We tested two alternative hypotheses about host preference by fleas in relation to the age of their rodent host. The first hypothesis suggests that fleas select adult over juvenile rodents because the latter represent a better nutritional resource (the “well-fed host” hypothesis), whereas the second hypothesis suggests that fleas prefer the weaker and less resistant juveniles because they are easier to colonise and exploit (“poorly fed host” hypothesis). We sampled fleas (Synosternus cleopatrae) on the gerbil (Gerbillus andersoni) in 23 different plots in the Negev desert and found an unequal distribution of fleas between adult and juvenile hosts. Furthermore, flea distribution changed as a function of flea density—from juvenile-biased flea parasitism (the “poorly fed host” hypothesis) at low densities to adult-biased flea parasitism (the “well-fed host” hypothesis) at high densities. Other factors that influenced flea preference were soil temperature and the presence of ticks. These results suggest that host selection is not an explicit alternative choice between adults and juveniles (“well-fed host” versus “poorly fed host” hypotheses), but rather a continuum where the distribution between adults and juveniles depends on host, parasite, and environmentally related factors.     

Differential responses to related hosts by nesting and non-nesting parasites in a brood-parasitic duck

Host-parasite relatedness may facilitate the evolution of conspecific brood parasitism, but empirical support for this contention remains inconclusive. One reason for this disparity may relate to the diversity of parasitic tactics, a key distinguishing feature being whether the parasite has a nest of her own. Previous work suggests that parasites without nests of their own may be of inferior phenotypic quality, but because of difficulties in identifying these parasitic individuals, little is known about their host selection criteria. We used high-resolution molecular maternity tests to assign parasitic offspring to known parasites with and without their own nests in a population of Barrow's goldeneyes (Bucephala islandica). We determined whether parasite nesting status, host-parasite relatedness and distance between host and parasite nests affected the probability of parasitizing a host and the number of eggs laid per host. We also investigated whether nesting parasites, conventionally nesting females and non-nesting parasites differed regarding their age, structural size, body condition, nesting phenology or total brood size. The probability of engaging in parasitism increased with host-parasite relatedness and spatial proximity to host nests for nesting and non-nesting females alike. However, nesting parasites increased the number of eggs donated with relatedness to the host, while non-nesting parasites did not do so. Non-nesting parasites laid fewer eggs in total, but did not differ by any of the other quality measures from conventional nesters or nesting parasites. Our study provides the first demonstration that nesting and non-nesting parasites from the same population may use different host selection criteria.     

Decoding dumping ducks

Conspecific brood parasitism, where females of the same species lay eggs in each other's nests, is common in waterfowl, and is usually considered costly to host females, which are stuck looking after eggs and chicks that are not their own. However, since female waterfowl often exhibit an unusual propensity to nest near where they were born, there has been some uncertainty over whether, in ducks and geese, laying in nests of conspecifics really is parasitism. Do parasitic and host females tend to be related? And is parasitism actually a form of cooperation in disguise? In a population in Hudson Bay, Andersson & Waldeck (this issue) found that ‘parasitic’ eggs in nests of the common eider, Somateria mollissima sedentaria, are more closely related to host eggs than expected by chance. In fact, host and ‘donor’ eggs are more closely related than are females breeding at neighbouring nests. The Hudson Bay population of common eiders is unusual, because unlike in more benign climates, females do not tend to breed near their natal nest. Spatial proximity alone cannot account for the high relatedness between host eggs and ‘dumped’ or donor eggs. Instead, the high relatedness values are probably the result of active recognition, where females favour kin, either when dumping or accepting eggs. These new data, along with evidence indicating that the donor lays the first egg in the nest nearly half the time, suggest that what appears to be parasitism in common eiders may be a form of kin‐based cooperation.     

Host selection by the Louse Fly Crataerina pallida, an avian nest ectoparasite of the Common Swift Apus apus

Preferences by parasites for particular hosts may have important implications for the functioning of host–parasite systems, however, this parasitic life-history trait remains little studied. No detrimental effect of Louse Fly Crataerina pallida parasitism has been found on Common Swift Apus apus nestling hosts. Host selection choices may be mediating the effect this parasite has and account for this apparent avirulence. Two aspects of parasite host selection were studied at a breeding colony of Common Swifts during 2008; (1) intra-brood differences in C. pallida parasitism were studied to determine the influence of nestling rank, (2) differences in male and female C. pallida parasitism were investigated, as they may result in varying costs of parasitism to hosts. C. pallida populations were found to preferentially parasitize higher rather than lower ranking nestlings within broods of both two and three chicks. Greater proportions of females were seen upon nestlings than at the nest, and upon higher ranking than lower ranking nestlings within broods. These results indicate that host selection occurs and this may thus account for the lack of parasitic virulence reported within this host–parasite system.     

Colony kin structure and host‐parasite relatedness in the barnacle goose

Conspecific brood parasitism (CBP), females laying eggs in the nest of other ‘host’ females of the same species, is a common alternative reproductive tactic among birds. For hosts there are likely costs of incubating and rearing foreign offspring, but costs may be low in species with precocial chicks such as waterfowl, among which CBP is common. Waterfowl show strong female natal philopatry, and spatial relatedness among females may influence the evolution of CBP. Here we investigate fine‐scale kin structure in a Baltic colony of barnacle geese, Branta leucopsis, estimating female spatial relatedness using protein fingerprints of egg albumen, and testing the performance of this estimator in known mother‐daughter pairs. Relatedness was significantly higher between neighbour females (nesting ≤ 40 metres from each other) than between females nesting farther apart, but there was no further distance trend in relatedness. This pattern may be explained by earlier observations of females nesting close to their mother or brood sisters, even when far from the birth nest. Hosts and parasites were on average not more closely related than neighbour females. In 25 of 35 sampled parasitized nests, parasitic eggs were laid after the host female finished laying, too late to develop and hatch. Timely parasites, laying eggs in the host’s laying sequence, had similar relatedness to hosts as that between neighbours. Females laying late parasitic eggs tended to be less related to the host, but not significantly so. Our results suggest that CBP in barnacle geese might represent different tactical life‐history responses.