Physiological ecology of Mediterranean blue tits (Parus caeruleus L.): effects of ectoparasites (Protocalliphora spp.) and food abundance on metabolic capacity of nestlings

The consequences of nest ectoparasites, such as Protocalliphora larvae, on nestling birds have been the subject of numerous studies. Despite observed reductions in mass and hematocrit of chicks from parasitized nests, no studies have found any effect of Protocalliphora on nestling survival, suggesting that fitness consequences of Protocalliphora are either weak or occur after fledging. From experiments on the metabolic performance of chicks, we found that parasitized chicks suffer from reduced thermogenic and metabolic capacities as a result of decreased mass and hematocrit. Hence, Protocalliphora may potentially affect nestling survival after fledging, when energetically costly activities such as flight and moult are undertaken. Previous studies have demonstrated an increase in parental feeding rate to compensate for the detrimental consequences of parasite infestation. We tested whether parasite effects on nestling aerobic capacity were dependent on food availability during the feeding period. Measures of caterpillar densities and experimental manipulations of parasite loads allowed us to investigate relationships among host, parasite, and environment. A positive relationship between chick aerobic and thermogenic performances and caterpillar density suggests that negative effects of parasitism may be offset by increased food availability. This study provides the first measurement of the effects of an ectoparasite on metabolic competence in wild birds and documentation of the effect of food availability on ectoparasite virulence using a quantitative measure of food abundance.     

Nest‐dwelling ectoparasites reduce begging effort in Pied Flycatcher Ficedula hypoleuca nestlings

Parasitized nestlings might be expected to increase begging effort to obtain additional resources to compensate for those sequestered by their parasites. However, begging is costly and chicks harbouring parasites may find it more difficult to attain high begging levels. Consequently, we predicted that, for the same level of nutritional need, nestlings that are parasitized will invest less in begging than those that are not parasitized. We tested this prediction by measuring begging in Pied Flycatcher Ficedula hypoleuca nestlings parasitized with haematophagous mites Dermanyssus gallinoides and Dermanyssus gallinae and blowfly larvae Protocalliphora azurea, and subjected to different levels of food deprivation in order to control for short‐term nutritional need. Nestlings from nests with ectoparasites spent less time begging than those from nests without parasites, especially when very hungry, although there was no association with latency to beg or begging intensity. Our results suggest that time invested in begging may indicate not only the level of need, but also nestling parasitism status.     

Assessing the effects of haematophagous ectoparasites on the health of nestling birds: haematocrit vs haemoglobin levels in House Wrens parasitized by blow fly larvae

We compared haematocrits and blood haemoglobin concentrations of nestling House Wrens Troglodytes aedon in nests with relatively large numbers of haematophagous larvae of the blow fly Protocalliphora parorum (>6.4 large larvae/nestling) and nests in which exposure to larvae was severely reduced or eliminated (0–2.0 larvae/nestling). Heavily parasitized nestlings showed no reduction in haematocrit levels but a significant 28% reduction in haemoglobin levels. Previous research on avian response to chronic blood loss suggests that parasitized nestlings may show normal volumes of red blood cells as a result of a rapid production of new cells in response to blood loss and, additionally, as a result of swelling of individual cells left in the bloodstream after parasite feeding. Rapid erythropoiesis places high numbers of haemoglobin-poor, immature cells into the bloodstream which would explain the reduced haemoglobin levels of parasitized nestlings. Our results refute the conclusion that larval feeding has "little direct effect" on nestling wrens in this parasite–host system, drawn earlier by Johnson and Albrecht (1993) based on examination of haematocrits alone. Our results also strongly suggest that researchers wanting to measure effects of blood-feeding parasites on birds measure haemoglobin levels, not haematocrits.     

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     

Aromatic plants in blue tit Cyanistes caeruleus nests: no negative effect on blood-sucking Protocalliphora blow fly larvae

Nesting birds use several behavioural or physiological defence mechanisms against parasites. On Corsica, female blue tits Cyanistes caeruleus incorporate fresh fragments of a limited number of aromatic plants in the nest cup, from the end of nest construction until fledging. Some of these plants negatively affect bacterial growth and host location by blood-sucking mosquitoes in laboratory conditions. In natural populations, Corsican blue tit chicks are exposed to the highest levels of blood-sucking ectoparasitic blow flies Protocalliphora spp. reported in Europe. These ectoparasites can have severe negative effects on chick development and survival probabilities, especially when food constraints are elevated. Here we investigated in several natural Corsican blue tit populations the hypothesis that aromatic plants brought to the nest have anti-blow fly effects during the chick-rearing stage. We predicted that: 1) the amount of aromatic plants should be negatively related to blow fly infestation intensity across nests, 2) experimental addition of aromatic plants in nests should reduce blow fly infestation intensity, and 3) nestlings should be in better physical condition in nests where aromatic plants were experimentally added. No significant relation was found between amount of aromatic plants in nests and blow fly infestation intensity. Experimental addition of aromatic plants did not reduce blow fly infestation intensity and did not affect the chick phenotypic parameters we measured. We conclude that aromatic plants in blue tit nests are not used as a defence against ectoparasitic Protocalliphora blow flies in our study population.     

Avoidance,tolerance, and resistance to ectoparasites in nestling and adult tree swallows

We examined avoidance, tolerance, and resistance strategies of nestling and adult tree swallows Tachycineta bicolor in response to ectoparasitic blowflies Protocalliphora sialia. Tree swallows avoided settling in north‐facing nest boxes early in the breeding season. These boxes were more likely to be parasitized later in the season, suggesting that box selection may facilitate blowfly avoidance. After experimentally manipulating blowfly intensity, we found that nestlings were generally tolerant of parasitism. Parasites significantly reduced nestling blood hemoglobin but had no effect on nestling body mass, primary feather growth, age at fledging, or fledging success. Parents of parasitized nestlings did not increase their food provisioning rate to promote nestling tolerance. Adult female tree swallows demonstrated both tolerance and resistance: blowfly parasitism had no effect on adult hemoglobin and body mass, and those with higher P. sialia‐binding antibody levels had fewer blowfly larvae in their nests. Nestling antibodies were unrelated to blowfly intensity. Despite considerable variation among years, our results suggest that the costs of blowfly parasitism to nestling and adult tree swallows are modest, and limited to blood loss in nestlings. Future work should examine the effects of reduced blood hemoglobin on fledgling survival and the importance of parasite‐specific antibodies.     

Habitat effects on physiological stress response in nestling blue tits are mediated through parasitism

Abstract We investigated determinants of the physiological stress response mediated by stress proteins in blue tit Cyanistes caeruleus nestlings growing up in oak forests in central Spain, resulting from different forest management practices. We assessed circulating levels of the heat-shock protein HSP60 as an integrated physiological measure of the conditions experienced by nestlings during postnatal development. The effects of habitat quality and parasite infections on nestling rearing environment were then assessed through this measurement of stress response. Our results showed that newly acquired ecto- and hemoparasite infections were associated with forest habitat structural characteristics, higher prevalence of fleas and blood parasites in more mature forests, and higher prevalence of blowflies in degraded forests. While habitat characteristics did not explain variation in stress protein levels, infestation by blowfly larvae of the genus Protocalliphora and hematozoa infection by Leucocytozoon were significantly associated with higher levels of HSP60. Thus, upregulation of the expression of certain stress proteins seems to be a common physiological mechanism to alleviate the negative impact of parasite infections in growing birds. Habitat characteristics may thus indirectly determine growth conditions for forest birds mediated through their association with one of the most important selection pressures for offspring development, parasite infections.     

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.     

Philornis infection in blue‐black grassquits: impact on nestlings and risk factors involved

Parasitic botfly larvae (Philornis ssp., Diptera: Muscidae) are found in nests of several bird taxa, although prevalence and impact on nestling survival vary considerably among species. Here we describe patterns of botfly infestation in blue‐black grassquit Volatinia jacarina nestlings. We identified the most typically affected nestling body parts and assessed parasite prevalence, impact on nestling survival, and changes in nestling body shape. Additionally, we tested whether climatic conditions, nest morphology and habitat characteristics are associated with larvae abundance. Blue‐black grassquits had low breeding success (16% of eggs/nestlings survived to fledged; 19% of the nests fledged at least one), but most failures resulted from predation by vertebrate predators. We estimated that 1% of nestlings died due to botfly infestation, and the number of subcutaneous larvae (range 1–18) in a nestling's body did not predict fledging success. Infected chicks exhibited higher tarsus asymmetry. Thus, we argue that although botflies had a small impact on offspring survival, they may reduce fitness in adulthood. There was no evidence that environmental conditions and nest morphology are linked to the number of larvae on nestlings. Nesting areas with higher food supply had lower infestation rates. Possibly, food‐rich habitats allow parents to invest more time in offspring care (brooding nestlings), thus protecting them from fly attacks. Alternatively, vegetation composition could influence local invertebrate diversity, which could provide a natural trophic buffer against adult Philornis. The present study brings to light new perspectives concerning bird–botfly interaction.     

Adaptive host-abandonment of ectoparasites before fledging? Within-brood distribution of nest mites in house sparrow broods

We studied the within-brood distribution of a haematophagous mite Pellonyssus reedi living on nestling house sparrows (Passer domesticus) near the time of fledging. We measured the natural level of infestation of individual nestlings, and determined the feeding efficiency of mites, by scoring their feeding status. Within-brood distribution of mite loads was unrelated to nestling body mass, tarsus length, or immunocompetence. These results did not support parasite preference for large or susceptible hosts. Mite feeding-efficiency was also unrelated to these nestling characteristics, confirming that large nestlings or nestlings with less-developed immunocompetence did not provide superior feeding conditions for mites. Therefore, our results do not support the hypothesis that within-brood distribution of avian ectoparasites is explained by the parasites' preferences for characteristics, such as large body size or low immunocompetence, that make nestlings suitable hosts. On the other hand, we found that mite loads were negatively correlated with nestling age and feather length, suggesting that nestlings closer to fledging harbored fewer mites then their less-developed nestmates. Furthermore, feather length had a stronger relationship with parasite distribution than did nestling age. We presume, therefore, that feather characteristics, i.e., length, may serve as a signal for mites to perceive the ready-to-fledge state of nestlings, inducing abandonment behavior. These results support another, largely neglected hypothesis, i.e., that the avoidance or abandonment of those nestlings that are close to fledging may also explain the parasites' distribution in a brood. This hypothesis is based on the argument that many nest-dwelling ectoparasites breed in the nest material and emerge only periodically to feed on nestlings. In such parasites, the ability to recognize and avoid mature fledglings can be adaptive because this may help the parasites to avoid their removal from the nest so they can continue to reproduce by feeding on unfledged chicks of the current or later broods. Our results suggest that adaptive host-abandonment by nest-dwelling ectoparasites can influence within-brood parasite distributions around the time of fledging.     

Trichomoniasis in a Bonelli's eagle population in Spain

During 1980-97, trichomoniasis was detected in nestlings of Bonelli's eagle Hieraaetus fasciatus in Catalonia (Spain). In 1993 Trichomonas gallinae was isolated in 36% of nestlings (n = 39) and affected 41% of broods (n = 22). Overall, trichomoniasis was one of the most important single nestling mortality factor, accounting for 22% of total chick mortality, and causing the death of 2% of chicks. Trichomoniasis deaths took place during the second half of the nestling period. The median age at death was 45.5 days. Although the presence of the parasite was not related to the composition of the diet or parental age, pairs that developed the disease ate more pigeons and included more often non-adult birds. At present trichomoniasis apparently has little demographic impact on the Bonelli's eagle population in Catalonia, but the eventual spread of this disease in chicks and its unknown effects on adults might be of concern.     

Great Spotted Cuckoo Nestlings but not Magpie Nestlings Starve in Experimental Age‐Matched Broods

Nestlings of non‐evicting avian brood‐parasites have to compete for food with foster parents' own nestlings. The outcome of these competitive contests is determined mainly by body size differences between parasitic and host nestlings. As part of the coevolutionary arms race between brood parasites and their hosts at the nestling stage, it has been reported that some host foster parents discriminate against parasitic chicks and are reluctant to feed them. Here, by experimentally creating size‐matched broods of different composition (only magpie Pica pica chicks, only great spotted cuckoo Clamator glandarius chicks or mixed broods), we show that great spotted cuckoo chicks starved in 20.2 per cent (17 of 84) of the parasitized magpie nests even in absence of size asymmetries, while in none (0 of 72) of the nests a magpie chick starved. As far as we know, this is the first record of non‐evictor brood parasitic nestlings starving without being smaller than their host nestmates in a frequently used host species. Nest composition had no effect on chick starvation. The cuckoo nestling starved even in two of the nests occupied by only one cuckoo chick. Our results could be explained by (1) magpies being reluctant to feed cuckoo chicks; (2) parasitic chicks receiving lower‐quality food items or cuckoo nestlings being sensitive to some particular component of the diet (e.g. cereal grains); and (3) the existence of cuckoo chick discrimination ability by magpie foster parents.     

Experimental manipulation of temperature reduce ectoparasites in nests of blue tits Cyanistes caeruleus

Several models predict changes in the distributions and incidences of diseases associated with climate change. However, studies that investigate how microclimatic changes may affect host–parasite relationships are scarce. Here, we experimentally increased the temperature in blue tit Cyanistes caeruleus nest boxes during their breeding season to determine its effects on the parasitic abundance (i.e. of nest‐dwelling ectoparasites, blood‐sucking flying insects and hemoparasites) in nests and the host condition of nestlings and adults. The temperature was increased using heat mats placed underneath the nest material, which resulted in an average temperature increase of 3ºC and a reduction in relative humidity of about six units. The abundance of mites Dermanyssus gallinoides and blowfly pupae Protocalliphora azurea was significantly reduced in heated nest boxes. Although not statistically significant, a lower prevalence of flea larvae Ceratophyllus gallinae was also found in heated nests. However, heat treatment did not affect hemoparasite infection of adult blue tits or the body condition of adult and nestling blue tits. In conclusion, heat treatment in blue tit nests reduced nest‐dwelling ectoparasites yet without any apparent benefit for the host.     

Habitat-specific effects of a food supplementation experiment on immunocompetence in Eurasian Magpie Pica pica nestlings

Parasite pressure and nutrition are two of the most important factors affecting the trade-off between nestling growth and immune development. During development, energy and nutrients are often limited, and nestlings should only dedicate differentially more valuable resources to their immune system when the associated benefits are high (i.e. in situations of an increased risk of parasitism). In this study, we manipulated nutritional condition of Eurasian Magpie Pica pica nestlings by providing a food supplement. Additionally, the study area was subdivided into two categories of habitat (irrigated and arid) based on the presence of irrigation canals. Nestling diet composition was more varied in the irrigated compared with in the arid habitat. In addition, nestlings of the irrigated habitat showed a significantly higher infestation of both ectoparasites and blood parasites and a significantly higher cell-mediated immunity, but lower tarsus length compared with nestlings of the arid habitat. Food supplementation to nestlings did not affect tarsus length, but increased nestling cell-mediated immunity in the arid habitat only. Based on the recent demonstrated trade-off between growth and immunocompetence in nestlings, we suggest that differences between habitats in nestling diet and parasite prevalence may have caused different priority rules in the allocation of resources between both fitness traits.     

Reliable Information Content and Ontogenetic Shift in Begging Calls of Grey Warbler Nestlings

The most critical assumption of communication models regarding parent–offspring conflict is that food solicitation displays of genetic offspring are honest signals to elicit beneficial parental care. A critical requirement of honesty is the reliable change of perceivable aspects of begging calls with physiological needs. We experimentally tested whether and how the acoustic structure and begging call rate of individual Grey Warbler Gerygone igata nestlings change with hunger level and age. We also examined a rarely documented component of chick begging calls, namely the temporal dynamics of acoustic modulation after nestlings heard parental feeding calls. Begging call structure narrowed in frequency range and, surprisingly, decreased in amplitude as chick hunger levels increased. We also found that begging calls changed with chick age, with the frequency increasing and the duration decreasing for older chicks. These results indicate that the acoustic properties of nestling Grey Warbler begging calls are complex and may be used to signal several aspects of nestling traits, including hunger level and age (or size, a correlate of age). Overall, begging calls of Grey Warbler chicks appear to be honest, implying that parents are likely to benefit from relying on the acoustic features of their progeny’s calls which predict chick need. Our results have important implications regarding the reliability and information content of nestling solicitation signals for the brood parasite shining cuckoo Chrysococcyx lucidus exploiting Grey Warbler parental care, in that these begging‐call mimetic specialist cuckoos might also need to match closely the dynamics of acoustic features of their host chicks’ calls.     

Parasitism reduces the potential for evolution in a wild bird population

We tested the effect of detrimental environmental conditions during growth on the heritability of chick body size in a wild population of blue tits (Parus caeruleus) highly parasitized by blowfly larvae. During nine years, we experimentally induced deparasitized broods, whereas unmanipulated control broods remained heavily infested by two species of Protocalliphora ectoparasites. The heritability of tarsus length was significantly higher in deparasitized broods than control broods, due in part to a very low common brood environment effect in deparasitized broods. We also found evidence for significant genotype-by-environment interactions, which further reflected the effect of the ecological conditions on the expression of additive genetic effects and could represent an additional constraint on the evolution of tarsus length. To our knowledge, this experiment provides the first evidence of host quantitative genetics being influenced by parasitism, and illustrates the potential for parasitism to constrain an evolutionary response to selection.     

Nestling immunocompetence and testosterone covary with brood size in a songbird

The social and ecological conditions that individuals experience during early development have marked effects on their developmental trajectory. In songbirds, brood size is a key environmental factor affecting development, and experimental increases in brood size have been shown to have negative effects on growth, condition and fitness. Possible causes of decreased growth in chicks from enlarged broods are nutritional stress, crowding and increased social competition, i.e. environmental factors known to affect adult steroid levels (especially of testosterone and corticosteroids) in mammals and birds. Little, however, is known about environmental effects on steroid synthesis in nestlings. We addressed this question by following the development of zebra finch (Taeniopygia guttata) chicks that were cross-fostered and raised in different brood sizes. In line with previous findings, nestling growth and cell-mediated immunocompetence were negatively affected by brood size. Moreover, nestling testosterone levels covaried with treatment: plasma testosterone increased with experimental brood size. This result provides experimental evidence that levels of circulating testosterone in nestlings can be influenced by their physiological response to environmental conditions.     

Experimental evidence for host preference in a tick parasitizing songbird nestlings

Mechanisms of host preference in ectoparasites are important to the understanding of host‐parasite interactions. Since ectoparasites negatively affect the condition of their hosts, while the hosts’ condition itself may affect the parasites’ choice, separating the factors that drive host preference from parasite impact asks for experiments. We combined the data of two choice experiments to investigate the preference of the nidicolous tick Ixodes arboricola when exposed to the nestlings of a passerine bird (Parus major). In the first experiment, in which complete broods at hatching were exposed to an ecologically relevant number of ticks, the relationship between tick loads and nestlings’ developmental status was characterized by a distribution with the highest tick loads on the more developed nestlings. Host preference became more apparent at a smaller brood size, suggesting a role for host density. In a second experiment we evaluated host choice in a pairwise choice experiment, exposing pairs of siblings with contrasting developmental status to eight ticks. In the first and the second pair, a median developed nestling was linked with the most developed and the least developed nestling, respectively. Seventy‐two h after tick exposure we measured the innate constitutive humoral immunity and haematocrit. No differences were found in innate immunity, but the least developed nestlings had on average a lower haematocrit than the median and most developed nestlings. Significantly fewer ticks attached on the least developed nestling compared to the median nestling, and this difference was more pronounced when the innate immunity of the median developed nestling was higher. No difference in tick load was found among the median and best developed nestlings. The linkage between host preference and host physiological condition provide further insight in the mechanisms driving ectoparasite aggregation, which is important for the population dynamics of host, ticks and tick‐transmitted pathogens.     

Parental infanticide in birds through early eviction from the nest: rare or under‐reported?

Avian parental infanticide is apparently a rare phenomenon judging from the scant reports in the literature. However, unexplained cases of single nestling disappearance or of apparent fall from the nest are rather common and are routinely attributed to parental eviction of dead nestlings, single chick predation or dislodging of nestlings through errors by nestlings or parents. During long‐term studies of pied flycatchers Ficedula hypoleuca in central Spain 29 cases of eviction from the nest cup of mostly hatchlings or small, heterothermic nestlings were recorded, leading invariably and quickly to death. Parental errors and failed attempts to predate single chicks are unlikely in these cases. Although the incidence of recorded evictions was mostly below 5% of nests, it reached higher levels in years and populations where reproductive success was low. Some cases were preceded by prior egg eviction. In these studies, there were unexplained disappearances affecting 3.7% of eggs laid which amounted to 20% of all losses. During studies of three other passerine cavity nesting species, similar cases were observed. The rarity of reports of parentally evicted nestlings is apparently based on the difficulty of directly observing parents evicting live nestlings but may also be due to observer bias as ejections of dead nestlings, erroneous dislodgings or single‐chick predation events are also rarely observed but are normally given as reasons for single‐chick losses. Field researchers should attempt to determine the real causes of partial brood loss before assuming that parsimony excludes parental infanticide through eviction.     

Weather dependent effects of nest ectoparasites on their bird hosts

This study reports the relationships between rainfall and ambient temperature with the abundances and prevalences of three species of ectoparasitic arthropods (viz, mites, blowfly larvae, fleas) in pied flycatcher Ficedula hypoleuca nests in three different breeding seasons In addition to its effects on the growth of nestling pied flycatchers, weather conditions were found to determine patterns of abundance and prevalence of ectoparasites Nest ectoparasites had detrimental effects on the fitness (nestling growth and survival until fledgling) of their hosts although the effects and the identity of harmful ectoparasites varied across the years Among the three species of nest ectoparasites, mites had the most consistent harmful effects on nestling growth Fleas were detrimental in the more cold and rainy year, while blowflies caused nestling mortality in the wanner year Different host-parasite interactions were present each year, most likely due to the effects of weather on the activity and timing of development of parasite populations