Reproductive effort and blood parasites of breeding pied flycatchers: the need to control for interannual variation and initial health state

The association between reproductive effort, as assessed by experimentally altered clutch size, and prevalence of blood parasite infections was studied during two breeding seasons in the pied flycatcher ( Ficedula hypoleuca ). Only in the first study year (1998), enlarged clutches resulted in more fledged young and birds presumably responded to the intended experimental increase in reproductive effort by increasing their provisioning rates. Only on this study year, female body mass was negatively affected by the clutch size manipulation. For both sexes, no significant effect of experimental treatment on the prevalence of blood parasite infections ( Trypanosoma spp., Haemoproteus balmorali ) on day 13 after chick hatching was found in both study years. However, only in the first study year, when the intended increase in parental reproductive effort was achieved, we found a higher within female seasonal increase in Trypanosoma spp. prevalence for birds with enlarged clutches compared to those with control and reduced clutches. In this year, the Trypanosoma spp. prevalence was significantly higher than in the second study year. These results suggest that more than one year has to be covered, and that the knowledge of the premanipulative health status of parents can facilitate detection of the proposed trade-off between reproductive effort and immunocompetence.     

Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health

Blood parasites may act as modulators of their hosts' ecology, life histories and fitness. We studied the prevalence of Plasmodium sp., Haemoproteus sp. and Leucocytozoon sp. and their effects on morphological, biochemical and haematological variables and on breeding effort of Great Tits Parus major . Total prevalence (percentage of individuals infected by any parasite) ranged from 7.7% to 61.1%. There was an overall positive association in prevalence between the three haematozoan parasites. No effect of sex or age on infection status was observed. Negative impacts of infection on physiological condition depended largely on year and/or season and included effects on body condition index, plasma protein and haemoglobin index. There were also indications that parasite infection increased immune response and stress levels and activated antioxidant defence mechanisms. Males with higher fledging success had a higher probability of Haemoproteus infection, and females laying heavier eggs had a higher probability of Plasmodium infection. However, clutch size was negatively associated with the probability of infection by Leucocytozoon and Haemoproteus . Surprisingly, males raising second broods had a lower prevalence of both Haemoproteus and Leucocytozoon . Only 5.7% of first-brood nestlings were infected, but those in infected nestboxes had a lower heterophil/lymphocyte ratio. This study confirms the pathogenicity of blood parasites to the host by demonstrating negative effects of infection on both physiology and breeding performance.     

Mate Choice and Reproductive Success in the American Kestrel: a Role for Blood Parasites?

Blood parasites of breeding American kestrels, Falco sparverius (40 males and 27 females), were investigated to determine their connections to male showiness, mating success and host fitness. The only haematozoan found in the blood films was Haemoproteus tinnunculi (overall prevalence of 74% for females and 53% for males). In adult (+ 1-year-old) males, the subterminal tail band (character apparently used in female mate choice) was wider in infected males than in non-infected males. This was consistent with the Hamilton—Zuk hypothesis of parasite-mediated sexual selection. Our results also suggest that reproductive effort may increase susceptibility to parasitism. In yearling males, the proportion of individuals infected with H. tinnunuli was higher among those tending a large than a small brood at the time of fledging. Hunting effort (proportion of time spent in flight-hunting and wind-hovering) was also higher for males tending large broods than for those tending small broods, and it was higher for yearling than adult males on a given brood size. Reproductive effort may result in greater exposure and/or decreased ability to control chronic latent infections. Parasitic infections, in turn, may have detrimental effects on host fitness.     

Reproductive investment and parasite susceptibility in the Great Tit

1. Reproduction and parasite defence are assumed to be costly activities for hosts, and therefore trade-offs might exist between reproduction and parasite defence.
2. Brood sizes were manipulated in a population of Great Tits ( Parus major L.) to assess trade-offs between reproduction and parasite defence. Blood samples were taken from males and females during the late nestling phase, and parasite prevalence was compared among parents raising enlarged, reduced and control broods.
3. A higher prevalence of protozoan blood parasites dominated by Haemoproteus majoris was found among parents with enlarged broods, as compared with parents with control and reduced broods, respectively. Brood size manipulation did not affect parasite prevalence between the sexes or between age classes differently.
4. Mean parasite intensity (number of parasites per microscope field) among adult birds only infected with H. majoris was higher for parents with experimentally enlarged broods than controls and reduced broods, respectively.
5. These results support the hypothesis of a trade-off between parasite defence and reproduction.     

Survival costs of reproduction in the blue tit (Parus caeruleus): a role for blood parasites?

One of the central tenets in life-history theory is that there is a trade-off between current and future reproduction (i.e. a cost of reproduction). The mechanism for this cost of reproduction is, however, largely unknown. One hypothesis is that the high workload during reproduction compromises resistance to parasites and that the resulting increase in parasitaemia has negative effects on the prospects of future survival. Although empirical evidence for a negative relationship between reproductive effort and parasite resistance exists, the causal relationships between reproductive effort, parasite resistance and future reproduction are still unclear. We use a path analytical approach to investigate whether a change in parasite resistance (as measured by intensities of infections by the blood parasite Haemoproteus) after manipulation of reproductive effort, translates into altered survival in female blue tits. Our results show a negative relationship between reproductive effort and parasite resistance, although evident only in first-year breeders. Moreover, we found survival costs of reproduction in first-year breeders. These costs were, however, not mediated by the blood parasite studied.     

Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus).

The Hamilton and Zuk hypothesis on haemoparasite-mediated sexual selection and certain studies of reproductive costs are based on the assumption that avian blood parasite infections are detrimental to their hosts. However, there is no experimental evidence demonstrating harmful effects of blood parasites on fitness in wild populations, it even having been suggested that they may be non-pathogenic. Only an experimental manipulation of natural blood parasite loads may reveal their harmful effects. In this field experiment we reduced through medication the intensity of infection by Haemoproteus majoris and the prevalence of infection by Leucocytoazoon majoris in blue tits (Parus caeruleus), and demonstrated detrimental effects of natural levels of infection by these common parasite species on host reproductive success and condition. The fact that some of the costs of infection were paid by offspring indicates that blood parasites reduce parental working capacity while feeding nestlings. Medicated females may be able to devote more resources to parental care through being released from the drain imposed upon them by parasites and/or through a reduced allocation to an immune response. Therefore, this work adds support to previous findings relating hosts' life-history traits and haematozoan infections.     

Does daylength explain the latitudinal variation in clutch size of Pied Flycatchers Ficedula hypoleuca?

Geographical trends in breeding parameters were studied in the Pied Flycatcher Ficedula hypoleuca in the western Palaearctic. Predictions arising from the hypothesis that daylength and/or energy requirements of the brood explain latitudinal clutch size variation were tested. The nestling period decreased with latitude, but nestling mass on day 13 after hatching did not show a trend with latitude. The length of the daily activity period (working day) at the time of peak brood demand showed a quadratic relationship with latitude and did not increase linearly with daylight hours. The present study supports the hypothesis that latitudinal clutch size variation is influenced by the duration of the working day and the energy requirements of the brood. The balance between the energy requirements of the brood and the parents, in relation to the duration of working day and ambient temperature, are proposed to explain the latitudinal variation in clutch size in the Pied Flycatcher.     

Avian malaria is associated with increased reproductive investment in the blue tit

Haemosporidians causing avian malaria are very common parasites among bird species. Their negative effects have been repeatedly reported in terms of deterioration in survival prospects or reproductive success. However, a positive association between blood parasites and avian fitness has also been reported. Here, we studied a relationship between presence of malaria parasites and reproductive performance of the host, a hole‐breeding passerine – the blue tit Cyanistes caeruleus. Since the malaria parasites might affect their hosts differently depending on environmental conditions, we performed brood size manipulation experiment to differentiate parental reproductive effort and study the potential interaction between infection status and brood rearing conditions on reproductive performance. We found individuals infected with malaria parasites to breed later in the season in comparison with uninfected birds, but no differences were detected in clutch size. Interestingly, infected parents produced heavier and larger offspring with stronger reaction to phytohemagglutinin. More importantly, we found a significant interaction between infection status and brood size manipulation in offspring tarsus length and reaction to phytohemagglutinin: presence of parasites had stronger positive effect among birds caring for experimentally enlarged broods. Our results might be interpreted either in the light of the parasite‐mediated selection or terminal investment hypothesis.     

Presence of Plasmodium and Haemoproteus in breeding prothonotary warblers (Protonotaria citrea: Parulidae): temporal and spatial trends in infection prevalence

Prothonotary warbler (Protonotaria citrea) has shown a long-term decline in abundance in the United States. As a long-range migrant, these warblers are exposed to parasites in both tropical and temperate regions. The focus of this study was to use molecular techniques to examine the temporal prevalence patterns of heamosopridian parasites Plasmodium and Haemoproteus in breeding prothonotary warblers. The prevalence (presence or absence) of Plasmodium and Haemoproteus species was assayed using primer sets for the cytochrome b gene of the mitochondrial DNA. Blood samples were obtained from 187 adult prothonotary warblers collected at 3 central Virginia, U.S.A., breeding sites. The relationship between haemosporidian parasite infections and reproductive success also was examined. We found that 71% of captured prothonotary warblers were infected with haemosporidian parasites, specifically, with 36% prevalence for Haemoproteus spp. and 44% prevalence for Plasmodium spp., during the 2008 breeding season; for both parasites, prevalence increased throughout the season. We found significant variation in haemosporidian parasite prevalence across the breeding season that was strongly site specific. Conversely, we found no significant effects of haemosporidian parasite infections on the reproductive success of prothonotary warblers. This is in sharp contrast to recent reports suggesting considerable effects of these parasites on the reproductive success of wild birds.     

Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation,host adaptation,or side effect?

Parasitic infections may cause alterations in host life history, including changes in reproductive investment (absolute amount of energy allocated to reproduction) and reproductive effort (proportion of available energy allocated to reproduction). Such changes in host life history may reflect: 1) a parasite tactic: the parasite adaptively manipulates energy flow within the host so that the host is induced to make a reduction in reproductive effort and reproductive investment, making more energy available to the parasite; 2) no tactic: there is no change in host reproductive effort and reproductive investment simply decreases as a side effect of the parasite depleting host energy stores; 3) a host tactic: the host adaptively increases reproductive effort in the face of infection and loss of body condition, reproductive investment possibly being reduced despite the increased reproductive effort. Females in Alaskan lake populations of threespine sticklebacks ( Gasterosteus aculeatus ) are capable of clutch production when parasitized by the cestode Schistocephalus solidus despite large relative parasite masses. We analyzed the somatic energy reserves, maturation stage and ovarian mass of female sticklebacks collected from an Alaska lake during a single reproductive season. We found that parasitized females were less likely to carry fully-matured gametes, had smaller ovarian masses, and had lower somatic energy stores than unparasitized females. The relationship between reproductive investment and energy storage did not differ between parasitized and unparasitized females. Thus, reproductive effort did not change in response to parasitic infection. We conclude there was no indication of either a parasite tactic or a host tactic. Simple nutrient theft is involved in the parasite's influence on host reproduction, consistent with an earlier hypothesis that reproductive curtailment in threespine sticklebacks is a side effect.     

Haematozoan Parasites and Migratory Behaviour in Waterfowl

Although it has been suggested that migratory species are exposed to a more diverse parasite community than sedentary species, this has not previously been demonstrated. To test this hypothesis, we analysed the diversity and prevalence of infections by haematozoan parasites reported in anseriform species (ducks, geese and swans) in relation to host migration patterns. Whilst controlling for research effort, the number of parasite species or genera reported per host was positively related to migration distance, but not to breeding latitude or size of the breeding or total annual range. In species undergoing longer distance migrations, a higher proportion of individuals were infected by haematozoa. Thus, there is indeed evidence that migratory birds are more susceptible or are exposed to a more diverse parasite fauna and higher risk of infection. This may help to explain why migratory species tend to have more exaggerated, sexually selected traits as well as larger immune system organs. This revised version was published online in July 2006 with corrections to the Cover Date.     

No evidence for long‐term effects of reproductive effort on parasite prevalence in great tits Parus major

Allocation of resources between the life history traits reproduction and parasite defence are expected because both are energetically costly. Experimental evidence for such allocation has been found in short‐term effects of reproduction on parasite prevalence or immune function. However, there is increasing evidence for long‐term negative effects of reproductive effort on individuals. This study investigates whether long‐term effects of reproductive effort on parasite prevalence exist. Brood sizes of great tits Parus major were experimentally altered in one breeding season and in the subsequent breeding season the prevalence of three parasites types (blood parasites, ticks and fleas) on the surviving parents were investigated. We detected no long‐term effects of brood size manipulation on the prevalence of parasites in the next year and therefore provide no evidence for inter‐seasonal effects of reproductive effort on parasite prevalence. The post hoc level of statistical power was reasonable for effects on blood parasite and flea prevalence, but low for effects on tick prevalence.     

Haematological health state indices of reproducing Great Tits: a response to brood size manipulation

1. A brood size manipulation experiment was performed in two Great Tit ( Parus major L.) populations in order to evaluate the effect of raising different numbers of nestlings on parental health state.
2. Brood enlargement resulted in elevated heterophile:lymphocyte ratios and decreased lymphocyte number in the peripheral blood, indicating that increased reproductive effort causes immunosuppression.
3. Haematocrit increased in response to brood enlargement, suggesting a response to the requirement of elevated oxygen-carrying capacity of the blood during increased work load.
4. Parental body mass revealed a tendency to decrease in response to brood enlargement.
5. No effect of brood size manipulation on total leucocyte count, heterophile count, intensity of Haemoproteus blood parasite infection or plasma proteins could be detected.
6. Health state indices were more sensitive to brood size manipulation in the Great Tits breeding in a rural habitat than urban birds.     

Effects of blood parasites on sexual and natural selection in the pied flycather

The occurrence of the blood parasites Haemoproteus and Trypanosoma in the pied flycatcher, Ficedula hypoleuca , was examined to test current hypotheses that parasites reduce the expression of secondary sexual traits, mating success, breeding success, and survival of infected individuals. The results showed that there was no significant relationship between male plumage brightness and Trypanosoma infection, but males infected with Haemoproteus tended to be brighter than uninfected males, partly because first-year males were less often infected than older males. Polygynous males did not have fewer parasites than monogamous males. Females did not choose uninfected males among those they had sampled. Clutch size and laying date were not related to female infection status, and the number and quality of nestlings was not related to parasite infections of either male or female parent. The ability of males to provide parental care was not related to their infection status. The return rate from one breeding season to the next of infected males was not lower than that of uninfected males. The lack of correlations between parasites and male plumage colour and female mate choice apparently do not support the Hamilton-Zuk hypothesis of sexual selection. However, the absence of demonstration of any negative effects of parasites suggests that infection status may not be a direct measure of parasite resistance, or the degree to which the host suffers. Instead, the results support the alternative view that infected individuals have demonstrated their ability to survive and to cope with the parasites, while uninfected individuals are probably not yet tested for their resistance. This points to problems in using parasite prevalences and distributions, at least of some protozoan blood parasites, for tests of Hamilton-Zuk hypothesis, even though this was done in the first test by Hamilton and Zuk and by many later researchers     

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.     

Diversity and distribution of avian haematozoan parasites in the western Indian Ocean region: a molecular survey

The genetic diversity of haematozoan parasites in island avifauna has only recently begun to be explored, despite the potential insight that these data can provide into the history of association between hosts and parasites and the possible threat posed to island endemics. We used mitochondrial DNA sequencing to characterize the diversity of 2 genera of vector-mediated parasites (Plasmodium and Haemoproteus) in avian blood samples from the western Indian Ocean region and explored their relationship with parasites from continental Africa. We detected infections in 68 out of 150 (45·3%) individuals and cytochrome b sequences identified 9 genetically distinct lineages of Plasmodium spp. and 7 lineages of Haemoproteus spp. We found considerable heterogeneity in parasite lineage composition across islands, although limited sampling may, in part, be responsible for perceived differences. Two lineages of Plasmodium spp. and 2 lineages of Haemoproteus spp. were shared by hosts in the Indian Ocean and also on mainland Africa, suggesting that these lineages may have arrived relatively recently. Polyphyly of island parasites indicated that these parasites were unlikely to constitute an endemic radiation and instead probably represent multiple colonization events. This study represents the first molecular survey of vector-mediated parasites in the western Indian Ocean, and has uncovered a diversity of parasites. Full understanding of parasite community composition and possible threats to endemic avian hosts will require comprehensive surveys across the avifauna of this region.     

Does supplementary calcium reduce the cost of reproduction in the Pied Flycatcher Ficedula hypoleuca?

Studies in acidified as well as in naturally base-poor areas have recently revealed that availability of extra calcium-rich food items is an important component of habitat quality affecting breeding performance in several bird species. However, these mostly short-term studies have provided equivocal results concerning the exact consequences of calcium shortage on different species in different regions. We studied the effect of calcium availability on reproduction of the Pied Flycatcher Ficedula hypoleuca breeding in pine forests in Estonia, NE Europe, over a period of 4 years. Experimental pairs were provided with supplementary calcium-rich material when breeding, while control pairs were left unsupplemented. Experimental females laid larger eggs and their nestlings had longer tarsi than those of controls. Moreover, the mass and condition of females tending larger than average clutches were increased by calcium-supplementation. Our results provide the first experimental evidence that calcium availability may affect the overall cost of reproduction in free-living passerines. We compared these results with similar data for the Great Tit Parus major , collected from the same area during the same study period. Great Tits responded to low calcium availability mainly by restrained reproductive behaviour and reduced breeding success, while Pied Flycatchers invested significantly more in current reproductive effort despite the increased cost of reproduction. Thus, the effects of calcium deficiency on birds seem to be species-specific or population-specific. This partly explains discrepancies between the results of earlier studies.     

Age-dependent reproductive costs and the role of breeding skills in the Collared flycatcher

This study addressed whether there are any age‐related differences in reproductive costs. Of especial interest was whether young individuals increased their reproductive effort, and thereby their reproductive cost, as much as older birds when brood size was enlarged. To address these questions, a brood‐size manipulation experiment with reciprocal cross‐fostering of nestlings of young and middle‐aged female Collared flycatchers, Ficedula albicollis, was performed on the Swedish island of Gotland. Nestlings’ body mass, tarsus length and survival were recorded to estimate the parental ability and parental effort of the experimental female birds. Female survival and clutch size were recorded in the following years to estimate reproductive costs. We found that middle‐aged female flycatchers coped better with enlarged broods than younger females or invested more in reproduction. In the following year, young female birds that had raised enlarged broods laid smaller clutches than the females from all the other experimental groups. This result shows that the young female birds pay higher reproductive costs than the middle‐aged females. Both young and middle‐aged female flycatchers seemed to increase their reproductive effort when brood size was increased. However, such an increase resulted in higher reproductive costs for the young females. The difference in reproductive costs between birds of different ages is most likely a result of insufficient breeding skills of the young individuals.     

Density dependence of avian clutch size in resident and migrant species: is there a constraint on the predictability of competitor density?

The presence of density dependence of clutch size is tested in 57 long-term population studies of 10 passerine bird species. In about half of the studies of tit species Parus spp. density dependence of clutch size was found, while none was found in studies of two flycatcher species Ficedula spp. One hypothesis explaining this difference is that migrants are less able to predict the final competitor density, because new pairs are still settling when the first females start laying eggs. Such unpredictability is only a problem for early laying females. If this explanation is true, the commonly observed negative correlation between clutch size and laying date should be stronger in high-density years. I tested this prediction in three populations of Pied Flycatcher Ficedula hypoleuca , and compared the results with three populations of Great Tit Parus major . In none of the six populations was there a significant correlation between the strength of the seasonal decline in clutch size and population density. Thus the lack of density dependence of clutch size in Pied Flycatchers was not consistent with the idea that this is caused by the unpredictability of final density at the time of egg-laying of the earliest females in the population. Furthermore, density does not have any adverse effect on reproductive output of Pied Flycatchers, and therefore they do not adjust clutch size to density.     

Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands

The degree to which haematozoan parasites can exploit a range of vectors and hosts has both ecological and evolutionary implications for their transmission and biogeography. Here we explore the extent to which closely related mosquito species share the same or closely related haematozoan parasites, and examine the overlap in parasite lineages with those isolated from avian hosts, Zosterops species, sampled across the same study sites. Mosquito samples were collected and analysed (14 species, n = 804) from four islands in Vanuatu and the main island of New Caledonia. Using polymerase chain reaction, 15.5% (14/90) of pooled mosquito (thoracic) samples showed positive amplifications. Subsequent phylogenetic analysis of the cytochrome b gene identified four genetically distinct Plasmodium and two Haemoproteus lineages from these samples, five of which were identical to parasite lineages (n = 21) retrieved from the avian hosts. We found that three Plasmodium lineages differing by a maximum of 0.9% sequence divergence were recovered from different species and genera of mosquitoes and two Haemoproteus lineages differing by 4.6% sequence divergence were carried by 10 distantly related (11-21% divergent) mosquito species. These data suggest a lack of both cospeciation and invertebrate host conservatism. Without experimental demonstration of the transmission cycle, it is not possible to establish whether these mosquitoes are the biological vectors of isolated parasite lineages, reflecting a limitation of a purely polymerase chain reaction-based approach. Nonetheless, our results raise the possibility of a new transmission pathway and highlight extensive invertebrate host shifts in an insular mosquito-parasite system.