Population biology of swift (Apus apus) ectoparasites in relation to host reproductive success

Abstract.

• 1 We censused ectoparasite populations of adult and nestling swifts over the course of the host's breeding season. Nearly all of the birds were infested with chewing lice and two-thirds of the nests were infested with louse flies. Feather mites were observed but not quantified.
• 2 Lice and louse flies both showed aggregated distributions among hosts. Louse eggs, hatched lice and adult louse flies had negative binomial distributions, whereas the aggregated distribution of louse fly pupae was not adequately described by negative binomial or Poisson models.
• 3 Transmission of lice from parents to offspring was documented. A comparison of the age structure of lice on parents and offspring indicated that most transmission was by nymphal lice.
• 4 Host reproductive success and survival appeared to be independent of the number of lice or louse flies. Neither parasite correlated with the number, body mass, or date of fledging of young birds, nor with the overwinter survival of adults. We caution, however, that experimental manipulations of parasite load are required for a definitive test of the impact of ectoparasites on evolutionary fitness components.

     

High blowfly parasitic loads affect breeding success in a Mediterranean population of blue tits

The detrimental effects of ectoparasites on the breeding success of birds have been especially well demonstrated in the case of ectoparasites that affect both chicks and their parents. Since blowfly larvae of the genus Protocalliphora attack only nestling birds, they represent a good model for testing the consequences of parasitism on nestlings. A Corsican population of blue tit suffers extremely high rates of infestation by blowflies, which are suspected to negatively affect young birds. Comparing experimentally deparasitized (treated) and naturally infested (control) broods, we showed that the attack by Protocalliphora causes anaemia and an important disturbance to the chicks. Therefore, we expected that these effects would have a negative impact on body condition and survival in the infested broods. Although we did not find any effect of treatment on fledging success, our predictions were confirmed by lower growth rate, body mass at fledging and tarsus length at fledging in the control compared with the treated group. This suggests that in this population, blowflies decrease the probability of recruitment of young blue tits. Received: 6 May 1997 / Accepted: 14 July 1997     

Horizontal and vertical ectoparasite transmission of three species of Malophaga, and individual variation in european bee-eaters (Merops apiaster)

Dispersal of avian ectoparasites can occur through either vertical transmission from adult birds to their offspring in the nest or through horizontal transmission between adult birds or through phoresy. In this study, we investigated the importance of the 2 main transmission modes in the colonial European bee-eater and examined whether individual differences in ectoparasite intensity exist in relation to age, sex, and morphological features of the birds. The intensity of 3 chewing lice species was investigated. Almost all adult bee-eaters (98.3%, n = 176) were infested with 1 of the 3 ectoparasite species, whereas only 10.8% (n = 167) of all chicks were infested. Meropoecus meropis was the most frequent ectoparasite species on adult bee-eaters (prevalence 94.3%), whereas Meromenopon meropis was the most common species on chicks (prevalence 9.6%). Our results suggest that chewing lice are mainly horizontally transmitted among adult bee-eaters and mainly among pair members, whereas vertical transmission between parents and nestlings is less frequent. These conclusions were supported by a relation in ectoparasite intensity of pair members and a parasite removal experiment. Ectoparasite intensity was in general low in nestlings and did not correlate with ectoparasite intensity of their parents. Host age, sex, weight, and other morphological features did not explain variation in chewing lice infestation.     

Behavioural responses to ectoparasites in pied flycatchers Ficedula hypoleuca: an experimental study

Nests of cavity‐nesting birds usually harbor some species of haematophagous ectoparasites that feed on the incubating adults and nestlings. Given the negative impact of ectoparasites on nestlings there will be selection on hosts to reduce parasite infestations through behavioural means. We have experimentally reduced the abundance of all ectoparasites in nests of pied flycatchers Ficedula hypoleuca to explore both whether there are changes in the frequency and duration of putative anti‐parasite behaviours by tending adults, as well as whether such anti‐parasite behaviours are able to compensate for the deleterious effects that parasites may have on nestlings. Heat treatment of nests substantially decreased the density of ectoparasites, and thereby positively affected nestling growth. The frequency and intensity of female grooming and nest sanitation behaviours during the incubation and nestling periods decreased as a consequence of the experimental reduction of ectoparasite infestation. Although nestlings begged more intensely in infested nests, the experiment had no significant effect on parental provisioning effort. Reduction of parasites resulted in larger nestlings shortly before fledging and increased fledging success. This study shows a clear effect of a complete natural nest ectoparasite fauna on parental behaviour at the nest and nestling growth in a cavity‐nesting bird. Although ectoparasites induce anti‐parasite behaviours in females, these behaviours are not able to fully remove parasite's deleterious effects on nestling growth and survival.     

Parasites as mediators of heterozygosity-fitness correlations in the Great Tit (Parus major)

Positive correlations between heterozygosity and fitness traits are frequently observed, and it has been hypothesized, but rarely tested experimentally, that parasites play a key role in mediating the heterozygosity-fitness association. We evaluated this hypothesis in a wild great tit (Parus major) population by testing the prediction that the heterozygosity-fitness association would appear in broods experimentally infested with a common ectoparasite, but not in parasite-free broods. We simultaneously assessed the effects of parental and offspring heterozygosity on nestling growth and found that body mass of nestlings close to independence, which is a strong predictor of post-fledging survival, increased significantly with nestling levels of heterozygosity in experimentally infested nests, but not in parasite-free nests. Heterozygosity level of the fathers also showed a significant positive correlation with offspring body mass under an experimental parasite load, whereas there was no correlation with the mothers' level of heterozygosity. Thus, our results indicate a key role for parasites as mediators of the heterozygosity-fitness correlations.     

Burrow Use and the Influence of Ectoparasites in Brants' Whistling Rat Parotomys brantsii

In Brants' whistling rat, Parotomys brantsii, single animals inhabit unusually complex burrow systems containing several nest chambers. We investigated burrow use and examined the effect of ectoparasites on choice of alternative nest chambers by radiotelemetrically monitoring the nocturnal sleeping locations of individual whistling rats, before and after treating them to remove ectoparasites. Prior to treatment, animals used several different nest chambers within a single burrow, moving from one chamber to another every 1.6 d on average, and most individuals also slept in more than one burrow. Anti‐parasite treatment reduced the rate at which animals switched from one nest chamber to another within a burrow. Screening of a separate sample of animals for ectoparasites revealed that they were infested with fleas, mainly Xenopsylla eridos. We suggest that by switching periodically from one nest chamber to another, whistling rats reduce the rate at which ectoparasites, especially fleas, accumulate.     

Intraseasonal variation in immune defence,body mass and hematocrit in adult house martins Delichon urbica

The intensity of parasite infections often increases during the reproductive season of the host as a result of parasite reproduction, increased parasite transmission and increased host susceptibility. We report within‐individual variation in immune parameters, hematocrit and body mass in adult house martins Delichon urbica rearing nestlings in nests experimentally infested with house martin bugs Oeciacus hirundinis and birds rearing nestlings in initially parasite‐free nests. From first to second broods body mass and hematocrit of breeding adult house martins decreased. In contrast leucocytes and immunoglobulins became more abundant. When their nests were infested with ectoparasites adults lost more weight compared with birds raising nestlings in nests treated with pyrethrin, whereas the decrease in hematocrit was more pronounced during infection with blood parasites. Neither experimental infestation with house martin bugs nor blood parasites had a significant effect on the amount of immune defences.     

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.     

Prenatal exposure to testosterone increases ectoparasite susceptibility in the common lizard (Lacerta vivipara)

High levels of testosterone can benefit individual fitness, for example by increasing growth rate or ornament size, which may result in increased reproductive success. However, testosterone induces costs, such as a suppressed immune system, thereby generating trade-offs between growth or mate acquisition, and immunity. In birds and reptiles, females allocate steroids to their eggs, which may be a mechanism whereby females can influence the phenotype of their offspring. To our knowledge, only the benefits of early androgen exposure have been experimentally investigated to date. However, to understand this phenomenon, the costs also need to be evaluated. We manipulated testosterone levels in eggs of the viviparous common lizard and monitored growth, endurance and post-parturient responses to ectoparasites of the offspring. Testosterone-treated individuals had significantly higher growth rates than controls, but suffered a significant decrease in growth rate when exposed to ticks, whereas the corresponding difference for controls was non-significant. There was no difference in observed parasite load or leucocyte count between manipulated and control offspring. Thus, our results suggest that high testosterone levels during embryonic development have detrimental effects on immune function resulting in reduced growth rate, and that this must be taken into consideration when evaluating the potential adaptive value of maternal androgen allocation to eggs.     

Maternal effects reduce oxidative stress in female nestlings under high parasite load

Mothers can adjust the phenotype of their offspring to the local environment through a modification of their egg investment and/or nestling provisioning. However, offspring health may be severely impaired if the conditions experienced by nestlings do not match with those anticipated by the mother. If maternal effects differentially affect the sexes or if one sex is more strongly affected by an environmental stressor, fitness benefits may also differ between male and female offspring. Here, we study maternal effects in male and female great tit Parus major nestlings by means of an ectoparasite treatment before egg‐laying combined with a partial cross‐foster experiment between broods of infested and uninfested nests. Nestlings that were raised in their own nest experienced the same conditions before and after cross‐fostering (either in parasite infested or uninfested nests), while cross‐fostered ones experienced different conditions (either changing from infested to uninfested or the other way around). We measured effects on nestling plasma levels of oxidative stress [reactive oxygen metabolites (ROMs) and total antioxidant capacity (OXY)], body condition (body size and mass) and post‐fledging survival. Daughters, but not sons, from matching conditions showed the lowest ROM and high OXY levels when exposed to parasites, while there was no effect of parasite exposure in any of both sexes in case of a mismatch. In contrast, body condition and post‐fledging survival were not (or only slightly) affected by any of the experimental treatments. Results of this study show that maternal effects can affect oxidative stress levels of nestlings in a sex‐specific way and that the outcome depends on the exposure to environmental stressors, such as parasites.     

Cooperation, conflict, and crèching behavior in goldeneye ducks

Crèching behavior, or brood amalgamation, results in offspring being reared by adults other than their genetic parents. Although a variety of hypotheses have been proposed to explain this behavior, most assume either that brood amalgamation is accidental (i.e., nonselected) or that adoption of young is selected for because of social benefits to the young and/or adopting parents. We propose, instead, that brood amalgamation is a function of two separate processes: brood desertion and brood adoption. To examine brood desertion, we develop a graphic model to predict when parents should abandon their young and we test this model experimentally for the Barrow's goldeneye (Bucephala islandica). As predicted, females deserted their offspring when the size of the brood was experimentally reduced. Brood adoption occurred when deserted ducklings joined other broods. However, the success of ducklings in doing so was strongly dependent on the availability of potential host broods and on the age of the recipient broods. Foreign ducklings were readily accepted into young broods (<10 d old) but invariably were rejected from old broods. We could detect no benefits or costs of brood adoption to the host females, contrary to the expectations of a social benefit hypothesis. Our experiments indicate that Crèching behavior is driven by selection on adults to abandon their brood when the benefits of continued investment are outweighed by the reduction in future reproduction and selection on deserted ducklings to join other broods to obtain parental care. Rather than a form of cooperative brood care, Crèching in goldeneyes is perhaps best considered as a form of reproductive parasitism, entailing parent-offspring conflict over brood desertion and intergenerational conflict over adoption of abandoned young.     

Low humidity reduces ectoparasite pressure: implications for host life history evolution

A parasite's potential effect, or "pressure", can influence the life history strategy of its host. In environments with high parasite pressure, hosts invest more in anti-parasite defense, which may limit their investment in other life history components, such as survival. This tradeoff is difficult to study in natural populations because pressure is hard to quantify. Pressure is not necessarily correlated with the abundance of the parasite. A host population can be under high pressure, yet have few parasites, because members of the population have invested heavily in defense. Therefore, the extent to which parasite pressure varies among host populations, and the cause of such variation, remain largely undocumented. In this paper we show that birds in arid regions have fewer ectoparasitic lice than birds in humid regions. We show experimentally that low humidity reduces the number of lice on birds, even when host defense is held constant. Comparisons of ambient humidity to humidity beneath the plumage demonstrate that plumage does not provide a buffer for lice against low humidity. Our results confirm that an abiotic factor can cause substantial variation in parasite pressure among host populations. We suggest that humidity may influence host life history evolution through its impact on ectoparasites.     

Costs of parasite resistance for female survival and parental care in a freshwater isopod

Parasite resistance is expected to be costly because activation and maintenance of immune system requires energy that will not be available for other fitness related functions. Here, we experimentally exposed gravid female isopods from two lake populations to trophically transmitted acanthocephalan parasite. Successful establishment of the parasite requires penetration to body cavity; therefore, it is likely to induce an immune response. Resistant females from a lake where the parasite occurs as well as from a lake without the parasite experienced higher mortality than susceptible or control females. Parasite exposure reduced the offspring size at birth in both susceptible, but especially, in resistant females, suggesting that resistant females had less resource to direct for parental care. Parasite exposure had no effect on brood dumping, time to release of offspring or offspring growth rate after birth. Hence, our results reveal costs of resistance in parental survival and parental care of offspring.     

Host density and ectoparasite avoidance in the common lizard (Lacerta vivipara)

Increased transmission of parasites and diseases is generally considered as a major cost of social life. In this study we tested the hypothesis regarding ectoparasites as a cost of living in crowded habitats in the common lizard (Lacerta vivipara). We used two approaches to explore this question. First, we tested if ectoparasite load and prevalence are positively correlated with host density in the field. Second, we experimentally tested if lizards avoid parasitized conspecifics. Contrary to expectation, we found that (1) ectoparasite load is negatively correlated with lizard density; (2) prevalence does not significantly increase with density; (3) unparasitized lizards do not avoid parasitized conspecifics but are attracted by them whatever their parasite load. These findings suggest that ectoparasites cannot be considered as a cost of living at high density in the common lizard, in spite of the potential negative impact mites may have on lizard fitness. Received: 18 August 1996 / Accepted: 7 February 1997     

Palatability of passerines to parasites: within-brood variation in nestling responses to experimental parasite removal and carotenoid supplementation

Asynchronous hatching of eggs in avian clutches produces a size hierarchy among nestlings that may lead to variation within broods in resistance to pathogens or parasites. In this study, we tested several predictions regarding variation in immunocompetence and distribution of parasites within avian broods by combining parasite removal and carotenoid supplementation treatments in nests of mountain bluebirds Sialia currucoides . Last-hatched nestlings were less likely to invest carotenoids in an induced cell-mediated immune response, suggesting they may be more susceptible to parasites; however, parasite removal disproportionately benefited middle-ranked nestlings. This supports the hypothesis that some avian ectoparasites balance host resistance against nutritional benefits by preferentially parasitizing nestlings of intermediate quality and immunocompetence. We found no evidence that males positioned last in the hatching sequence were differentially affected by ectoparasites, and, contrary to some previous studies in other passerines, last-hatched nestlings in asynchronously hatching broods were not less immunocompetent than their nest mates. In fact, junior nestlings exhibited weaker immune responses than their siblings in more synchronously hatching broods, and we suggest this may reflect environment-dependent maternal effects that warrant further investigation. Overall, our results highlight the importance of understanding the feeding and host selection behaviour of ectoparasites, as well as the fitness consequences thereof, since many predictions related to within-brood distribution of parasites require that parasites are able to discern the relative quality of available hosts.     

Heterozygosity is linked to the costs of immunity in nestling great tits (Parus major)

There is growing evidence that heterozygosity–fitness correlations (HFCs) are more pronounced under harsh conditions. Empirical evidence suggests a mediating effect of parasite infestation on the occurrence of HFCs. Parasites have the potential to mediate HFCs not only by generally causing high stress levels but also by inducing resource allocation tradeoffs between the necessary investments in immunity and other costly functions. To investigate the relative importance of these two mechanisms, we manipulated growth conditions of great tit nestlings by brood size manipulation, which modifies nestling competition, and simultaneously infested broods with ectoparasites. We investigated under which treatment conditions HFCs arise and, second, whether heterozygosity is linked to tradeoff decisions between immunity and growth. We classified microsatellites as neutral or presumed functional and analyzed these effects separately. Neutral heterozygosity was positively related to the immune response to a novel antigen in parasite‐free nests, but not in infested nests. For nestlings with lower heterozygosity levels, the investments in immunity under parasite pressure came at the expenses of reduced feather growth, survival, and female body condition. Functional heterozygosity was negatively related to nestling immune response regardless of the growth conditions. These contrasting effects of functional and neutral markers might indicate different underlying mechanisms causing the HFCs. Our results confirm the importance of considering marker functionality in HFC studies and indicate that parasites mediate HFCs by influencing the costs of immune defense rather than by a general increase in environmental harshness levels.     

Factors affecting the survival of founding individuals in translocated New Zealand Saddlebacks Philesturnus carunculatus

Successful founders of new populations may represent a non-random sample of potential founding individuals. Using a recent Saddleback Philesturnus carunculatus translocation as a natural experiment, we related morphology, parasite load and genetic variation of translocated individuals to subsequent survivorship to assess the traits of successful founders. We also included capture location and holding time in our models to account for variables particular to translocations. Generalized linear model results suggest that, in addition to capture location, poor body condition (males) and the presence of ectoparasites (females) significantly reduced survivorship. Despite recent claims in the literature, we found no evidence that genetic variation was associated with survivorship or parasite load.     

Effects of maternal parasite load on offspring life-history traits in the common lizard (Lacerta vivipara)

We studied the effect of maternal ectoparasite load (measured at parturition) on the life-history traits of the offspring of the host Lacerta vivipara, the European common lizard. The ectoparasite, a mite belonging to the family Laelapidae, had a detrimental effect on its host: parasite load was associated with increased host mortality, and was negatively correlated with host body mass. Parasite load was persistent over time, suggesting that parasite load can be predictable. Offspring of highly parasitised mothers had higher values of several fitness components early in life than offspring of parasite-free mothers or lightly infested mothers. This was expressed in terms of increased F₁ yearling growth rate, and reproductive investment at first reproduction (measured as F₂ hatchling mass). These results are interpreted as a host adaptation to attenuate the impact of parasites. Indeed, if high parasite loads arise from long exposure time to a constant population of parasites, and if the negative effects of parasites are additive over time, hosts could reduce the impact of parasites simply by investing more during the earlier stages of life. Naturally, having better performance early in life should lead to higher mortality rates and/or lower fecundity later in life.     

Species divergence in offspring begging intensity: difference in need or manipulation of parents?

Conflicts over the delivery and sharing of food among family members are expected to lead to evolution of exaggerated offspring begging for food. Coevolution between offspring begging intensity and parent response depends on the genetic architecture of the traits involved. Given a genetic correlation between offspring begging intensity and parental response, there may be fast and arbitrary divergence in these behaviours between populations. However, there is limited knowledge about the genetic basis of offspring solicitation and parental response and whether these traits are genetically correlated. In this study, we performed a partial cross-fostering experiment of young between pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) and recorded the behaviour of individual offspring and their (foster)parents. We found that nestling collared flycatchers reached a higher phenotypic quality, estimated both as mass at fledging and as intensity of their T-lymphocyte-mediated immune response when raised by heterospecific foster parents. However, although collared flycatchers begged relatively more intensively, we found no evidence of corresponding higher resistance (i.e. lower feeding rate) of adult collared flycatchers than of adult pied flycatchers. Thus, the difference in offspring begging intensity between the two species seems not to be a result of a difference in escalation of the parent-offspring conflict. Instead, the species' divergence in exaggeration of offspring begging intensity 'honestly' matches a difference between the species in offspring need. This interpretation is strengthened by the fact that the difference in begging intensity between the two species increased as the season progressed, coinciding with the higher sensitivity of nestling collared flycatchers to the seasonal decline in food availability. Thus, the behavioural differentiation appears to be a direct consequence of a life-history differentiation (offspring growth patterns).     

Why do goose parents adopt unrelated goslings? A review of hypotheses and empirical evidence,and new research questions

Adoption of unrelated offspring by successful breeders is one form of brood mixing and alloparental care that is widespread among geese and other waterfowl. Biparental care and long-lasting family bonds in geese are likely to affect the costs and benefits of adoption. Most hypotheses that have been proposed to explain this behaviour assume that the separation of the gosling from its original family is accidental, and that adoption forms the 'best of a bad job' solution. For the gosling, adoption is therefore thought to be the only, and thus adaptive, option. For parents, some hypotheses assume that there are costs of adoption (intergeneration conflict), while others assume that there are benefits (mutually beneficial). The few studies of adoption in wild goose populations indicate cost-neutrality or that there are small benefits to parents of adopting young. This agrees with studies of brood size, which suggest that large families provide benefits for goslings and parents alike. By contrast, most observed adoption attempts involve parental aggression against the lone gosling. However, incidental observations are likely to be biased towards adoptions that involve conspicuous behaviour, such as aggression, and might overlook inconspicuous adoptions. Studies of individually marked goslings are needed to identify the background of the adoption goslings in order to identify whether in geese, as in some larids and altricial species, adoption might be an active strategy of offspring to improve their fitness prospects. In addition, more experimental studies are needed to test predictions about the costs and benefits of large families in geese.