Luz Garcia-Longoria

Malaria infection and feather growth rate predict reproductive success in house martins

Carry-over effects take place when events occurring in one season influence individual performance in a subsequent season. Blood parasites (e.g. Plasmodium and Haemoproteus) have strong negative effects on the body condition of their hosts and could slow the rate of feather growth on the wintering grounds. In turn, these winter moult costs could reduce reproductive success in the following breeding season. In house martins Delichon urbica captured and studied at a breeding site in Europe, we used ptilochronology to measure growth rate of tail feathers moulted on the winter range in Africa, and assessed infection status of blood parasites transmitted on the wintering grounds. We found a negative association between haemosporidian parasite infection status and inferred growth rate of tail feathers. A low feather growth rate and blood parasite infections were related to a delay in laying date in their European breeding quarters. In addition, clutch size and the number of fledglings were negatively related to a delayed laying date and blood parasite infection. These results stress the importance of blood parasites and feather growth rate as potentially mechanisms driving carry-over effects to explain fitness differences in wild populations of migratory birds.

Do malaria parasites manipulate the escape behaviour of their avian hosts? An experimental study

Escape behaviour is the behaviour that birds and other animals display when already caught by a predator. An individual exhibiting higher intensity of such anti-predator behaviour could have greater probabilities of escape from predators. Parasites are known to affect different aspects of host behaviour to increase their own fitness. Vector-transmitted parasites such as malaria parasites should gain by manipulating their hosts to enhance the probability of transmission. Several studies have shown that malaria parasites can manipulate their vectors leading to increased transmission success. However, little is known about whether malaria parasites can manipulate escape behaviour of their avian hosts thereby increasing the spread of the parasite. Here we used an experimental approach to explore if Plasmodium relictum can manipulate the escape behaviour of one of its most common avian hosts, the house sparrow Passer domesticus. We experimentally tested whether malaria parasites manipulate the escape behaviour of their avian host. We showed a decrease in the intensity of biting and tonic immobility after removal of infection with anti-malaria medication compared to pre-experimental behaviour. These outcomes suggest that infected sparrows performed more intense escape behaviour, which would increase the likelihood of individuals escaping from predators, but also benefit the parasite by increasing its transmission opportunities.

Volume and antimicrobial activity of secretions of the uropygial gland are correlated with malaria infection in house sparrows

BackgroundAnimals have developed a wide range of defensive mechanisms against parasites to reduce the likelihood of infection and its negative fitness costs. The uropygial gland is an exocrine gland that produces antimicrobial and antifungal secretions with properties used as a defensive barrier on skin and plumage. This secretion has been proposed to affect the interaction between avian hosts and their ectoparasites. Because uropygial secretions may constitute a defense mechanism against ectoparasites, this may result in a reduction in prevalence of blood parasites that are transmitted by ectoparasitic vectors. Furthermore, other studies pointed out that vectors could be attracted by uropygial secretions and hence increase the probability of becoming infected. Here we explored the relationship between uropygial gland size, antimicrobial activity of uropygial secretions and malaria infection in house sparrows Passer domesticus.MethodsA nested-PCR was used to identify blood parasites infection. Flow cytometry detecting absolute cell counting assessed antimicrobial activity of the uropygial gland secretionResultsUninfected house sparrows had larger uropygial glands and higher antimicrobial activity in uropygial secretions than infected individuals. We found a positive association between uropygial gland size and scaled body mass index, but only in uninfected sparrows. Female house sparrows had larger uropygial glands and higher antimicrobial activity of gland secretions than males.ConclusionThese findings suggest that uropygial gland secretions may play an important role as a defensive mechanism against malaria infection.

Molecular identification of the chitinase genes in Plasmodium relictum

BackgroundMalaria parasites need to synthesize chitinase in order to go through the peritrophic membrane, which is created around the mosquito midgut, to complete its life cycle. In mammalian malaria species, the chitinase gene comprises either a large or a short copy. In the avian malaria parasites Plasmodium gallinaceum both copies are present, suggesting that a gene duplication in the ancestor to these extant species preceded the loss of either the long or the short copy in Plasmodium parasites of mammals. Plasmodium gallinaceum is not the most widespread and harmful parasite of birds. This study is the first to search for and identify the chitinase gene in one of the most prevalent avian malaria parasites, Plasmodium relictum.MethodsBoth copies of P. gallinaceum chitinase were used as reference sequences for primer design. Different sequences of Plasmodium spp. were used to build the phylogenetic tree of chitinase gene.ResultsThe gene encoding for chitinase was identified in isolates of two mitochondrial lineages of P. relictum (SGS1 and GRW4). The chitinase found in these two lineages consists both of the long (PrCHT1) and the short (PrCHT2) copy. The genetic differences found in the long copy of the chitinase gene between SGS1 and GRW4 were higher than the difference observed for the cytochrome b gene.ConclusionThe identification of both copies in P. relictum sheds light on the phylogenetic relationship of the chitinase gene in the genus Plasmodium. Due to its high variability, the chitinase gene could be used to study the genetic population structure in isolates from different host species and geographic regions.

Environmental conditions during winter predict age- and sex-specific differences in reproductive success of a trans-Saharan migratory bird

Previous studies have linked winter habitat with subsequent breeding phenology and physical condition of migratory birds, but few have found delayed effects of winter habitat on subsequent reproductive success. The aim of this study was to test if African winter habitat is related to subsequent reproductive success of house martins (Delichon urbicum) breeding at a colony in Spain. We measured stable isotope (δ2H, δ13C, δ15N) values from feathers moulted in West Africa and used confirmatory path analysis to test if isotopic values of winter-grown feathers were related to reproductive success through the mediation of breeding phenology and body condition. We conducted separate analyses for males, females and age classes (yearlings vs ≥ 2 years old). Experienced males wintering in habitats of higher rainfall (as inferred from lower feather δ2H values) were in better body condition and produced more offspring during the subsequent breeding season. In contrast, we did not find any effect of winter habitat on reproductive success of young males or females. These findings provide evidence consistent with a complex causal link between winter habitat quality and subsequent breeding success of long-distance migratory songbirds.

Detecting transmission areas of malaria parasites in a migratory bird species.

The identification of the regions where vector-borne diseases are transmitted is essential to study transmission patterns and to recognize future changes in environmental conditions that may potentially influence the transmission areas. SGS1, one of the lineages of Plasmodium relictum, is known to have active transmission in tropical Africa and temperate regions of Europe. Nuclear sequence data from isolates infected with SGS1 (based on merozoite surface protein 1 (MSP1) allelic diversity) have provided new insights on the distribution and transmission areas of these allelic variants. For example, MSP1 alleles transmitted in Africa differ from those transmitted in Europe, suggesting the existence of two populations of SGS1 lineages. However, no study has analysed the distribution of African and European transmitted alleles in Afro-Palearctic migratory birds. With this aim, we used a highly variable molecular marker to investigate whether juvenile house martins become infected in Europe before their first migration to Africa. We explored the MSP1 allelic diversity of P. relictum in adult and juvenile house martins. We found that juveniles were infected with SGS1 during their first weeks of life, confirming active transmission of SGS1 to house martins in Europe. Moreover, we found that all the juveniles and most of adults were infected with one European transmitted MSP1 allele, whereas two adult birds were infected with two African transmitted MSP1 alleles. These findings suggest that house martins are exposed to different strains of P. relictum in their winter and breeding quarters.

Host-parasite interaction explains variation in prevalence of avian haemosporidians at the community level

Parasites are a selective force that shape host community structure and dynamics, but host communities can also influence parasitism. Understanding the dual nature from host-parasite interactions can be facilitated by quantifying the variation in parasite prevalence (i.e. the proportion of infected host individuals in a population) among host species and then comparing that variation to other ecological factors that are known to also shape host communities. Avian haemosporidian parasites (e.g. Plasmodium and Haemoproteus) are abundant and widespread representing an excellent model for the study of host-parasite interactions. Several geographic and environmental factors have been suggested to determine prevalence of avian haemosporidians in bird communities. However, much remains to be known regarding whether host and parasite traits, represented by phylogenetic distances among species and degree of specialization in host-parasite relationships, can influence parasite prevalence. The aims of this study were to analyze factors affecting prevalence in a bird community and to test whether the degree of parasite specialization on their hosts is determined by host traits. Our statistical analyses suggest that prevalence is mainly determined by the interaction between host species and parasite lineages where tolerance and/or susceptibility to parasites plays an essential role. Additionally, we found that although some of the parasite lineages infected a low number of bird species, the species they infected were distantly related and therefore the parasites themselves should not be considered typical host specialists. Prevalence was higher for generalist than for specialist parasites in some, but not all, host species. These results suggest that prevalence mainly results from the interaction between host immune defences and parasite exploitation strategies wherein the result of an association between particular parasite lineages and particular host species is idiosyncratic.

New Approaches for an Old Disease: Studies on Avian Malaria Parasites for the Twenty-First Century Challenges

Emerging infectious diseases (EIDs) impose a burden on economies and public health. Because EIDs on wildlife are mainly affected by environmental and ecological factors, the study of EIDs in wildlife provides valuable insights to improve our understanding on their causes and their impact on global health. Malaria is an EID that has increased its prevalence in the last few decades at an alarming rate. Avian malaria parasites are abundant, widespread and diverse, which turn these parasites into an excellent model for the study of EIDs. In the face of new health and environmental challenges in the twentyirst century, studies on avian malaria will provide new approaches for this old disease. The identfiication of essential genes for the malaria invasion, the study of modification of host behaviour by malaria parasites in order to promote the parasite transmission, and the knowledge of factors contributing to the emergence of infectious diseases in wildlife are essential for understanding parasite epidemiology, local patterns of virulence and evolution of host resistance. In this chapter, we will review the results of some recent investigations on these topics that will be useful for predicting and preventing EIDs in wildlife, livestock and humans.