Juan Rivero-de Aguilar

On the specificity of avian blood parasites: revealing specific and generalist relationships between haemosporidians and biting midges

The study of host–parasite relationships involving vector‐borne parasites requires understanding interactions between parasites and vectors. The capacity of haemosporidians to infect insects has clear evolutionary consequences for the transmission of diseases. Here, we investigated (i) the associations between blood parasites, biting midges and birds and (ii) the potential specificity between biting midge and haemosporidian haplotypes. A total of 629 parous biting midges Culicoides and 224 wild birds (belonging to seven species) from a locality of central Spain were individually examined for the presence of Haemoproteus and Plasmodium parasites by sequencing a fragment of cytochrome B. Biting midges were identified morphologically and characterized on the basis of a fragment of the cytochrome c oxidase (COI) gene. Overall, 12 Haemoproteus and three Plasmodium haplotypes were isolated and sequenced. Among them, 10 haplotypes were exclusively isolated from biting midges, three haplotypes only from birds and two haplotypes from both biting midges and birds. Biting midge haplotypes showed both specific and generalist relationships with Haemoproteus haplotypes but only generalist relationships with Plasmodium haplotypes. Several C. festivipennis and C. kibunesis haplotypes established significant coevolutionary links with Haemoproteus haplotypes. These results shed light on the specificity of interactions between vectors and blood parasites.

Carotenoid-based plumage colouration is associated with blood parasite richness and stress protein levels in blue tits (Cyanistes caeruleus).

Carotenoids are molecules that birds are not able to synthesize and therefore, must be acquired through their diet. These pigments, besides their function of giving birds red and yellow colouration when deposited in feathers, seem to act as immune-stimulators and antioxidants in the organism. Hence, only the healthiest individuals would be able to express carotenoid-based ornaments to a larger extent without compromising the physiological functions of carotenoids. Various studies have reported that birds infected by parasites are paler than those uninfected, but, to our knowledge, none of them has assessed the possible effect of multiple infections by blood parasites on plumage colour. By comparing the yellow colour in the breast plumage of blue tits, Cyanistes caeruleus, between birds infected by different numbers of blood parasite genera, we found that those birds infected by more than one genus were paler than those parasitized just by one. In addition, we examined the potential role of carotenoid-based plumage colour of blue tits as a long-term indicator of other parameters of health status, such as body condition and immunoglobulin and heat shock protein (HSP) levels. Our results indicate that more brightly coloured birds had lower HSP70 levels than paler birds, but we did not find any significant association between colour and body condition or immunoglobulin levels. In addition, we found a positive significant association between Haemoproteus density of infection and HSP60 levels. Overall, these results support the role of carotenoid-based colours as indicators of health status in blue tits and show detrimental effects of parasitism on this character.

Nest-Dwelling Ectoparasites of Two Sympatric Hole-Nesting Passerines in Relation to Nest Composition: An Experimental Study

Abstract: There are often marked differences in the incidence of nest-dwelling ectoparasite species on different coexisting and similar avian host species. This has been shown especially for fleas (Siphonaptera), larvae of flies (Diptera), and mites (Acarina) in nests of tits and flycatchers breeding in nest-boxes in close proximity to each other. One of the possible reasons for these differences is the marked differences in nest composition between avian species. We show here differences in ectoparasite presence and nest composition for blue tits (Cyanistes caeruleus) and pied flycatchers (Ficedula hypoleuca) coexisting in oak forests in central Spain. There also may be intraspecific differences in local preferences for nest-building materials according to availability of plant materials, which could be due to arthropod repellent properties of different potential nest components. We show here a local difference in nest composition between 2 pied flycatcher populations in relation to availability of a preferred material associated with higher ectoparasite presence in the locality without the preferred nest material. We test the hypotheses that differential incidence of ectoparasites at the interspecific and intraspecific levels may depend on nest composition. We conducted a nest exchange experiment in one study locality in 2007 placing in nest-boxes occupied by flycatchers 1) nests constructed by blue tits in 2006 in another locality and removed before use and stored frozen, 2) nests constructed by flycatchers in 2006 in another locality with different nest composition and removed before use and stored frozen, and 3) nests constructed by other flycatcher pairs in the same study locality in 2007. Another group of flycatcher nests was kept as pure control, while a few blue tit nests constructed in 2007 and taken over by flycatchers were used for comparison with nests of treatment 1. No effect on presence of mites and blowflies of either nest-constructing species or locality of construction was observed for pied flycatcher nests, and for fleas only an effect of locality but not of nest constructing species was detected. On the other hand, presence of mites and blowflies differed between nests constructed by blue tits and occupied by either blue tits or pied flycatchers. Nest composition does not explain the differential incidence of nest-dwelling ectoparasites on coexisting avian host species. Nomenclature: Moss, 1978; Cramp, Perrins & Brooks, 1993.

Characterization of MHC-I in the blue tit (Cyanistes caeruleus) reveals low levels of genetic diversity and trans-population evolution across European populations

The major histcompatibility complex (MHC) is a vital component of the adaptive immune system in all vertebrates. This study is the first to characterize MHC class I (MHC-I) in blue tits (Cyanistes caeruleus), and we use MHC-I exon 3 sequence data from individuals originating from three locations across Europe: Spain, the Netherlands to Sweden. Our phylogeny of the 17 blue tit MHC-I alleles contains one allele cluster with low nucleotide diversity compared to the remaining more diverse alleles. We found a significant evidence for balancing selection in the peptide-binding region in the diverse allele group only. No separation according to geographic location was found in the phylogeny of alleles. Although the number of MHC-I loci of the blue tit is comparable to that of other passerine species, the nucleotide diversity of MHC-I appears to be much lower than that of other passerine species, including the closely related great tit (Parus major) and the severely inbred Seychelles warbler (Acrocephalus sechellensis). We believe that this initial MHC-I characterization in blue tits provides an important step towards understanding the mechanisms shaping MHC-I diversity in natural populations.

Assessing the effects of climate on host-parasite interactions: a comparative study of European birds and their parasites.

Background Climate change potentially has important effects on distribution, abundance, transmission and virulence of parasites in wild populations of animals. Methodology/Principal Finding Here we analyzed paired information on 89 parasite populations for 24 species of bird hosts some years ago and again in 2010 with an average interval of 10 years. The parasite taxa included protozoa, feather parasites, diptera, ticks, mites and fleas. We investigated whether change in abundance and prevalence of parasites was related to change in body condition, reproduction and population size of hosts. We conducted analyses based on the entire dataset, but also on a restricted dataset with intervals between study years being 5–15 years. Parasite abundance increased over time when restricting the analyses to datasets with an interval of 5–15 years, with no significant effect of changes in temperature at the time of breeding among study sites. Changes in host body condition and clutch size were related to change in temperature between first and second study year. In addition, changes in clutch size, brood size and body condition of hosts were correlated with change in abundance of parasites. Finally, changes in population size of hosts were not significantly related to changes in abundance of parasites or their prevalence. Conclusions/Significance Climate change is associated with a general increase in parasite abundance. Variation in laying date depended on locality and was associated with latitude while body condition of hosts was associated with a change in temperature. Because clutch size, brood size and body condition were associated with change in parasitism, these results suggest that parasites, perhaps mediated through the indirect effects of temperature, may affect fecundity and condition of their hosts. The conclusions were particularly in accordance with predictions when the restricted dataset with intervals of 5–15 years was used, suggesting that short intervals may bias findings.

Do secretions from the uropygial gland of birds attract biting midges and black flies

Bird susceptibility to attacks by blood-sucking flying insects could be influenced by urogypial gland secretions. To determine the effect of these secretions on biting midges and black flies, we set up a series of tests. First, we placed uropygial gland secretions from blue tit Cyanistes caeruleus broods inside empty nest boxes while empty nest boxes without gland secretions were treated as controls. Blue tit broods, from which we had obtained uropygial secretions, were affected by biting midges and black flies. However, these insects were absent in nest boxes both with and without secretions from nestlings’ uropygial glands. We subsequently tested for the effects of uropygial gland secretions from feral pigeons Columba livia monitoring the number of biting midges captured using miniature CDC traps. There was no significant difference in the number of biting midges captured. Overall, our results did not support a potential role of avian uropygial gland secretions in attracting biting midges and black flies.

MHC class II B diversity in blue tits: a preliminary study

In this study, we partly characterize major histocompatibility complex (MHC) class II B in the blue tit (Cyanistes caeruleus). A total of 22 individuals from three different European locations: Spain, The Netherlands, and Sweden were screened for MHC allelic diversity. The MHC genes were investigated using both PCR-based methods and unamplified genomic DNA with restriction fragment length polymorphism (RFLP) and southern blots. A total of 13 different exon 2 sequences were obtained independently from DNA and/or RNA, thus confirming gene transcription and likely functionality of the genes. Nine out of 13 alleles were found in more than one country, and two alleles appeared in all countries. Positive selection was detected in the region coding for the peptide binding region (PBR). A maximum of three alleles per individual was detected by sequencing and the RFLP pattern consisted of 4–7 fragments, indicating a minimum number of 2–4 loci per individual. A phylogenetic analysis, demonstrated that the blue tit sequences are divergent compared to sequences from other passerines resembling a different MHC lineage than those possessed by most passerines studied to date.

Testing a New Method for Reducing Ectoparasite Infestation in Nest-Boxes

Summary. In wild bird populations nestlings are commonly infested by ectoparasites. The effects that ectoparasites exert on host fitness usually become evident after the complete elimination of parasites or a substantial reduction in their abundance. Among the most common elimination methods in ecological studies, the use of chemical insecticides is traditionally preferred. However, the application of several doses is usually needed because the efficiency of insecticides decreases over time. This results in increasing toxicity effects and disturbance of both parents and nestlings. In the present study, we tested the efficacy of Inesfly, a new insecticidal paint. Inesfly acts by releasing active water-soluble compounds progressively over a period, therefore having a longer-lasting effect than other insecticides. By applying this insecticidal paint inside nest-boxes used by blue tits Cyanistes caeruleus during the breeding season, we investigated its effect on the abundance of blackfly (Simuliidae), biting midge (Culicidae), flea (Ceratophyllidae), mite (Dermanyssidae) and blowfly (Calliphoridae) larvae. The insecticide significantly reduced the abundance of Protocalliphora azurea blowflies, while other parasites remained unaffected. Our results show that Inesfly was ineffective against ectoparasites infesting blue tit nest-boxes, blowflies excepted, at least at the dose applied. Finally, no negative effects on nestlings were reported following the use of this insecticide.