Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone

Character displacement can reduce costly interspecific interactions between young species. We investigated the mechanisms behind divergence in three key traits-breeding habitat choice, timing of breeding, and plumage coloration-in Ficedula flycatchers. We found that male pied flycatchers became expelled from the preferred deciduous habitat into mixed forest as the superior competitor, collared flycatchers, increased in numbers. The peak in food abundance differs between habitats, and the spatial segregation was paralleled by an increased divergence in timing of breeding between the two species. Male pied flycatchers vary from brown to black with brown coloration being more frequent in sympatry with collared flycatchers, a pattern often proposed to result from selection against hybridization, that is, reinforcement. In contrast to this view, we show that brown male pied flycatchers more often hybridize than black males. Male pied flycatcher plumage coloration influenced the territory obtained in areas of co-occurrence with collared flycatchers, and brown male pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition. We suggest that allopatric divergence in resource defense ability causes a feedback loop at secondary contact where male pied flycatchers with the most divergent strategy compared to collared flycatchers are favored by selection.     

Presence of other species may counter seasonal decline in breeding success: a field experiment with pied flycatchers Ficedula hypoleuca

Seasonal decline in breeding success limits fitness in many bird species nesting in the temperate, boreal and arctic zones. Factors affecting this decline, especially if the decline is reduced, can thus have significant ecological and evolutionary importance. In an experiment designed to investigate fitness consequences of heterospecific attraction, no seasonal decline in breeding success was observed for pied flycatchers Ficedula hypoleuca breeding in the presence of resident titmice Parus spp., whereas a pattern of steep decline was observed for birds breeding in areas where residents were removed. Randomisation of removal treatment and pied flycatcher territories with respect to arrival date leaves enhanced foraging that results from the presence of resident titmice during breeding as the best, albeit currently hypothetical, explanation for the observed absence of a seasonal decline. Among terrestrial vertebrates, reports of this kind of direct positive interactions are rare.     

Temporal differences in food abundance promote coexistence between two congeneric passerines

Many related species share the same environment and utilize similar resources. This is surprising because based on the principle of competitive exclusion one would predict that the superior competitor would drive the other species to extinction; coexistence is only predicted if interspecific competition is weaker than intraspecific competition. Interspecific competition is frequently reduced by differential resource use, resulting in habitat segregation. In this paper, we use the closely related collared and pied flycatcher to assess the potential of habitat differences to affect interspecific competition through a different mechanism, namely by generating temporal differences in availability of similar food resources between the two species. We found that the tree species composition of the breeding territories of the two species differed, mainly by a higher abundance of coniferous species around nest-boxes occupied by pied flycatchers. The temporal availability of caterpillars was measured using frass traps under four deciduous and two coniferous tree species. Deciduous tree species showed an early and narrow peak in abundance, which contrasted with the steady increase in caterpillar abundance in the coniferous tree species through the season. We subsequently calculated the predicted total caterpillar biomass available in each flycatcher territory. This differed between the species, with biomass decreasing more slowly in pied flycatcher territories. Caterpillar biomass is strongly correlated with the reproductive success of collared flycatchers, but much less so with pied flycatchers. However, caterpillar availability can only partly explain the differences in seasonal decline of reproductive success between the two species; we discuss additional factors that may contribute to this species difference. Overall, our results are consistent with the suggestion that minor habitat differences between these two species may contribute to promoting their coexistence.     

Combined effects of interspecific competition and hybridization impede local coexistence of Ficedula flycatchers

At secondary contact closely related species may both compete over similar resources and/or hybridize. Simulation models suggest that hybridization increases the risk of extinction beyond the risk resulting from interspecific competition alone, but such combined effects are rarely studied empirically. Here, we use detailed records on pairing patterns, breeding success, local recruitment and immigration collected during 8?years (2002–2009) to investigate the underlying mechanism of the rapid displacement of pied flycatchers by collared flycatchers on the Swedish island of ?land. We found no differences in average reproductive success or reproductive lifespan between the two species. However, we show that young male pied flycatchers failed to establish new territories as the density of male collared flycatchers increased. In addition, as the relative frequency of collared flycatchers increased, the risk of hybridization dramatically increased for female pied flycatchers, which speeds up the exclusion process since there is a high fitness cost associated with hybridization between the two species. In a nearby control area, within the same island, where pied flycatchers breed in the absence of collared flycatchers, no decline in the number of breeding pairs was observed during the same period of time. Our results demonstrate the crucial importance of studying the combined effects of various types of heterospecific interactions to understand and predict the ecological and evolutionary implications of secondary contact between congeneric species. These findings are particularly interesting in the light of recent climate change since the expected range shifts of many taxa will increase competitive and sexual interactions between previously separated species.     

Can environmental fluctuation prevent competitive exclusion in sympatric flycatchers?

Ecology has been characterized by a central controversy for decades: namely, whether the distribution and abundance of organisms are determined by species interactions, such as competitive exclusion, or by environmental conditions. In part, this is because competitive exclusion has not been convincingly demonstrated in open, natural systems. In addition, traditional theoretical models cannot predict the outcome of competitive interactions in the presence of environmental variability. In this paper we document the limiting influence of strong interspecific competition on population dynamics and nestling mortality in a mixed population of pied flycatchers (Ficedula hypoleuca) and collared flycatchers (F. albicollis in a narrow zone of sympatry. Whereas the former species was limited mainly by interspecific competition, the latter species was limited by the concerted influences of intraspecific competition and climate. The analysis suggests a march towards competitive exclusion of the pied flycatcher during warm periods. However, competitive exclusion is apparently prohibited on a local scale because intraspecific competition among individual collared flycatchers intensifies when they are forced to cope with severe environmental conditions, promoting the temporary and local presence of pied flycatchers.     

Competition‐driven build‐up of habitat isolation and selection favoring modified dispersal patterns in a young avian hybrid zone

Competition‐driven evolution of habitat isolation is an important mechanism of ecological speciation but empirical support for this process is often indirect. We examined how an on‐going displacement of pied flycatchers from their preferred breeding habitat by collared flycatchers in a young secondary contact zone is associated with (a) access to an important food resource (caterpillar larvae), (b) immigration of pied flycatchers in relation to habitat quality, and (c) the risk of hybridization in relation to habitat quality. Over the past 12 years, the estimated access to caterpillar larvae biomass in the habitat surrounding the nests of pied flycatchers has decreased by a fifth due to shifted establishment possibilities, especially for immigrants. However, breeding in the high quality habitat has become associated with such a high risk of hybridization for pied flycatchers that overall selection currently favors pied flycatchers that were forced to immigrate into the poorer habitats (despite lower access to preferred food items). Our results show that competition‐driven habitat segregation can lead to fast habitat isolation, which per se caused an opportunity for selection to act in favor of future “voluntarily” altered immigration patterns and possibly strengthened habitat isolation through reinforcement.     

Climate change can alter competitive relationships between resident and migratory birds

Climate change could affect resource competition between resident and migratory bird species by changing the interval between their onsets of breeding or by altering their population densities. We studied interspecific nest-hole competition between resident great tits and migrant pied flycatchers in South-Western Finland over the past five decades (1953-2005). We found that appearance of fatal take-over trials, the cases where a pied flycatcher tried to take over a great tit nest but was killed by the tit, increased with a reduced interspecific laying date interval and with increasing densities of both tits and flycatchers. The probability of pied flycatchers taking over great tit nests increased with the density of pied flycatchers. Laying dates of the great tit and pied flycatcher are affected by the temperatures of different time periods, and divergent changes in these temperatures could consequently modify their competitive interactions. Densities are a result of reproductive success and survival, which can be affected by separate climatic factors in the resident great tit and trans-Saharan migrant pied flycatcher. On these bases we conclude that climate change has a great potential to alter the competitive balance between these two species.     

Fear factor: prey habitat selection and its consequences in a predation risk landscape

Predation risk influences prey use of space. However, little is known about how predation risk influences breeding habitat selection and the fitness consequences of these decisions. The nest sites of central-place foraging predators may spatially anchor predation risk in the landscape. We explored how the spatial dispersion of avian predator nests influenced prey territory location and fitness related measures. We placed 249 nest boxes for migrant pied flycatchers Ficedula hypoleuca , at distances between 10 and 630 m, around seven different sparrowhawk nests Accipiter nisus . After closely monitoring flycatcher nests we found that flycatcher arrival dates, nest box occupation rates and clutch size showed a unimodal relationship with distance from sparrowhawk nests. This relationship suggested an optimal territory location at intermediate distances between 330 and 430 m from sparrowhawk nests. Furthermore, pied flycatcher nestling quantity and quality increased linearly with distance from sparrowhawk nests. These fitness related measures were between 4 and 26% larger in flycatcher nestlings raised far from, relative to those raised nearby, sparrowhawk nests. Our results suggest that breeding sparrowhawk affected both flycatcher habitat selection and reproductive success. We propose that nesting predators create predictable spatial variation in predation risk for both adult prey and possibly their nests, to which prey individuals are able to adaptively respond. Recognising predictable spatial variation in perceived predation risk may be fundamental for a proper understanding of predator-prey interactions and indeed prey species interactions.     

Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone

Parasites may influence the outcome of interspecific competition between closely related host species through lower parasite virulence in the host with which they share the longer evolutionary history. We tested this idea by comparing the prevalence of avian malaria (Haemosporidia) lineages and their association with survival in pied and collared flycatchers (Ficedula hypoleuca and F. albicollis) breeding in a recent contact zone on the Swedish island of Öland. A nested PCR protocol amplifying haemosporidian fragments of mtDNA was used to screen the presence of malaria lineages in 1048 blood samples collected during 6 years. Competitively inferior pied flycatchers had a higher prevalence of blood parasites, including the lineages that were shared between the two flycatcher species. Multistate mark–recapture models revealed a lower survival of infected versus uninfected female pied flycatchers, while no such effects were detected in male pied flycatchers or in collared flycatchers of either sex. Our results show that a comparatively new host, the collared flycatcher, appears to be less susceptible to a local northern European malarial lineage where the collared flycatchers have recently expanded their distribution. Pied flycatchers experience strong reproductive interference from collared flycatchers, and the additional impact of species‐specific blood parasite effects adds to this competitive exclusion. These results support the idea that parasites can strongly influence the outcome of interspecific competition between closely related host species, but that the invading species need not necessarily be more susceptible to local parasites.     

Cross-fostering reveals seasonal changes in the relative fitness of two competing species of flycatchers

Spatial and temporal heterogeneity in relative fitness of competing species is a key factor affecting the structure of communities. However, it is not intuitive why species that are ecologically similar should differ in their response to environmental changes. Here we show that two sympatric flycatchers differ in reproductive strategy and in sensitivity to harsh environment. The fitness of collared flycatchers (Ficedula albicollis), which are dominant in interference competition, is more sensitive than the fitness of pied flycatchers (Ficedula hypoleuca) to the seasonal decline in environmental conditions. In order to control for the possibility that this pattern arises solely from differences in microhabitat use (i.e. a local niche differentiation), we performed a partial cross-fostering experiment of young between the two species (i.e. resulting in nests containing young of both species). Our results show that the growth of nestling pied flycatchers is less influenced by the seasonal decline in environmental conditions. We suggest that a life-history trade-off between interference competitive ability and robustness to harsh environment promotes a regional coexistence of the two species.     

Difference in plasticity of resting metabolic rate – the proximate explanation to different niche breadth in sympatric Ficedula flycatchers

Variation in relative fitness of competing recently formed species across heterogeneous environments promotes coexistence. However, the physiological traits mediating such variation in relative fitness have rarely been identified. Resting metabolic rate (RMR) is tightly associated with life history strategies, thermoregulation, diet use, and inhabited latitude and could therefore moderate differences in fitness responses to fluctuations in local environments, particularly when species have adapted to different climates in allopatry. We work in a long‐term study of collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca) in a recent hybrid zone located on the Swedish island of Öland in the Baltic Sea. Here, we explore whether differences in RMR match changes in relative performance of growing flycatcher nestlings across environmental conditions using an experimental approach. The fitness of pied flycatchers has previously been shown to be less sensitive to the mismatch between the peak in food abundance and nestling growth among late breeders. Here, we find that pied flycatcher nestlings have lower RMR in response to higher ambient temperatures (associated with low food availability). We also find that experimentally relaxed nestling competition is associated with an increased RMR in this species. In contrast, collared flycatcher nestlings did not vary their RMR in response to these environmental factors. Our results suggest that a more flexible nestling RMR in pied flycatchers is responsible for the better adaptation of pied flycatchers to the typical seasonal changes in food availability experienced in this hybrid zone. Generally, subtle physiological differences that have evolved when species were in allopatry may play an important role to patterns of competition, coexistence, or displacements between closely related species in secondary contact.     

Mechanisms and fitness effects of interspecific information use between migrant and resident birds

Interactions with potential competitors are an important componentof habitat quality. Due to the costs of coexistence with competitors,a breeding habitat selection strategy that avoids competitorsis expected to be favored. However, many migratory birds appearto gain benefits from an attraction to the presence of residentbirds, even though residents are assumed to be competitivelydominant. Thus far the mechanisms of this habitat selectionprocess, heterospecific attraction, are unknown, and the consequencesfor resident birds of migrant attraction remain untested. Throughheterospecific attraction, migrants may gain benefits if thedensity or territory location of residents positively reflectshabitat quality, and/or they gain benefits through increasedfrequency of social interactions with residents in foragingor predator detection. In this experiment, we examined the reciprocaleffects of spatial proximity on fitness-related traits in migrantpied flycatcher (Ficedula hypoleuca) and resident great tit(Parus major) by experimentally forcing them to breed eitheralone or in close proximity to each other. Surprisingly, greattits bore all the costs of coexistence while flycatchers wereunaffected, even gaining slight benefits. In concert with anearlier study, these results suggest that flycatchers use titsas information about good-quality nest-site locations whilebenefits from social interactions with tits are possible butless important. We suggest that utilizing interspecific socialinformation may be a common phenomenon between species sharingsimilar resource needs. Our results imply that the effects ofinterspecific information use can be asymmetric and may thereforehave implications for the patterns and consequences of speciescoexistence.     

Experimental evidence for the use of density based interspecific social information in forest birds

Reproductive success and habitat preference are generally assumed to be negatively associated with densities of con- and heterospecific competitors. However, recent theoretical studies have suggested that in some cases habitat preference may have a nonlinear unimodal function in relation to con- or heterospecific competitor densities – intermediate densities being preferred. Such a pattern is expected if con- or heterospecific densities are used as a proximate cue in habitat selection, which may produce benefits by reducing searching costs and providing information about current habitat quality and costs of competition. At low density the use of such cues, and hence habitat selection, are hampered, whereas at high density costs of competition exceed the benefits of using cues, leading to avoidance. Here, we tested this hypothesis by examining whether arboreal migratory birds use the density of resident titmice ( Parus spp.) in habitat selection decisions. Many migrants and titmice species share similar resource needs making titmice density a reliable source of information for migrants. At the scale of habitat patches, we experimentally created a range of titmice densities from low to very high and subsequently measured the density response of migrants. In contrast to the unimodal habitat preference hypothesis, the average species number and total density of migratory birds were positively and linearly correlated with manipulated titmice density. Thus, migrants probably use titmice density as a relative indicator of habitat quality (abundance or quality of food) because foliage gleaners that share similar food resource with titmice, but not ground foragers, showed a positive association with manipulated titmice density. These results emphasize the positive effect of interspecific social information on habitat choice decisions and diversity of migratory bird community.     

Reproductive character displacement of female,but not male song discrimination in an avian hybrid zone

Divergence of male sexual signals and female preferences for those signals often maintains reproductive boundaries between closely related, co‐occurring species. However, contrasting sources of selection, such as interspecific competition, can lead to weak divergence or even convergence of sexual signals in sympatry. When signals converge, assortative mating can be maintained if the mating preferences of females diverge in sympatry (reproductive character displacement; RCD), but there are few explicit examples. Pied flycatchers (Ficedula hypoleuca) are sympatric with collared flycatchers (F. albicollis) on the Baltic island of Öland, where males from both species compete over nestboxes, their songs converge, and the two species occasionally hybridize. We compare song discrimination of male and female pied flycatchers on Öland and in an allopatric population on the Swedish mainland. Using field choice trials, we show that male pied flycatchers respond similarly to the songs of both species in sympatry and allopatry, while female pied flycatchers express stronger discrimination against heterospecific songs in sympatry than in allopatry. These results are consistent with RCD of song discrimination of female pied flycatchers where they co‐occur with collared flycatchers, which should maintain species assortative mating despite convergence of male sexual signals.     

Climate change and fitness components of a migratory bird breeding in the Mediterranean region

The increase in spring temperatures in temperate regions over the last two decades has led to an advancing spring phenology, and most resident birds have responded to it by advancing their onset of breeding. The pied flycatcher (Ficedula hypoleuca) is a long‐distance migrant bird with a relatively late onset of breeding with respect to both resident birds and spring phenology in Europe. In the present correlational study, we show that some fitness components of pied flycatchers are suffering from climate change in two of the southernmost European breeding populations. In both montane study areas, temperature during May increased between 1980 and 2000 and an advancement of oak leafing was detected by using the normalized difference vegetation index (NDVI) to assess tree phenology. This might result in an advancement of the peak in availability of caterpillars, the main prey during the nestling stage. Over the past 18 yr, the time of egg laying and clutch size of pied flycatchers were not affected by the increase in spring temperatures in these Mediterranean populations. However, this increase seems to have an adverse effect on the reproductive output of pied flycatchers over the same period. Our data suggest that the mismatch between the timing of peak food supply and nestling demand caused by recent climate change might result in a reduction of parental energy expenditure that is reflected in a reduction of nestling growth and survival of fledged young in our study populations. The data seem to indicate that the breeding season has not shifted and it is the environment that has shifted away from the timing of the pied flycatcher breeding season. Mediterranean pied flycatchers were not able to advance their onset of breeding, probably, because they are constrained by their late arrival date and their restricted high altitude breeding habitat selection near the southern border of their range.     

Direct benefits and costs for hybridizing Ficedula flycatchers

It is well understood that females may gain direct benefits from breeding with attractive males. However, the direct fitness effects of mate-choice are rarely considered with respect to mating between different species (hybridization), a field dominated by discussion of indirect costs of producing unfit hybrid offspring. Hybridizing females may also gain by the types of direct benefits that are important for intraspecific mate choice, and in addition may have access to certain benefits that are restricted to mating with males of an ecologically diverged sister-taxon. We investigate possible direct benefits and costs female Ficedula flycatchers gain from breeding with a heterospecific male, and demonstrate that hybridizing female collared flycatchers (F. albicollis) breed in territories that do not suffer the seasonal decline in habitat quality experienced by females breeding with conspecifics. We exclude the hypotheses that heterospecific males provide alternative food-types or assume a greater amount of the parental workload. In fact, the diets of the two species (F. albicollis and F. hypoleuca) were highly similar, suggesting possible interspecific competition over food resources in sympatry. We discuss the implications of direct fitness effects of hybridization, and why there has been such a disparity in the attention paid to such benefits and costs with regard to intraspecific and interspecific mate-choice.     

Large-scale effect of climate change on breeding parameters of pied flycatchers in Western Europe

Variations in laying date and clutch size of pied flycatchers Ficedula hypoleuca across populations throughout western Europe are examined in relation to climatic fluctuations, measured by the winter North Atlantic Oscillation (NAO) index. Across breeding sites, the winter-NAO index affected laying date such that females lay earlier after warmer and moister winters (positive values of winter NAO-index). Female pied flycatchers breed progressively earlier because presumably the whole breeding season is being shifted, as a direct result of the positive values of winter NAO-index. Moreover, clutch size of pied flycatchers across populations was negatively related to winter NAO-index during the last 50 yr. These analyses controlled for potentially confounding variables such as latitude, longitude, elevation and habitat of each study site. The present study conclude that pied flycatchers across western Europe are breeding earlier and laying smaller clutch sizes and that the most likely cause is a long-term increase in spring temperature. On the other hand, this study shows that climate change may not act uniformly between breeding populations in Western Europe. From those results, this study concludes that northern pied flycatcher populations are more sensitive to climate change than southern populations breeding in montane habitats.     

Direct interference or indirect exploitation? An experimental study of fitness costs of interspecific competition in voles

Studies on competing mammalian species in the past have focused mainly on the competitive exclusion of one species from the preferred habitat of the other. Investigations on effects of competition and coexistence on individual fitness are rare . In this study we were able to measure effects of interspecific competition on major fitness components, using a system with two vole species in asymmetric competition. Survival, reproduction and space use of bank vole Clethrionomys glareolus females were monitored in 32 enclosed populations over four replicates of eight parallel run enclosures. Into half of the enclosures we introduced an additional number of field voles Microtus agrestis , a dominant competitor.
Survival of bank vole females was lower under competitive conditions. Total number of breeding females was lower in populations coexisting with competitors. Territory size of bank vole females decreased. Females body weight and litter size bank vole litters conceived during the experiment were not affected by interspecific competition. These characteristics should respond to differences in food resources, and territory size should increase if food was scarce, thus we found no indication of direct exploitation competition between the two species. Space use was overlapping between the species, but individuals of both species were never caught together in the same trap, indicating avoidance behaviour.
We conclude that adult bank vole females do suffer fitness consequences through interference competition with field voles, probably basing on increased number of aggressive encounters in the presence of the dominant species. Our results suggest, that direct interference rather than indirect exploitation competition may be the cause for observed fitness decrease in bank vole females.     

Relative performance of hybrid nestlings in Ficedula flycatchers: a translocation experiment

Ecological speciation predicts that hybrids should experience relatively low fitness in the local environments of their parental species. In this study, we performed a translocation experiment of nestling hybrids between collared and pied flycatchers into the nests of conspecific pairs of their parental species. Our aim was to compare the performance of hybrids with purebred nestlings. Nestling collared flycatchers are known to beg and grow faster than nestling pied flycatchers under favorable conditions, but to experience higher mortality than nestling pied flycatchers under food limitation. The experiment was performed relatively late in the breeding season when food is limited. If hybrid nestlings have an intermediate growth potential and begging intensity, we expected them to beg and grow faster, but also to experience lower survival than pied flycatchers. In comparison with nestling collared flycatchers, we expected them to beg and grow slower, but to survive better. We found that nestling collared flycatchers indeed begged significantly faster and experienced higher mortality than nestling hybrids. Moreover, nestling hybrids had higher weight and tended to beg faster than nestling pied flycatchers, but we did not detect a difference in survival between the latter two groups of nestlings. We conclude that hybrid Ficedula nestlings appear to have a better intrinsic adaptation to food limitation late in the breeding season compared with nestling collared flycatchers. We discuss possible implications for gene flow between the two species.     

Differential response to abiotic conditions and predation risk rather than competition avoidance determine breeding site selection by anurans

Co‐existence of species has been a central debate in ecology for decades but the mechanisms that allow co‐existence are still heatedly disputed. The main paradigms have shifted among the importance of competition, predation and abiotic conditions as determinants of community structure. Differential habitat selection is considered to reduce competition and hence allow co‐existence. Our goal was to test hypotheses regarding how breeding site use of a population that was patchily distributed on a dynamic floodplain may facilitate coexistence: 1) do species co‐occur randomly or do they occur more or less often than expected by chance? 2) Do species use the same habitat types in equal proportions or do they use them differentially? 3) If they use habitat types differentially, is this differential use related to abiotic and biotic conditions? 4) Does interspecific competition predict breeding site use or do abiotic conditions and predation risk better predict habitat use? We collected presence/absence (i.e. detection/nondetection) data of egg clutches and larvae of four pond‐breeding anuran species during a two year study at a total of 353 ponds. We used site occupancy models and model averaging techniques to predict breeding site selection in relation to habitat types, abiotic and biotic factors. These parameters were corrected for imperfect detection of species. The rates of co‐occurrence were consistently higher than expected by chance. Species differed in the use of the main habitat types. Habitat types that were used by multiple species were used in a species‐specific manner in relation to both abiotic conditions and predation risk. Species preferred ponds where other species and fish were present. Although niche differentiation in breeding site selection is evident, our results do not support the pervasive role of competition avoidance in governing current breeding site selection. We conclude that differential habitat use and differences in response to abiotic conditions and predation risk can override competitive interactions, thereby facilitating local co‐existence and high species diversity.