Low intensity blood parasite infections do not reduce the aerobic performance of migratory birds

Blood parasites (Haemosporidia) are thought to impair the flight performance of infected animals, and therefore, infected birds are expected to differ from their non-infected counterparts in migratory capacity. Since haemosporidians invade host erythrocytes, it is commonly assumed that infected individuals will have compromised aerobic capacity, but this has not been examined in free-living birds. We tested if haemosporidian infections affect aerobic performance by examining metabolic rates and exercise endurance in migratory great reed warblers (Acrocephalus arundinaceus) experimentally treated with Plasmodium relictum pGRW04 and in naturally infected wild birds over consecutive life-history stages. We found no effect of acute or chronic infections on resting metabolic rate, maximum metabolic rate or exercise endurance in either experimentally treated or free-living birds. Oxygen consumption rates during rest and while undergoing maximum exercise as well as exercise endurance increased from breeding to migration stages in both infected and non-infected birds. Importantly, phenotypic changes associated with preparation for migration were similarly unaffected by parasitaemia. Consequently, migratory birds experiencing parasitaemia levels typical of chronic infection do not differ in migratory capacity from their uninfected counterparts. Thus, if infected hosts differ from uninfected conspecifics in migration phenology, other mechanisms besides aerobic capacity should be considered

Postglacial Colonisation Patterns and the Role of Isolation and Expansion in Driving Diversification in a Passerine Bird

Pleistocene glacial cycles play a major role in diversification and speciation, although the relative importance of isolation and expansion in driving diversification remains debated. We analysed mitochondrial DNA sequence data from 15 great reed warbler (Acrocephalus arundinaceus) populations distributed over the vast Eurasian breeding range of the species, and revealed unexpected postglacial expansion patterns from two glacial refugia. There were 58 different haplotypes forming two major clades, A and B. Clade A dominated in Western Europe with declining frequencies towards Eastern Europe and the Middle East, but showed a surprising increase in frequency in Western and Central Asia. Clade B dominated in the Middle East, with declining frequencies towards north in Central and Eastern Europe and was absent from Western Europe and Central Asia. A parsimonious explanation for these patterns is independent postglacial expansions from two isolated refugia, and mismatch distribution analyses confirmed this suggestion. Gene flow analyses showed that clade A colonised both Europe and Asia from a refugium in Europe, and that clade B expanded much later and colonised parts of Europe from a refugium in the Middle East. Great reed warblers in the eastern parts of the range have slightly paler plumage than western birds (sometimes treated as separate subspecies; A. a. zarudnyi and A. a. arundinaceus, respectively) and our results suggest that the plumage diversification took place during the easterly expansion of clade A. This supports the postglacial expansion hypothesis proposing that postglacial expansions drive diversification in comparatively short time periods. However, there is no indication of any (strong) reproductive isolation between clades and our data show that the refugia populations became separated during the last glaciation. This is in line with the Pleistocene speciation hypothesis invoking that much longer periods of time in isolation are needed for speciation to occur

Genetic diversity of avian blood parasites in SE Europe: Cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from Bulgaria

We used a nested PCR protocol to examine the genetic diversity of cytochrome b (cyt b) lineages from blood parasites of the genera Plasmodium and Haemoproteus in birds in Bulgaria. In total, 460 birds of 43 species and 14 families (mostly passerines) were examined for the presence of infections. Of them, 267 were recognised as infected with haemosporidian parasites. Mixed infections were recorded in 24 individuals (9%). Besides the 24 individuals with mix infections, 114 (43%) were positive for Plasmodium spp. and 129 (48%) for Haemoproteus spp. We identified 52 genetic lineages of haemosporidian parasites: 38 of Haemoproteus and 14 of Plasmodium. Twelve new cyt b lineages of Haemoproteus were recorded; they occurred in the following hosts: grey-faced woodpecker (Picus canus), golden oriole (Oriolus oriolus), jay (Garrulus glandarius), barred warbler (Sylvia nisoria), song thrush (Turdus philomelos), spotted flycatcher (Muscicapa striata), spanish sparrow (Passer hispaniolensis), hawfinch (Coccothraustes coccothraustes), and cirl bunting (Emberiza cirlus). We also detected 22 new host records for previously known lineages. The most common lineage was SGS1 (Plasmodium relictum), which had a total prevalence of 14% and occurred in 8 host species belonging to 5 families. Three of the cyt b lineages of genus Haemoproteus (DURB1, DURB2 and SYNIS2) showed more than 5% divergence from all described morphologically lineages. These lineages probably represent at least 2 different morphospecies which remains to be identified

Autumn orientation behaviour of paddyfield warblers, Acrocephalus agricola, from a recently expanded breeding range on the western Black Sea coast

The paddyfield warbler, Acrocephalus agricola, has extended its breeding range from Central Asia to the western Black Sea coast. The Balkan population offers a unique chance to test the effect of breeding range expansion on the genetically programmed migratory direction. We studied 21 paddyfield warblers at Durankulak Lake, NE Bulgaria, by recording their autumn migratory orientation in circular orientation cages. Our data show that the preferred migratory orientation is directed along a NE-SW axis. Paddyfield warblers seem to avoid direct crossing of the Black Sea by following the western coast. The mean bearing was parallel to the nearest coastline and corresponds to the direction of the historical breeding range expansion of the species. In our experiment many individuals showed south-western orientation in autumn, a course which would potentially lead the birds to exploratory movements outside the current breeding range. An axial orientation response has been often shown in circular cage tests, and can be due to factors such as coastal orientation or reverse orientation triggered by the physiological condition of some individuals. However, it might also be one of the driving mechanisms for range expansion. Hence, we can expect the future expansion of Balkan paddyfield warblers to continue towards south-west. (c) 2010 Elsevier B.V. All rights reserved

Temporal dynamics of passerine bird migration in the Eastern part of the Balkan Peninsula.

In species that breed and winter in different areas, migration is a key period of the annual cycle with important effects on subsequent events in life. In order to investigate relationships between migration and other events in the annual cycle or environmental factors, we first need to acquire a basic knowledge of the dynamics (pattern and timing) of migration of various species. Our current knowledge of migration dynamics of European passerine birds is based mainly on studies of populations passing via the Western flyway. In contrast, relatively little is known about populations migrating via the Eastern flyway. We examined the seasonal pattern and timing of migration of several abundant passerine species flying across the eastern part of the Balkan Peninsula. We tested whether these were consistent between years within species and also among species within two ecological groups (long- and short-distance migrants). For most species the dynamics of migration were consistent between years. The pattern of migration was consistent among species of long- and of short-distance migrants. The two groups differed in timing of passage in autumn, with long-distance migrants passing significantly earlier than short distance ones

A survey of biting midges of the genus Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) in NE Bulgaria, with respect to transmission of avian haemosporidians

This study presents data from a molecular survey of the species of the genus Culicoides from the region of Kalimok Field Station (NE Bulgaria) and haemosporidian parasites occurring in them in order to investigate the host-parasite specificity of haemosporidians to their dipteran vectors. The identification of Culicoides spp. was carried out by morphological and molecular-genetic methods. We collected and analysed 230 individuals of the genus Culicoides. Nine species were found. Eight species were identified morphologically; Culicoides obsoletus, C. riethi, C. newsteadi, C. circumscriptus, C. festivipennis, C. punctatus, C. pictipennis and C. puncticollis. The ninth species might be classified as either of C. nubeculosus or C. riethi and its identification needs additional investigations. The total prevalence of Haemoproteus in the examined biting midges was 2.17%. Three individuals of C. pictipennis were infected with the Haemoproteus lineage TURDUS2 (prevalence 16.67%), a common parasite of thrushes (Turdidae). Two individuals of C. circumscriptus contained Haemoproteus lineages (prevalence 2.78%); these were the lineage HAWF2 (previously reported from Coccothraustes coccothraustes) and a new lineage CULCIR1 not previously reported in the literature

Degree of associations among vectors of the genus Culicoides (Diptera: Ceratopogonidae) and host bird species with respect to haemosporidian parasites in NE Bulgaria

The occurrence of haemosporidians in biting midges of the genus Culicoides is examined in North-East Bulgaria in order to reveal their potential role for parasite transmission. A PCR-based technique amplifying part of the mitochondrial cytochrome b gene of the parasite is applied on naturally infected biting midges. Totally, 640 parous individuals of four species and 95 blood-fed individuals of six species of Culicoides are examined for the presence of DNA of haemosporidians. Haemosporidian genetic lineages are identified in individuals of three insect species: Culicoides alazanicus (12 lineages, nine lineages of Haemoproteus and three lineages of Plasmodium), Culicoides festivipennis and Culicoides circumscriptus (with two and one lineages of Haemoproteus, respectively). Two genetic lineages of Haemoproteus are recorded in more than one vector species. These results demonstrate variations in the specificity of Haemoproteus genetic lineages to their potential vectors, since some lineages are recorded in a single vector species and others occur in two or more vector species

Mixed haemosporidian infections are associated with higher fearfulness in Yellow Wagtail, Motacilla flava

Blood parasite infections have been shown to influence behavioural traits of their avian hosts, in particular activity level and boldness. Following the hypothesis that a mixed infection by different parasite species should have higher effects than single-species infections, we analysed activity and boldness in wild-caught Yellow Wagtails (Motacilla flava L., 1758), a trans-Saharan migrant, during the energetically demanding spring migration. Eighty-five percent of the birds were naturally infected with Haemoproteus or Plasmodium (Sporozoa, Haemosporida) and 27% of individuals had parasites from both genera. No differences in activity were found among uninfected, single and mixed infection groups. Birds with infections from both genera appeared to be more fearful when first introduced to a cage. These birds also tended to be less likely to approach a novel object compared to uninfected birds and birds infected by a single genus only.The accepted manuscript in pdf format is listed with the files at the bottom of this page. The presentation of the authors' names and (or) special characters in the title of the manuscript may differ slightly between what is listed on this page and what is listed in the pdf file of the accepted manuscript; that in the pdf file of the accepted manuscript is what was submitted by the author

A new approach to evaluate multimodal orientation behaviour of migratory passerine birds recorded in circular orientation cages

Circular orientation cages have been used for several decades to record the migratory orientation of passerine migrants, and have been central to the investigation of the functional characteristics of the biological compasses used for orientation. The use of these cages offers unique possibilities to study the migratory behaviour of songbirds, but suffers from statistical limitations in evaluating the directions of the activity recorded in the cages. The migratory activity has been reported to vary, including complex multimodal orientation of migratory passerines tested in orientation cages irrespective of species studied. The currently applied circular statistical methods fail to describe orientation responses differing from unimodal and axial distributions. We propose for the first time a modelling procedure enabling the analysis of multimodal distributions at either an individual or a group level. In this paper we compare the results of conventional methods and the recommended modelling approach. Migratory routes may be more complex than a simple migratory direction, and multimodal behaviour in migratory species at the individual and population levels can be advantageous. Individuals may select the expected migratory direction, but may also return to safer sites en route, i.e. sites already known, which provide food and/or shelter in reverse directions. In individual birds, several directions may be expressed in the same test hour. At the species level, multimodal orientation may give an opportunity to expand the range or may refer to differential migration route preferences in different populations of birds. A conflicting experimental situation may also result in a different preferential orientation. In this paper we suggest a statistical solution to deal with these types of variations in orientation preference

Molecular characterization of haemosporidian parasites (Haemosporida) in yellow wagtail (Motacilla flava), with description of in vitro ookinetes of Haemoproteus motacillae

In studies of haemosporidian systematics and taxonomy, a combination of microscopic examination and molecular identification has been recommended. The yellow wagtail (Motacilla flava) is a frequently used species in studies of host-parasite interactions; blood parasites of this bird have been well studied using microscopic examination of blood films, but data on molecular characterization of the parasites are scattered. Here we present the first study linking several haemosporidian cyt b sequences with their morphospecies parasitizing the yellow wagtail, combining light microscopy and nested PCR methods. The lineage hYWT1 of Haemoproteus motacillae was the most prevalent parasite; it was recorded in 38% of the birds. The latter lineage and the lineages hYWT2, hYWT3, hYWT5 and hYWT6 form a well-supported clade on the phylogenetic tree and likely represent intraspecific genetic variation of H. motacillae, with genetic divergence of 0.3-1.5 % among these lineages. Microscopic examination of smears prepared during an in vitro experiment, which was designed for observation of developing ookinetes, showed that H. motacillae ookinetes were present 5 hours after exposure of blood to air at 18-20 degrees C. Ookinetes of this parasite belong to a group of large Haemoproteus spp. ookinetes (19.9 mu m in length on average). Illustrations of the parasites are given. Two of reported Plasmodium lineages, pCOLL1 and pYWT4 are phylogenetically closely related to the widespread host generalist parasites Plasmodium relictum (cyt b lineages pSGS1, pGRW4 and pGRW11), but it was not possible to establish this morphologically. This study contributes to the molecular identification of avian haemosporidian parasites and provides information on morphology of H. motacillae ookinetes, which is additional information assisting the microscopic identification of this species