The effects of urbanization on physiological indicators of welfare in bats

Overview

One of the major challenges facing biodiversity in our changing world is modifications in land use from a rapidly increasing human population (Grimm et al. 2008). Several studies have documented the impacts of urbanization on wildlife due to habitat loss and fragmentation, chemical, light and noise pollution, direct disturbance, harvesting, predation from cats and dogs, and road mortality (Russo & Ancillotto 2015). While some aspects of urbanization have direct detrimental effects on wildlife, others are less clear cut. For example, the heat generated by urban environments might benefit some wildlife, but be detrimental to others at certain times of the year (e.g. hibernating species in winter).

Bats are both one of the most diverse mammalian groups represented in urban environments (Jung & Threlfall 2016) but also one of the most threatened groups in Europe (Jones et al. 2009). Urban and rural roost sites are likely to differ in quality on the basis of chemical, noise and light pollution, temperature and thermal variability, disturbance and access to food and water. Some bat species are relatively common in urban areas (e.g. Pipistrellus pipistrellus in Europe), and have been described as ‘urban-adaptors’. However, recent work has indicated that the activity of even these species decreases with increasingly urbanized landscapes (Lintott et al. 2016). The mechanism for this is unclear; most work on bat responses to urbanization has focused on foraging and roosting patterns with little information on physiological effects.

This studentship will use a number of novel and relatively non-invasive welfare indicators to assess levels of physiological stress in wild bats living in urban and rural environments. Glucocorticoids are commonly used indicators of baseline stress levels, and are generally assayed from blood. However, non-invasive faecal glucocorticoid measurements have recently been validated to assess chronic stress in a bat (Eptesicus isabellinus; Kelm et al. 2016). Glucocorticoids can also be extracted from hair, providing a hormone profile that tracks the period of hair growth. This will be carried out in bats for the first time in this project. The microbial community inhabiting the gut, which has recently been assayed in a bat for the first time (the lesser horseshoe bat, Rhinolophus monoceros; Selvin et al. 2019), holds potential as an indicator of gut and wider health and welfare.

The aim of this project is to investigate the effects of urbanization on physiological indicators of welfare in bats. Key objectives include:
• Validating novel physiological indicators of welfare in bats
• Testing for variation in glucocorticoid levels along a gradient of increasing urbanization
• Evaluating whether gut microflora communities are compromised in urban pipistrelle bats compared to rural populations
• Testing for differences in the signature of chemical pollutants in bat fur between urban and rural populations
• Testing for differences in the temperature and thermal stability of roosts in urban and rural sites
• Modeling population growth from habitat use and composition to inform conservation and survey effort
The student will investigate these questions in two common UK bat species, the common pipistrelle (Pipistrellus pipistrellus) and soprano pipistrelle (Pipistrellus pygmaeus), to improve our understanding of ecological and human factors influencing physiological stress in bats. It is anticipated that the findings of this work will inform landowners and policymakers on conservation management.

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Image Captions

Loch Lomond, one of our rural study sites, and the location of the Iapetus training course in statistics Image by © User:Colin / Wikimedia Commons, CC BY-SA 4.0, https://commons.wikimedia.org/w/index.php?curid=45427681

Soprano Pipistrelle, Pipistrellus pygmaeus, one of the focal species for the project. Image by Evgeniy Yakhontov, CC BY-SA 3.0, https://commons.wikimedia.org/w/index.php?curid=14637689

Methodology

Fieldwork

The student will use an established gradient of urbanization running from Loch Lomond and the Trossachs National Park to Central Glasgow (used for ongoing studies on birds by Dr Davide Dominoni, University of Glasgow). Bat boxes in the area are already monitored by local bat groups. Boxes will be fitted with iButtons to continuously monitor environmental temperature.

In summer 2020 and 2021 faeces will be collected from pipistrelles during routine monitoring. Bats will be held individually in a cloth bag and faeces deposited will be preserved in ethanol. Bat will be weighed, sexed, aged (juvenile or adult) and measured (forearm), and the species identified before release. Condition score will be calculated from the ratio between body mass and forearm length.

In 2021 and 2022 a harp trap will be set up along the gradient to catch bats. The harp trap will be checked at regular intervals and bats will be released after collection of faecal samples and phenotypic data (see above).

Analysis of samples

Glucocorticoids will be assayed from faeces and hair using Enzyme-Linked Immunosorbent assay (ELISA). We will use high-throughput sequencing of the 16S rRNA marker to investigate the gut microbial community in faecal samples from rural (Loch Lomond) and urban (Glasgow) sites in collaboration with Dr Martin Llewellyn (University of Glasgow). Trace metal concentrations in bat fur will be quantified using inductively coupled plasma-optical emission spectrometry (Flache et al. 2015). Statistical analysis will be carried out in R.

Population modeling

Habitats along the gradient will be classification using Google Earth. Data on habitat composition and habitat use (bat location data) will be used to predict population growth or decline via a Habitats-to-Populations approach (Mattiopoulous et al. 2015).

Project Timeline

Year 1

The student will carry out a comprehensive literature review of the effects of urbanization on physiological indicators of welfare in wildlife and plan the study design.
The student will undertake skill and theory training (e.g. capture methods; animal ethics) as required and apply for relevant licenses.
Bat boxes will be fitted with iButtons.
The student will collect faecal and hair samples from monitored bat boxes and roosts with the assistance of local bat groups.
Validation of faecal and hair glucocorticoids will be carried out. The student will begin writing up these results as a methods paper towards the end of Year 1.

Year 2

Collection of faecal and hair samples from monitored bat boxes and roosts with the assistance of local bat groups.
Analytical and quantitative skills training.
Microbiome analysis from faecal samples.
Glucocorticoid and chemical analysis from hair and faecal samples.
Classification of habitat composition using Google Earth.
Key findings will be presented at a national conference (e.g. British Ecological Society).
Manuscript preparation and thesis writing will begin.

Year 3

Data analysis and modelling will be completed in Year 3 of the project.
The student will use data on habitat composition and habitat selection to predict population growth or decline via a Habitats-to-Populations approach (Mattiopoulous et al., 2015). The main findings will be presented at one or two national conferences and one international conference. The results will be published in high impact scientific journals.

Year 3.5

Thesis preparation and submission. Summaries will be provided to the Bat Conservation Trust to inform survey effort and site selection. There will be opportunities for outreach activities working with local bat groups and Glasgow Science Festival.

Training
& Skills

The PhD will be based at the University of Glasgow, and the student will visit Stirling for meetings and seminars. Training will be carried out by recognized experts in welfare physiology, statistics and bat ecology. This includes:
Enzyme-linked immunosorbent assay (Glasgow Vet School).
Bat handling, harp trap and mist netting, if needed (Field Studies Council and local bat groups)
Habitat mapping and sampling design.
Ethics, legislation and welfare (Home Office accredited skills and theory course).
Toxicological hair analysis.
Microbiome analysis.
Environmental temperature measurements.
Training in statistical and population modeling via the Iapetus Consortium (e.g. Programming and Analysis of Environmental Data in R, SCENE Field Station).
The student will also be trained in core transferable skills that will assist with preparing manuscripts and presenting results at conferences.

References & further reading

Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, Briggs JM (2008) Global change and the ecology of cities. Science 319:756-760

Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators. Endangered Species Research 8(1-2):93-115

Jung K, Threlfall CG (2016) Urbanisation and its effects on bats – a global meta-analysis. In: Voigt CC, Kingston T (eds) Bats in the Anthropocene: conservation of bats in a changing world. Springer International Publishing, pp 13-33

Lintott, P.R., Barlow, K., Bunnefeld, N., Briggs, P., Gajas Roig, C. and Park, K.J. (2016) Differential responses of cryptic bat species to the urban landscape. Ecology and evolution 6(7), 2044-2052.

Matthiopoulos J, Fieberg J, Aarts G, Beyer HL, Morales JM, Haydon DT. (2015) Establishing the link between habitat selection and animal population dynamics. Ecological Monographs. 85: 413-436.

Russo, D and Ancillotto, L (2015) Sensitivity of bats to urbanization: a review. Mammalian Biology 80(3): 205-212.

Further Information

Applications: to apply for this PhD please use the url: https://www.gla.ac.uk/study/applyonline/?CAREER=PGR&PLAN_CODES=CF18-7316

Bat Conservation Trust:
https://www.bats.org.uk/

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