Urbanisation and avian fitness: an investigation of avian malaria prevalence and feather corticosterone level of blue tit Cyanistes caeruleus nestlings across two breeding seasons

Albalawi, Bedur Faleh A. (2020) Urbanisation and avian fitness: an investigation of avian malaria prevalence and feather corticosterone level of blue tit Cyanistes caeruleus nestlings across two breeding seasons. PhD thesis, University of Glasgow.

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Urbanised landscapes vary significantly from natural habitats because of their different and unique ecological features. These features can affect the ability of both animals and plants to occupy urban habitats. Ecological studies on avian species have often reported a reduction in several breeding parameters of urban populations compared to their rural counterparts. However, how the urban environment can influence the breeding success of these species remains largely unknown. One hypothesis is that urban-specific factors alter key physiological traits modulated by stress hormone levels in birds. Indeed, long-term exposure to high levels of stress can lead to sustained elevation of basal glucocorticoid levels and consequent detrimental effects, such as impaired immunity, inhibited growth and reduced survival. For instance, alterations to the microclimate, pollution, and limitations of food resources may act as strong stressors, resulting in an increased likelihood of parasite infection and related fitness costs, affecting the capacity of hosts to occupy urban areas.
Environmental conditions can fluctuate from year to year, affecting birds directly or indirectly by limiting food availability, especially for carnivorous birds of which the main food (insects, e.g. caterpillars) is highly dependent on weather conditions. As the urban conditions are already harsh, fluctuations in the other environmental factors, like weather conditions, have the potential to severely affect urban birds. Conversely, the more favourable conditions in rural habitats may allow the birds to buffer against other potentially negative environmental factors. Therefore, in order to understand the impact of urbanization on bird stress and fitness across fluctuating environmental conditions, the first aim of my thesis was to explore and compare the fitness of an urban and a rural population of blue tit Cyanistes caeruleus across two breeding seasons (2016 and 2017) in relation to the stress levels they experience. Previous studies have suggested the use of corticosterone (CORT, the main avian glucocorticoid) levels as a biomarker of stress experienced by animals. In birds, long term or chronic exposure to stressors can be measured from feather corticosterone (fCORT). This non-invasive method can measure the level of CORT that has been metabolised and deposited in feathers during feather growth. Thus, I compared two populations of blue tits in relation to the level of stress experienced by nestlings, throughout their first thirteen days of life, that may influence their fitness in urban and rural habitats. CORT levels in nestlings can also be directly influenced by parents before oviposition (e.g. by maternal deposition of CORT in yolk). Therefore, I also tested the role of origin of the bird on their fCORT levels, experimentally, to assess whether the pre-oviposition environment has a role in nestling’s fitness (Chapter 2). Then, as parasite infections can play a major role in fitness differences between urban and rural birds, I decided to measure the prevalence of avian malaria (haemosporidian parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon), which are widespread parasites in birds, infecting blood cells. Specifically, I compared avian malaria prevalence in nestlings from the two populations across the two breeding seasons, as well as tested the role of parental origin (based on a cross-fostering experiment) on their susceptibility to infection (Chapter 4). However, to detect haemosporidian parasite acute infection and identify the parasite genera in the studied blue tit populations, I developed a new molecular method, as current tools did not allow these investigations (Chapter 3). Using this new approach, I explored my next aim, where I tested the effect of Leucocytozoon infection prevalence on fitness-related traits (body weight and survival) of nestling blue tits from the two populations during the two breeding seasons. I also tested the potential synergistic impact of infection and urban-related stress on blue tit fitness by examining the relationship between the two factors – fCORT level and Leucocytozoon infection prevalence (Chapter 5). I accomplished these aims using both experimental and correlational approaches, the former involving a cross-fostering experiment and a vector-manipulation experiment. In 2016, I cross-fostered some clutches between and within sites to test for any effects that may be derived from inherited or maternal traits from parents to their offspring. Additionally, as both populations showed high malaria prevalence in 2016, in the 2017 breeding season, I conducted a vector-repellent experiment to experimentally reduce infections in nestlings; this was done with the goal of better understanding the impact of parasites on bird’s fitness.
The key findings of my thesis are as follows: First, monitoring the two populations of blue tit over two breeding seasons revealed that most breeding parameters are significantly different between the urban and rural blue tits. In both seasons, urban birds showed a significantly lower clutch size, hatching and fledging success compared to the rural ones. Additionally, fledging success at both sites was considerably lower in one breeding season (2017), during which nestling body weight was significantly lower in urban than rural birds; however, in 2016, when fledging success was higher, the two populations barely differed in their weight. Second, mirroring nestling body weight, during the 2017 breeding season, fCORT levels in nestlings were significantly higher in the urban nestlings compared to their rural counterparts, but not in 2016, further suggesting that 2017 was a more challenging year. However, I found no association between the reduction in fitness-related traits (body weight and fledging success) and fCORT. This lack of association between fCORT levels and nestlings’ fitness-related traits could have been missed as I pooled the feather samples per nest and did not measure individual nestlings for fCORT level, thus losing the inter-individual variation in fCORT levels that could be associated with fitness-related traits. Third, mirroring the fCORT variations, Leucocytozoon parasite infections varied in the two populations across seasons, showing that urban populations had lower or higher prevalence compared to rural birds depending on the year (2016 and 2017, respectively). I found a strong association between infection with Leucocytozoon prevalence and lower weight of urban nestlings just before fledging (day 13 of age) as well as a reduction in urban nestling survival, which instead was not observed in rural birds. I found no association between infection prevalence and fCORT level, measured per nest, not individuals. Finally, experimentally tested in the field, the origin of the bird did not influence the infection susceptibility to Leucocytozoon, nor did it influence fCORT levels.
In summary, my thesis highlighted the importance of year to year variation between the two populations (i.e. the urban and the rural populations of blue tits), that could be influenced by fluctuating environmental factors such as weather and food availability. Urban and rural populations that show similarities in certain traits during one year of study may be different during another year (e.g. fCORT level and body weight). Prevalence of vector-borne pathogens like Leucocytozoon parasites in a given population may also differ between populations, which can vary from year to year. The extent of the fitness effect of parasite infection also depends on various factors fluctuating from one year to another. This emphasises the need for longitudinal studies monitoring individuals and populations over multiple years and across a wide range of habitats that differ in quality and features.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Keywords: Blue tit, Cyanistes caeruleus, stress, urban, corticosterone, feather, maternal effect, avian malaria.
Subjects: Q Science > QH Natural history > QH301 Biology
Q Science > QH Natural history > QH426 Genetics
Q Science > QL Zoology
Colleges/Schools: College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
Supervisor's Name: Baldini, Dr. Francesco
Date of Award: 2020
Depositing User: Mrs Bedur Albalawi
Unique ID: glathesis:2020-79043
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 11 Mar 2020 16:30
Last Modified: 11 Mar 2020 16:32
URI: http://theses.gla.ac.uk/id/eprint/79043

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