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.     

Uropygial gland size correlates with feather holes,body condition and wingbar size in the house sparrow Passer domesticus

The uropygial gland is an organ exclusive of birds that secretes an oily substance, the uropygial secretion, the functions of which are still debated. One of the proposed hypothesis is its possible action against chewing lice (order Phthiraptera), a group of avian ectoparasites that feed on feathers, causing different types of harm. However, this hypothesis lacks support. The present study analyses the relationship between uropygial gland size and the number of feather holes (which is correlated with the load of chewing lice) in the house sparrow Passer domesticus. Moreover, the relationship between the uropygial gland size and different aspects of sparrow health (body condition, immunocompetence and haematocrit), as well as sexually selected traits in males (badge and wingbar size), is tested. The results show a negative correlation between uropygial gland size and number of feather holes, a result found both years of the study. This result supports the hypothesis that uropygial secretion is used against chewing lice. Uropygial gland size also correlated positively with body condition (residuals of body mass relative to tarsus length) and immunocompetence, being therefore related to bird health. After a year in captivity, with resources provided ad libitum, no correlation was found between individual uropygial gland size and body condition or haematocrit, perhaps because the negative effect that chewing lice exert on bird health was offset by captivity conditions. Uropygial gland size was not correlated with badge size, but it was correlated with wingbar size, which furthermore supports the contention that this sexually selected signal acts as an indicator of lice resistance in the house sparrow. In summary, this study supports the idea of a positive relationship between uropygial gland and bird health in the house sparrow, the gland secretion affording resistance against chewing lice.     

Septum volume and food-storing behavior are related in parids

The hippocampal formation (HF) of food-storing birds is larger than non-storing species, and the size of the HF in food-storing Black-Capped Chickadees (Poecile atricapillus) varies seasonally. We examined whether the volume of the septum, a medial forebrain structure that shares reciprocal connections with the HF, demonstrates the same species and seasonal variation as has been shown in the HF. We compared septum volume in three parid species; non-storing Blue Tits (Parus caeruleus) and Great Tits (Parus major), and food-storing Black-Capped Chickadees. We found the relative septum volume to be larger in chickadees than in the non-storing species. We also compared septum and nucleus of the diagonal band (NDB) volume of Black-Capped Chickadees at different times of the year. We found that the relative septum volume varies seasonally in food-storing birds. The volume of the NDB does not vary seasonally. Due to the observed species and seasonal variation, the septum, like the hippocampal formation of food-storing birds, may be specialized for some aspects of food-storing and spatial memory.     

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.     

Multiple ornaments are positively related to male survival in the common pheasant

Several empirical studies have reported a positive relation between male viability and the expression of sexually selected traits, but others have reported a significant negative relation. Using the ability to evade predators as an indicator of male viability, we evaluated the direction of this relationship in a free-ranging population of common pheasants,Phasianus colchicus , which have multiple ornaments and are sexually dimorphic in tail length and in ornaments such as wattles and tarsal spurs. We translocated 72 males into a protected area and radiotracked them during the breeding seasons of 3 years. Before releasing them, we measured their body weight, wing and tail length, wattle height and spur length. Male survivors had larger multiple ornaments, regardless of age, than males that were killed by predators but survival selection on wing length and body weight was nonsignificant, showing that selection on male ornaments was not the result of selection on correlated traits.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Discovering the migration and non‐breeding areas of sand martins and house martins breeding in the Pannonian basin (central‐eastern Europe)

The central‐eastern European populations of sand martin and house martin have declined in the last decades. The drivers for this decline cannot be identified as long as the whereabouts of these long distance migrants remain unknown outside the breeding season. Ringing recoveries of sand martins from central‐eastern Europe are widely scattered in the Mediterranean basin and in Africa, suggesting various migration routes and a broad non‐breeding range. The European populations of house martins are assumed to be longitudinally separated across their non‐breeding range and thus narrow population‐specific non‐breeding areas are expected. By using geolocators, we identified for the first time, the migration routes and non‐breeding areas of sand martins (n = 4) and house martins (n = 5) breeding in central‐eastern Europe. In autumn, the Carpathian Bend and northern parts of the Balkan Peninsula serve as important pre‐migration areas for both species. All individuals crossed the Mediterranean Sea from Greece to Libya. Sand martins spent the non‐breeding season in northern Cameroon and the Lake Chad Basin, within less than a 700 km radius, while house martins were widely scattered in three distinct regions in central, eastern, and southern Africa. Thus, for both species, the expected strength of migratory connectivity could not be confirmed. House martins, but not sand martins, migrated about twice as fast in spring compared to autumn. The spring migration started with a net average speed of > 400 km d^–1 for sand martins, and > 800 km d^–1 for house martins. However, both species used several stopover sites for 0.5–4 d and were stationary for nearly half of their spring migration. Arrival at breeding grounds was mainly related to departure from the last sub‐Saharan non‐breeding site rather than distance, route, or stopovers. We assume a strong carry‐over effect on timing in spring.     

Problem‐solving skills are linked to parental care and offspring survival in wild house sparrows

Individuals within a population often exhibit consistent differences in important behavioral traits such as parental care. One interesting, yet largely unexplored explanation for the existence of these consistent differences among parents is the idea that cognitive differences between individuals could lead to between‐individual variation in parenting behavior. I used a wild population of house sparrows (Passer domesticus) to test the nature of the relationship between aspects of cognitive ability (problem‐solving performance and learning) and parental care behavior, both measured in the wild. Furthermore, because parental care is tightly linked to fitness, I also investigated the relationship between problem‐solving performance and offspring survival. Parent sparrows were presented with a novel problem‐solving task that required them to remove an obstacle to obtain food. While there was no relationship between the ability to complete the task and measures of parental care (nestling provisioning rate or likelihood of provisioning with large food items), parents that solved the task quickly had higher provisioning rates than slow solvers. Additionally, the ability of fathers to complete the problem‐solving task was positively related to offspring survival. These results provide evidence that aspects of problem‐solving performance are positively correlated with parenting behavior and fitness in the wild.     

Genetic dissection of Plasmodium falciparum blood infection levels and other complex traits related to human malaria infection

There is accumulating evidence of host genetic control in malaria infection and, in humans, some genes have been associated with severe malaria. Nevertheless, other important genes controlling blood infection levels, malarial disease and immune responses are likely to be identified. In this paper, we focus on segregation and linkage analyses of blood infection levels in an urban population living in Burkina Faso. We found evidence of a complex genetic control and a linkage to chromosome 5q31-q33. The identification of genes controlling complex traits related to malaria infection should be helpful in understanding protective mechanisms and the relationship between infection, malaria attacks and severe malaria.     

Intraseasonal patterns in shorebird nest survival are related to nest age and defence behaviour

Nest survival may vary throughout the breeding season for many bird species, and the nature of this temporal variation can reveal the links between birds, their predators, and other components of the ecosystem. We used program Mark to model patterns in nest survival within the breeding season for shorebirds nesting on arctic tundra. From 2000 to 2007, we monitored 521 nests of five shorebird species and found strong evidence for variation in nest survival within a nesting season. Daily nest survival was lowest in the mid-season in 5 of 8 years, but the timing and magnitude of the lows varied. We found no evidence that this quadratic time effect was driven by seasonal changes in weather or the abundance of predators. Contrary to our prediction, the risk of predation was not greatest when the number of active shorebird nests was highest. Although nest abundance reached a maximum near the middle of the breeding season, a daily index of shorebird nest activity was not supported as a predictor of nest survival in the models. Predators’ access to other diet items, in addition to shorebird nests, may instead determine the temporal patterns of nest predation. Nest survival also displayed a positive, linear relationship with nest age; however, this effect was most pronounced among species with biparental incubation. Among biparental species, parents defended older nests with greater intensity. We did not detect a similar relationship among uniparental species, and conclude that the stronger relationship between nest age and both nest defence and nest survival for biparental species reflects that their nest defence is more effective.     

Uropygial gland size,feather holes and moult performance in the House Sparrow Passer domesticus

Feather holes represent damage to the plumage of birds and are correlated with delayed moult. Uropygial gland size is negatively correlated with feather holes. Consequently, it was predicted that birds with smaller uropygial glands would have more feather holes, and that this would affect moult performance. I examined this prediction in the House Sparrow Passer domesticus. Individuals with smaller uropygial glands had more feather holes, and those with more feather holes moulted later and faster. Therefore, uropygial gland size seemed to affect moult performance via its effect on feather holes. Uropygial gland size may have a positive effect on plumage quality, through a negative effect on feather holes, and therefore on moult timing and speed.     

Migration phenology and winter habitat quality are related to circulating androgen in a long‐distance migratory bird

In migratory birds, the timing of departure from wintering grounds is often dependant on the quality of habitat on an individual's territory and may influence individual fitness, resulting in an interaction of life history stages across large geographical distances. American redstart Setophaga ruticilla males who overwinter in high quality habitats arrive early to breed and subsequently produce more offspring than late arrivers. Since many migratory species overlap vernal migration with the physiological transition to breeding, we examined if breeding preparation plays a role in this seasonal interaction. We tested the hypothesis that early arriving male redstarts from high quality winter habitats are in superior breeding condition by simultaneously measuring winter habitat quality (stable‐carbon isotopes) and breeding preparation (circulating androgen, cloacal protuberance (CP) diameter) upon arrival at breeding grounds. Compared with late arrivers, early arriving males were from higher quality winter habitats and had higher androgen, but smaller CPs. Males arriving with higher androgen were in more advanced physiological migratory condition, as measured by haematocrit. Early arrivers were more likely to successfully breed, but there was no significant relationship between androgen upon arrival and breeding success. One possible explanation for these relationships is that androgen measured during arrival is most relevant in a migratory context, such that birds with high androgen may benefit from effects on migratory condition, positively influencing fitness through earlier arrival.     

Hepatocyte growth factor and its receptor are required for malaria infection

Plasmodium, the causative agent of malaria, must first infect hepatocytes to initiate a mammalian infection. Sporozoites migrate through several hepatocytes, by breaching their plasma membranes, before infection is finally established in one of them. Here we show that wounding of hepatocytes by sporozoite migration induces the secretion of hepatocyte growth factor (HGF), which renders hepatocytes susceptible to infection. Infection depends on activation of the HGF receptor, MET, by secreted HGF. The malaria parasite exploits MET not as a primary binding site, but as a mediator of signals that make the host cell susceptible to infection. HGF/MET signaling induces rearrangements of the host-cell actin cytoskeleton that are required for the early development of the parasites within hepatocytes. Our findings identify HGF and MET as potential targets for new approaches to malaria prevention.     

Associations between malaria and MHC genes in a migratory songbird

Malaria parasites are a widespread and species-rich group infecting many wild populations of mammals, birds and reptiles. Studies on humans have demonstrated that genetic factors play a key role in the susceptibility and outcome of malaria infections. Until the present study, it has not been examined whether genetic variation in hosts is important for the outcome of malaria infections in natural avian populations. We investigated associations between major histocompatibility complex (MHC) genes and prevalence of three different avian malaria parasites (Haemoproteus payevskyi (GRW1), Plasmodium sp. (GRW2) and Plasmodium sp. (GRW4)) in a long-term study of great reed warblers Acrocephalus arundinaceus. We hypothesized that the MHC genes could either give full protection against a malaria infection, or confer protection against lethal malaria and direct the infection towards being milder. We found a positive association between numbers of MHC class I alleles (a measure of level of heterozygosity) and prevalence of the GRW2 parasite, suggesting the latter scenario. There was also a positive association between a specific MHC allele (B4b), previously shown to be under frequency-dependent selection in the study population, and prevalence of GRW2. These associations suggest that individuals carrying either a large number of MHC alleles or a specific MHC allele are protected against lethal malaria infections.     

Septum volume and food‐storing behavior are related in parids

The hippocampal formation (HF) of food‐storing birds is larger than non‐storing species, and the size of the HF in food‐storing Black‐Capped Chickadees (Poecile atricapillus) varies seasonally. We examined whether the volume of the septum, a medial forebrain structure that shares reciprocal connections with the HF, demonstrates the same species and seasonal variation as has been shown in the HF. We compared septum volume in three parid species; non‐storing Blue Tits (Parus caeruleus) and Great Tits (Parus major), and food‐storing Black‐Capped Chickadees. We found the relative septum volume to be larger in chickadees than in the non‐storing species. We also compared septum and nucleus of the diagonal band (NDB) volume of Black‐Capped Chickadees at different times of the year. We found that the relative septum volume varies seasonally in food‐storing birds. The volume of the NDB does not vary seasonally. Due to the observed species and seasonal variation, the septum, like the hippocampal formation of food‐storing birds, may be specialized for some aspects of food‐storing and spatial memory. © 2002 Wiley Periodicals, Inc. J Neurobiol 51: 215–222, 2002     

Primary peak and chronic malaria infection levels are correlated in experimentally infected great reed warblers

SUMMARY Malaria parasites often manage to maintain an infection for several months or years in their vertebrate hosts. In humans, rodents and birds, most of the fitness costs associated with malaria infections are in the short initial primary (high parasitaemia) phase of the infection, whereas the chronic phase (low parasitaemia) is more benign to the host. In wild birds, malaria parasites have mainly been studied during the chronic phase of the infection. This is because the initial primary phase of infection is short in duration and infected birds with severe disease symptoms tend to hide in sheltered places and are thus rarely caught and sampled. We therefore wanted to investigate the relationship between the parasitaemia during the primary and chronic phases of the infection using an experimental infection approach. We found a significant positive correlation between parasitaemia in the primary peak and the subsequent chronic phase of infection when we experimentally infected great reed warblers (Acrocephalus arundinaceus) with Plasmodium ashfordi. The reason for this association remains to be understood, but might arise from individual variation in exoerythrocytic parasite reservoirs in hosts, parasite antigenic diversity and/or host genetics. Our results suggest that the chronic phase parasitaemia can be used to qualitatively infer the parasitaemia of the preceding and more severe primary phase, which is a very important finding for studies of avian malaria in wild populations.     

Increase in a heat-shock protein from blood cells in response of nestling house martins (Delichon urbica) to parasitism: an experimental approach

Heat-shock proteins (HSPs) are synthesized by animals and plants in response to various stressors. The level of the HSP60 stress protein was measured from the cell fraction of peripheral blood obtained from nestling house martins (Delichon urbica) to test whether ectoparasitism increased the concentration of stress protein. We assessed HSP from nestlings raised in nests previously treated with an insecticide or infested with 50 martin bugs (Oeciacus hirundinis). In addition, haematozoa infections were checked in blood smears. Nestlings from parasite-infested nests, or nestlings infected with trypanosomes, had increased levels of HSP in their blood cells. Nestling growth as determined from wing length was negatively related to HSP60 levels and within-brood variation in wing length increased with increasing levels of the stress protein independently of treatment and infection by trypanosomes. These results suggest HSPs may play a role in host-parasite interactions, and that they can be used reliably for measuring physiological responses to parasites. Received: 4 February 1998 / Accepted: 4 May 1998     

Exploring the adjustment to parasite pressure hypothesis: differences in uropygial gland volume and haemosporidian infection in palearctic and neotropical birds

Parasites are globally widespread pathogenic organisms, which impose important selective forces upon their hosts. Thus, in accordance with the Adjustment to parasite pressure hypothesis, it is expected that defenses among hosts vary relative to the selective pressure imposed by parasites. According to the latitudinal gradient in diversity, species richness and abundance of parasites peak near the equator. The uropygial gland is an important defensive exocrine gland against pathogens in birds. Size of the uropygial gland has been proposed to vary among species of birds because of divergent selection by pathogens on their hosts. Therefore, we should expect that bird species from the tropics should have relatively larger uropygial glands for their body size than species from higher latitudes. However, this hypothesis has not yet been explored. Here, we analyze the size of the uropygial gland of 1719 individual birds belonging to 36 bird species from 3 Neotropical (Peru) and 3 temperate areas (Spain). Relative uropygial gland volume was 12.52% larger in bird species from the tropics than from temperate areas. This finding is consistent with the relative size of this defensive organ being driven by selective pressures imposed by parasites. We also explored the potential role of this gland as a means of avoiding haemosporidian infection, showing that species with large uropygial glands for their body size tend to have lower mean prevalence of haemosporidian infection, regardless of their geographical origin. This result provides additional support for the assumption that secretions from the uropygial gland reduce the likelihood of becoming infected with haemosporidians.