A mechanistic approach to understanding the colour polymorphism in black sparrowhawks (Accipiter melanoleucus)

Species that exhibit large variation in phenotypic traits, are commonly considered to have a stronger evolutionary potential. However, how they are capable to maintain polymorphisms remains a fundamental problem in evolutionary biology. Colour polymorphic species provide ideal study systems to explore the processes that lead to variation maintenance. About 3.5% of all bird species are colour polymorphic, but it is an especially common phenomenon in Accipitridae (22%), which indicates that it has an adaptive function in this bird group and makes them ideal model systems to study evolutionary processes. The black sparrowhawk (Accipiter melanoleucus) occurs in two discrete colour variants: dark and light. The two morphs differ in the expression of white and black feathers on the breast, belly and underwing coverts. The morph has been associated with ambient light-dependent foraging success and activity behaviour: Dark morphs forage more and have higher foraging success under low light conditions whereas light morphs forage independently of light levels but are better foragers under bright light conditions. This is hypothesized to be due to a crypsis advantage for the morphs under these conditions. During the winter breeding period, the predominating low light conditions on the Cape Peninsula (Western Cape, South Africa) could create an advantage for dark morphs, which should result in their higher survival and higher breeding success. However, this is not the case and only when the two morphs come together to breed, there is a fitness difference: mixed-morph pairs (that consist of a dark and a light morph) have higher breeding success than like-morph pairs (that consist of the same morph) and offspring of mixed-morphs have higher survival rates. This higher success of mixed-morph pairs is hypothesized to be due to emergent pair-level properties with the two morphs being able to expand the hunting niche as a pair. This ‘complementarity hypothesis' is based on previous research conducted on the study system. The aim of this PhD was to explore the mechanistic background of colour polymorphism maintenance in the black sparrowhawk. (i) I performed an experiment in which I test whether there is a morph- and ambient light-dependent crypsis advantage in the black sparrowhawk. I measure the reaction time of feral pigeons towards a simulated hawk attack but did not find indication of such an effect as pigeons reacted the same towards the two morphs. In line with the complementarity hypothesis, (ii) I found that mixed-morph parents provide food more consistently to the nest than like-morph parents. This results in a more predictable food supply for nestlings and buffers against long periods of malnourishment. However, (iii) I was unable to determine the mechanistic link between food supply and higher survival: nestlings of mixedand like-morph pairs had the same levels of innate immune function. Thus, an improved innate immune function in nestlings of mixed-morph pairs is unlikely associated with their higher survival rates. (iv) I performed individual-based model simulations which incorporate multiple key fitness parameters and found that complementarity – in combination with morphdependent seasonality-associated fitness effects – explains the stable colour morph equilibrium in this population. I conclude that emergent pair-level properties which arise due to the complementary nature of the two morphs play an important role in maintaining polymorphism in this species. Complementarity might not only be restricted to colour polymorphic species but could be present in other polymorphic traits that allow parents to behaviourally complement each other when raising their young

Parental morph combination does not influence innate immune function in nestlings of a colour-polymorphic African raptor

Conditions experienced during early life can have long-term individual consequences by influencing dispersal, survival, recruitment and productivity. Resource allocation during development can have strong carry-over effects onto these key parameters and is directly determined by the quality of parental care. In the black sparrowhawk (Accipiter melanoleucus), a colour-polymorphic raptor, parental morphs influence nestling somatic growth and survival, with pairs consisting of different colour morphs ('mixed-morph pairs') producing offspring with lower body mass indices, but higher local apparent survival rates. Resource allocation theory could explain this relationship, with nestlings of mixed-morph pairs trading off a more effective innate immune system against somatic growth. We quantified several innate immune parameters of nestlings (hemagglutination, hemolysis, bacteria-killing capacity and haptoglobin concentration) and triggered an immune response by injecting lipopolysaccharides. Although we found that nestlings with lower body mass index had higher local survival rates, we found no support for the proposed hypothesis: neither baseline immune function nor the induced immune response of nestlings was associated with parental morph combination. Our results suggest that these immune parameters are unlikely to be involved in providing a selective advantage for the different colour morphs' offspring, and thus innate immunity does not appear to be traded off against a greater allocation of resources to somatic growth. Alternative hypotheses explaining the mechanism of a low nestling body mass index leading to subsequent higher local survival could be related to the post-fledgling dependency period or differences in dispersal patterns for the offspring from different morph combinations

Innate immune function and antioxidant capacity of nestlings of an African raptor covary with the level of urbanisation around breeding territories

Urban areas provide breeding habitats for many species. However, animals raised in urban environments face challenges such as altered food availability and quality, pollution and pathogen assemblages. These challenges can affect physiological processes such as immune function and antioxidant defences which are important for fitness. Here, we explore how levels of urbanisation influence innate immune function, immune response to a mimicked bacterial infection and antioxidant capacity of nestling Black Sparrowhawks Accipiter melanoleucus in South Africa. We also explore the effect of timing of breeding and rainfall on physiology since both can influence the environmental condition under which nestlings are raised. Finally, because urbanisation can influence immune function indirectly, we use path analyses to explore direct and indirect associations between urbanisation, immune function and oxidative stress. We obtained measures of innate immunity (haptoglobin, lysis, agglutination, bactericidal capacity), indices of antioxidant capacity (total non-enzymatic antioxidant capacity (tAOX) and total glutathione from nestlings from 2015 to 2019. In addition, in 2018 and 2019, we mimicked a bacterial infection by injecting nestlings with lipopolysaccharide and quantified their immune response. Increased urban cover was associated with an increase in lysis and a decrease in tAOX, but not with any of the other physiological parameters. Furthermore, except for agglutination, no physiological parameters were associated with the timing of breeding. Lysis and bactericidal capacity, however, varied consistently with the annual rainfall pattern. Immune response to a mimicked a bacterial infection decreased with urban cover but not with the timing of breeding nor rainfall. Our path analyses suggested indirect associations between urban cover and some immune indices via tAOX but not via the timing of breeding. Our results show that early-life development in an urban environment is associated with variation in immune and antioxidant functions. The direct association between urbanisation and antioxidant capacity and their impact on immune function is likely an important factor mediating the impact of urbanisation on urban-dwelling animals. Future studies should explore how these results are linked to fitness and whether the responses are adaptive for urban-dwelling species

Reduced ectoparasite load, body mass and blood haemolysis in Eurasian kestrels (Falco tinnunculus) along an urban-rural gradient

Urbanisation is proceeding at an alarming rate which forces wildlife to either retreat from urban areas or cope with novel stressors linked to human presence and activities. For example, urban stressors like anthropogenic noise, artificial light at night and chemical pollution can have severe impacts on the physiology of wildlife (and humans), in particular the immune system and antioxidant defences. These physiological systems are important to combat and reduce the severity of parasitic infections, which are common among wild animals. One question that then arises is whether urban-dwelling animals, whose immune and antioxidant system are already challenged by the urban stressors, are more susceptible to parasitic infections. To assess this, we studied nestlings of Eurasian kestrels (Falco tinnunculus) in Vienna, Austria, during 2015 and 2017. We measured biomarkers of innate immune function, oxidative stress and body mass index and ectoparasite infection intensity in 143 nestlings (from 56 nests) along an urban gradient. Nestlings in more urbanised areas had overall fewer ectoparasites, lower haemolysis (complement activity) and lower body mass index compared to nestlings in less urbanised areas. None of the other immune or oxidative stress markers were associated with the urban gradient. Despite some non-significant results, our data still suggest that kestrel nestlings experience some level of reduced physiological health, perhaps as a consequence of exposure to more urban stressors or altered prey availability in inner-city districts even though they had an overall lower ectoparasite burden in these heavily urbanised areas.</p

Parental morph combination does not influence innate immune function in nestlings of a colour-polymorphic African raptor

Conditions experienced during early life can have long-term individual consequences by influencing dispersal, survival, recruitment and productivity. Resource allocation during development can have strong carry-over effects onto these key parameters and is directly determined by the quality of parental care. In the black sparrowhawk (Accipiter melanoleucus), a colour-polymorphic raptor, parental morphs influence nestling somatic growth and survival, with pairs consisting of different colour morphs (‘mixed-morph pairs’) producing offspring with lower body mass indices, but higher local apparent survival rates. Resource allocation theory could explain this relationship, with nestlings of mixed-morph pairs trading off a more effective innate immune system against somatic growth. We quantified several innate immune parameters of nestlings (hemagglutination, hemolysis, bacteria-killing capacity and haptoglobin concentration) and triggered an immune response by injecting lipopolysaccharides. Although we found that nestlings with lower body mass index had higher local survival rates, we found no support for the proposed hypothesis: neither baseline immune function nor the induced immune response of nestlings was associated with parental morph combination. Our results suggest that these immune parameters are unlikely to be involved in providing a selective advantage for the different colour morphs’ offspring, and thus innate immunity does not appear to be traded off against a greater allocation of resources to somatic growth. Alternative hypotheses explaining the mechanism of a low nestling body mass index leading to subsequent higher local survival could be related to the post-fledgling dependency period or differences in dispersal patterns for the offspring from different morph combinations

Large-scale genotypic identification reveals density-dependent natal dispersal patterns in an elusive bird of prey

Abstract Background Natal dispersal, the distance between site of birth and site of first breeding, has a fundamental role in population dynamics and species’ responses to environmental changes. Population density is considered a key driver of natal dispersal. However, few studies have been able to examine densities at both the natal and the settlement site, which is critical for understanding the role of density in dispersal. Additionally, the role of density on natal dispersal remains poorly understood in long-lived and slowly reproducing species, due to their prolonged dispersal periods and often elusive nature. We studied the natal dispersal of the white-tailed eagle (Haliaeetus albicilla) in response to local breeder densities. We investigated the effects of the number of active territories around the natal site on (a) natal dispersal distance and (b) the difference between natal and settlement site breeder density. We were interested in whether eagles showed tendencies of conspecific attraction (positive density-dependence) or intraspecific competition (negative density-dependence) and how this related to settlement site breeder density. Methods We used a combination of long-term visual and genotypic identification to match individuals from their breeding site to their natal nest. We identified natal dispersal events for 355 individuals hatched between 1984 and 2015 in the Baltic Sea coast and Arctic areas of Finland. Of those, 251 were identified by their genotype. Results Individuals born in high-density areas dispersed shorter distances than those born in low-density areas, but settled at lower density breeding sites in comparison to their natal site. Eagles born in low natal area densities dispersed farther but settled in higher density breeding sites compared to their natal site. Conclusions We show that eagles might be attracted by conspecifics (positive density-dependence) to identify high-quality habitats or find mates, but do not settle in the most densely populated areas. This indicates that natal dispersal is affected by an interplay of conspecific attraction and intraspecific competition, which has implications for population dynamics of white-tailed eagles, but also other top predators. Furthermore, our study demonstrates the value of long-term collection of both nestling and (non-invasive) adult DNA samples, and thereafter using genotype matching to identify individuals in long-lived and elusive species

Early-life diet specificity is associated with long-lasting differences in apparent survival in a generalist predator

Peer reviewe

Reduced ectoparasite load, body mass and blood haemolysis in Eurasian kestrels (Falco tinnunculus) along an urban–rural gradient

Urbanisation is proceeding at an alarming rate which forces wildlife to either retreat from urban areas or cope with novel stressors linked to human presence and activities. For example, urban stressors like anthropogenic noise, artificial light at night and chemical pollution can have severe impacts on the physiology of wildlife (and humans), in particular the immune system and antioxidant defences. These physiological systems are important to combat and reduce the severity of parasitic infections, which are common among wild animals. One question that then arises is whether urban-dwelling animals, whose immune and antioxidant system are already challenged by the urban stressors, are more susceptible to parasitic infections. To assess this, we studied nestlings of Eurasian kestrels (Falco tinnunculus) in Vienna, Austria, during 2015 and 2017. We measured biomarkers of innate immune function, oxidative stress and body mass index and ectoparasite infection intensity in 143 nestlings (from 56 nests) along an urban gradient. Nestlings in more urbanised areas had overall fewer ectoparasites, lower haemolysis (complement activity) and lower body mass index compared to nestlings in less urbanised areas. None of the other immune or oxidative stress markers were associated with the urban gradient. Despite some non-significant results, our data still suggest that kestrel nestlings experience some level of reduced physiological health, perhaps as a consequence of exposure to more urban stressors or altered prey availability in inner-city districts even though they had an overall lower ectoparasite burden in these heavily urbanised areas

Contrasting parental color-morphs increase regularity of prey deliveries in an African raptor: Data

The paper based on this dataset has been published in Behavioral Ecology with the title "Contrasting parental color-morphs increase regularity of prey deliveries in an African raptor"Abstract: Disassortative mating in color-polymorphic raptors is a proposed mechanism for the maintenance of color polymorphism in populations. Selection for such a mating system may occur if there are fitness advantages of mating with a contrasting morph. In the black sparrowhawk (Accipiter melanoleucus), mixed-morph pairs may have a selective advantage, since they produce offspring which have higher survival rates. Two hypotheses, which may explain the mechanism, are the 'avoidance-image' and 'complementarity' hypotheses: The first suggests that within a predator's territory, prey develop a search-image for the more commonly encountered parental morph, for example, the male morph during incubation and brooding. Females of a contrasting morph to their partner would then have higher capture rates once they commence hunting in the later nestling phase. Thus, the avoidance-image hypothesis predicts higher provisioning rates for mixed-morph pairs. Alternatively, the 'complementarity' hypothesis posits that different color morphs exploit different environmental conditions, allowing mixed-morph pairs to hunt under a wider range of conditions and predicts that food is delivered more consistently. We test these hypotheses using nest cameras to record prey delivery rates during the late nestling phase when both parents are foraging. We found support for the 'complementarity' hypothesis, with mixed-morph pairs delivering food more consistently, but not at a higher rate. The higher consistency in prey deliveries may explain the improved survival of the offspring of mixed-morph pairs, and therefore play a role in maintaining the stability of color-polymorphism in this system.</div

Data: Large-scale genotypic identification reveals density-dependent natal dispersal patterns in an elusive bird of prey

This data is produced for white-tailed eagle population study at the University of Turku, Finland, to study density-dependence in natal dispersal. Data consists of 285 white-tailed eagle individuals in Finland. For each individual the natal dispersal distance and local breeder density (number of active territories) within 10 km and 30 km buffer is included. </p