The Department of Biological Sciences has an expanding research base, which, in addition to providing leading researchers of national and international standing in these areas, most importantly underpins the delivery of teaching. Research in Biological Sciences at Chester can be divided into three broad groups of expertise, namely Animal Behaviour and Conservation, Food Nutrition and Health, and Stress and Disease.

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  • Lower pollen nutritional quality delays nest building and egg laying in Bombus terrestris audax micro-colonies leading to reduced biomass gain

    Ryder, Jordan T.; Thompson, Helen M.; Walters, Keith F. A.; Cherrill, Andrew; Harper Adams University; University of Chester; Syngenta; Imperial College London (Springer, 2021-09-27)
    The performance of Bombus terrestris micro-colonies fed five diets differing in pollen species composition and level of nine essential amino acids (EAA; leucine, lysine, valine, arginine, isoleucine, phenylalanine, threonine, histidine, methionine) was assessed for 37 days by recording total biomass gain, nest building initiation, brood production (eggs, small and large larvae, pupae, drones), nectar, and pollen collection. Stronger colony performance was linked to higher amino acid levels but no consistent differences in biomass gain were recorded between mono- and poly-species diets. Poorest performance occurred in micro-colonies offered pure oilseed rape (OSR) pollen which contained the lowest EAA levels. Reduced micro-colony development (delayed nest initiation and lower brood production) was related to OSR proportion in the diet and lower EAA levels. Results are discussed in relation to selection of plant species in the design of habitats to promote bee populations.
  • Depth and temperature profiles reflect individual differences in the daytime diving behaviours of pelagic thresher sharks

    Oliver, Simon P.; Grothues, Thomas M.; Mayo, Zoe J.; Williams, Aimie L.; Silvosa, Medel; Cases, Gary; University of Chester; The Thresher Shark Research and Conservation Project; The State University of New Jersey; University of Liverpool; NatureScot; Mindanao State University; Divelink Cebu
    We used acoustic telemetry to investigate the roles of depth and temperature in the daytime foraging behaviours of 13 tagged pelagic thresher sharks by monitoring their fine scale vertical movements in the Philippines. Cumulatively, pelagic thresher shark dives traversed the entire water column where they encountered temperatures that ranged from 33oC at the surface to 12oC at 250m depths throughout the day, but the movements of individuals varied in the extent of both their deep and shallow water limits. Dives were not synchronized to diurnal cycles, and periodicity reflected cycles of similar dives, the dives themselves, deviations, cruising, and individuality. Pelagic thresher shark movements between the warm surface layer and cooler waters below the thermocline (155 – 175 m) may reflect a common Alopiid strategy that balances maintaining tolerable ambient water temperatures with opportunities to search for and forage on spatially patchy distributions of prey.
  • See you in spring: overwinter survival is higher than post summer in the Alpine marmot

    Ferrari, Caterina; Cerri, Jacopo; Rolando, Antonio; Bassano, Bruno; von Hardenberg, Achaz; Bertolino, Sandro (Informa UK Limited, 2023-01-09)
  • Interacting effects of environmental enrichment across multiple generations on early life phenotypes in zebrafish

    Green, Michael R.; Swaney, William T.; University of Chester; Liverpool John Moores University (Wiley, 2022-12-07)
    The environment plays an important role in an individual's development during early life, however, parents may also influence offspring development through so called “parental effects.” We examined the effects of environmental enrichment in zebrafish (Danio rerio) across two generations through the paternal lineage. Fathers and grandfathers were exposed to either standard or high levels of housing enrichment for 4-weeks during adulthood. First-generation (F1) and second-generation (F2) offspring were obtained from controlled breeding and tested as larvae for changes in morphology at hatching stage (72hpf), and in locomotor activity at larval stage (120hpf) in both generations. We found paternal experience of enrichment resulted in changes in trunk length of F1 offspring and changes in spine curvature and dorsal length of F2 offspring, while changes in snout morphology of F2 offspring seemed to be driven by whether grandpaternal and paternal experience of the environment was matched or not. We found that while paternal enrichment increased the frequency of spontaneous movement in F1 and F2 offspring, interacting effects of paternal and grandpaternal enrichment on movement distance were seen in F2 offspring, and that spontaneous movement and the distance that larvae swam are thus distinct phenotypes that were differentially affected by the experiences of previous paternal generations. Taken together, these findings suggest that the parental and grandparental environment influence zebrafish behavior and morphology. The nature of these effects and the design of this study mean that these phenotypes were likely the result of nongenetic transmission through the paternal germline.
  • Degree of egg-taking by humans determines the fate of maleo (Macrocephalon maleo) nesting grounds across Sulawesi

    Summers, Marcy; Geary, Matthew; Djuni, Nurlin; Kresno, Pandji, A.; Laya, Augustian; Stallin, Sawuwu; Bawotong, Adrianus; Abas, Wiranto; Oga, Vivi Megayanti T.; Nur, Ahmad Muh; et al. (Springer, 2022-12-17)
    The maleo (Macrocephalon maleo) of Sulawesi, Indonesia, is culturally iconic and Critically Endangered, but the causes of its decline have never been systematically analyzed nor its nesting grounds comprehensively surveyed. We visited 122 previously known and 58 previously unrecorded sites, collecting data and interviewing local people at each site. We used ordinal logistic regression to fit models with combinations of 18 different predation, habitat, and nesting ground variables to determine the strongest predictors of nesting ground success, as represented by maleo numbers. At least 56% of known nesting grounds are now inactive (abandoned), and 63% of remaining active sites host ≤ 2 pairs/day at peak season. Egg-taking by humans is the single biggest driver of maleo decline. Protecting eggs in situ predicts higher numbers than protecting eggs through hatchery methods. After egg-taking, quality (not length) of the travel corridor connecting nesting ground to primary forest best predicts nesting ground success. Being inside a federally protected area is not a primary driver of success, and does not ensure persistence: 28% of federally protected nesting grounds have become inactive. Local conservation efforts protected nesting grounds 2‒3 times better than federal protection. We update the methodology for assessing nesting ground status, and recommend five measures for maleo conservation, the foremost being to protect nesting grounds from egg-taking by humans at all remaining active sites.
  • Distribution of the reef manta ray Mobula alfredi and the oceanic manta ray Mobula birostris in the Philippines: A collaborative effort for conservation

    Rambahiniarison, Joshua; Agustines, Ariana; Alexopoulos, Konstantinos; Araujo, Gonzalo; Armstrong, Asia O.; Arnold, Shannon; Barruga, Aldrin; Cañete, Titus; Conales, Segundo; Delijero, Kymry; et al. (Wiley, 2022-11-30)
    Little is known about manta ray population size, structure, and connectivity in the Philippines. In collaboration with dive operators, non-governmental organizations, and authorities, sightings of manta rays were collated into a single national database. Using in-water photographs and videos gathered through citizen science and dedicated research efforts, this study compiled sightings between 2004 and 2020, showing 22 separate sites throughout the archipelago with manta rays present. A total of 392 individual reef manta rays (Mobula alfredi) and 107 oceanic manta rays (Mobula birostris) were identified from the collected footage. Four specific sites in the provinces of Masbate and Palawan together hosted 87% of all identified individuals and accounted for 94% of sightings, highlighting these areas are key aggregation sites. This study also reports movements of M. birostris within the Philippines, based on photo-identification of three individuals moving 150 km between Cebu and Masbate. Despite the growing number of recreational divers in Daanbantayan and San Jacinto, an 80% decline in M. birostris sightings was observed at these sites. To ensure effective future conservation, it is recommended that efforts focus on the identification and protection of manta ray hotspots and migratory corridors, the creation of a sustainable tourism framework, and most importantly, on the implementation of mitigation strategies to reduce fisheries interactions.
  • Distribution and habitat requirements of the Bahama Warbler Setophaga flavescens on Grand Bahama in 2018

    Pereira, David J.; Gardner, Matthew A.; Geary, Matthew; Bell, Diana J.; Collar, Nigel J.; University of East Anglia; BirdLife International
    The Bahama Warbler Setophaga flavescens is restricted to Grand Bahama and Abaco in the Bahamas Islands, where in recent decades its pine forest habitat has been seriously affected by hurricanes. To assess its conservation status and determine its habitat requirements, we conducted point transects with playback and simultaneously took measurements at 464 locations in pine forest across Grand Bahama from April to June 2018. Warbler presence was predicted by taller Thatch Palms Thrinax radiata and some fire disturbance; and its absence by a higher number of needleless pines. A comparison of these habitat predictors between the combined regions where warblers were detected (Lucayan Estates and East End) vs. where they were not (West End and Freeport) also revealed that Bahama Warblers showed a marked preference for taller Thatch Palms (>140 cm) and habitat plots within the middle fire disturbance category. These findings suggest that the species is adapted to a climax pine forest habitat maintained under a standard fire regime. Our research was intended to provide a first baseline study of the warbler’s distribution and ecology on Grand Bahama, but the distribution may have radically changed following Hurricane Dorian’s devastation of the island in 2019, and the species may now only survive on Abaco. Nevertheless, ecological insights from Grand Bahama seem likely to help conservation management on Abaco; but both islands now need to be surveyed.
  • Factors affecting the survival of harbor (Phoca vitulina) and gray seal (Halichoerus grypus) juveniles admitted for rehabilitation in the UK and Ireland

    Zatrak, Michal; Brittain, Sam; Himmelreich, Lauren; Lovick-Earle, Susie; Pizzi, Romain; Shaw, Kirsty J.; Grant, Robyn A.; Geary, Matthew; Manchester Metropolitan University; University of Chester; Seal Rescue Ireland; Northcoast Marine Mammal Center, California; University of St Andrews; Tynemouth Seal Hospital; Wildlife Surgery International, Roslin (Wiley, 2022-10-14)
    The UK shores are home to approximately 40% of the world's population of gray seals (Halichoerus grypus) and 40% of Europe's harbor seals (Phoca vitulina). Stranded juvenile seals of both species are frequently rescued and admitted for rehabilitation. This study investigates the causes of P. vitulina and H. grypus admittance to rehabilitation centers in the UK and Ireland and identifies factors that can affect juvenile seal survival. Rehabilitation records for 1,435 P. vitulina and 2,691 H. grypus were used from five rehabilitation centers from 1988 through 2020. The most common nonexclusive reasons for seal admission to rehabilitation centers included malnourishment (37%), injuries (37%), maternal abandonment (15%), lethargy (12%), and parasite infections (8%). A mixed effects logistic regression model showed that H. grypus had 4.55 times higher survival odds than P. vitulina and that the odds of survival to release multiplied by 1.07 for every kilogram over their age-predicted weight. This weight-dependent survival could be attributed to the importance of fat in thermoregulation, hydration, and buoyancy during foraging. We recommend that seal rehabilitators pay special attention to the weight of admitted juvenile seals during triage and treatment to enhance their odds of survival and consequent release to the wild
  • Camera traps and genetic identification of faecal samples for detection and monitoring of an Endangered ungulate.

    Geary, Matthew; Hartley, Matthew; Ball, Zoe; Wilkes, Sammie; Khean, Mao; Ball, Rachel J.; Peters, Catherine M.; Muir, Anna P.; University of Chester; Wildlife Conservation Society Cambodia, Kampong Pranak, Preah Vihear
    Almost all Indochinese ungulates are classified as globally threatened but efforts to assess and monitor population status have been hampered by their rarity, cryptic nature and uncertainty in accurate identification from sightings. An improved approach is urgently needed to gather information about threatened ungulate species in order to effectively conserve them as, a lack of reliable monitoring methods means that basic information such as population sizes, distribution and habitat associations is currently unknown. Here, we used a combination of camera trapping and genetic detection of the Endangered Eld’s deer, Rucervus eldii, to investigate the utility of these methods to infer intensity of site use within a protected Cambodian dry forest. We asked: 1) Are Eld's deer present in our study area?; 2) How is site use influenced by local habitat?; and 3) Do camera traps or genetic detection perform better in terms of detection and monitoring? Camera traps were deployed and faecal samples collected from Chhaeb Wildlife Sanctuary in Northern Cambodia during the 2017 dry season. Faecal samples were identified as Eld’s deer using newly developed species-specific mitochondrial DNA primers. Camera traps recorded 20 Eld’s deer observations across 3905 trap-nights and 44 out of 71 collected faecal samples, identified by fieldworkers as likely to belong to Eld’s deer, were positively identified to be so. Camera trap surveys and genetic detection demonstrated that Eld’s deer were present in Chhaeb Wildlife Sanctuary, although the number of detections relative to sampling effort was low in both methods (detected at 29% and 1% of sample sites, respectively). Occupancy models showed that water level and tree diameter both had positive relationships, whilst human and domestic or feral pig activity had a negative relationship, with the relative intensity of Eld’s deer site use. Overall, our data suggest that both of our methods can prove effective for monitoring Eld’s deer but that repeated sampling is necessary to account for their low detectability in this area. We suggest that faecal samples are collected during future camera trap monitoring visits to maximise efficiency, increase detectability, and provide the most information to support conservation.
  • Intra- and inter-operator variability of refractometric total proteins measurement of canine plasma

    Venier, F.; Jamont, W.; McLennan, Krista; Rosa, C.; Northwest Veterinary Specialists; University of Chester (AOSIS, 2022-11-07)
    Refractometric total proteins are commonly used in practice as a quick and inexpensive way to measure total protein concentration in bodily fluids. Little information is available about how the operator performing the measurement affects the results. The aim of our study was to determine the inter- and intra-operator variability of refractometric total proteins measured on canine plasma using a temperature-compensated handheld refractometer. A pooled sample of canine lithium-heparin plasma was created using leftover samples from dogs presented to our hospital. The sample was then divided into three aliquots. Total proteins of these aliquots were measured by veterinary nurses, interns, residents and specialists working at our hospital. Statistical analysis revealed excellent inter-operator (ICC 0.99, CI 95% 0.971–1.00) and intra-operator (ICC 0.997, CI 95% 0.990–0.999) variability. Having different operators measuring refractometric total plasma proteins in practice should not affect the results. This suggests different operators can be used when monitoring total plasma proteins of a patient over time and when designing a study that involves this test.
  • The status of cetaceans in Trinidad and Tobago

    Nelson, Howard P.; Oliver, Simon; Lawrence, Andrew; Naranjit, Alёsha R. (University of Chester, 2021-12-14)
    Marine ecosystems provide vital resources for humans and habitat for a vast number of other species. However, these ecosystems are being extensively degraded by human activities, and without effective management, will be unable to provide for humans or other species. In Trinidad and Tobago, as in other countries, one of the major obstacles to effective environmental management is a lack of appropriate information. This thesis aims to enhance the management of cetaceans in Trinidad and Tobago by providing much needed information on cetacean species within the country’s EEZ (Exclusive Economic Zone). Cetacean species diversity and distribution in Trinidad and Tobago is examined through the collation and verification of records from multiple data sources including systematic surveys, reports, skeletal remains, strandings and social media posts. This research provides the first comprehensive overview of the knowledge of cetacean species around Trinidad and Tobago through a verified cetacean species list, estimation of species diversity from local data and maps of species occurrence records. Species Distribution Models were developed for four species (Humpback Whales, Bottlenose Dolphins, Atlantic Spotted Dolphins and Rough-toothed Dolphins) which provide the first estimates of cetacean species distribution across the Trinidad and Tobago EEZ and identify possible cetacean species richness hotspots around the country. Fisher interviews were used to examine the threat posed by artisanal fisheries within the Trinidad and Tobago EEZ and provide the first comprehensive information on cetacean-fisheries interactions for the country. Hunting, depredation (a behaviour in which foraging cetaceans damage or remove catch or bait from fishing gear) and bycatch were all reported in the area. Bycatch was identified as the greatest threat posed by artisanal fisheries locally and analysis indicated that fishing with gillnets or fishing on the south coast of Trinidad with any gear increased the risk of bycatch. The findings of this study were used to recommend actions to improve cetacean management in Trinidad and Tobago, including the creation of a cetacean data management system, the development of a cetacean research programme to guide future research and mitigation of anthropogenic threats on the continental shelf, including cetacean bycatch in artisanal fisheries.
  • The effects of allogrooming and social network position on behavioural indicators of stress in female lion-tailed macaques (Macaca silenus)

    Yates, Kerrie; Stanley, Christina R.; Bettridge, Caroline; Manchester Metropolitan University; University of Chester; Bangor University (Elsevier, 2022-08-28)
    Allogrooming serves an important social function in primates and confers short term benefits such as parasite removal and stress-relief. There is currently mixed evidence as to the immediate impact of allogrooming on an individual’s stress levels, which may be influenced by their role in the grooming dyad, position in their social network, or their relationship with their grooming partner. In this study of seven captive adult female lion-tailed macaques (Macaca silenus) in a mixed sex group at Chester Zoo, UK, we found evidence to support a tension-reduction function of allogrooming. Focal animal sampling showed that the duration of self-directed behaviour (SDB), which indicates moderate to high levels of stress, was significantly lower in the five-minute period following allogrooming than the five-minute minute period preceding it for both recipients and groomers. However, when compared to match-control periods, both SDB rates and durations were significantly lower across all individuals in the five-minute period both before and after allogrooming, indicating that although allogrooming reduces stress, it is also more likely to occur when individuals are already in a relatively relaxed state. The rate and duration of SDB post-grooming did not correlate with the strength of a dyad’s bond (based on proximity). This suggests that it is the act of allogrooming itself, rather than the identity of the partner, that reduces stress for both parties. Analysis of the proximity network highlighted a clear cost to social integration; node strength, a measure of the number and strength of an individual’s direct relationships, positively correlated with the duration of self-directed behaviour, suggesting that more gregarious individuals may experience higher levels of stress. These findings add to the growing body of literature that examines the effect of the individual social environment on primate stress levels, and also highlight the need to further investigate the link between social integration and the stress experienced by group-living animals.
  • From dyads to collectives: a review of honeybee signalling

    Hasenjager, Matthew; Franks, Victoria; Leadbeater, Ellouise; University of Tennessee; University of Chester; Royal Holloway University of London (Springer, 2022-08-22)
    The societies of honeybees (Apis spp) are microcosms of divided labour where the fitness interests of individuals are so closely aligned that, in some contexts, the colony behaves as an entity in itself. Self-organization at this extraordinary level requires sophisticated communication networks, so it is not surprising that the celebrated “waggle dance”, by which bees share information about locations outside the hive, evolved here. Yet bees within the colony respond to several other lesser-known signalling systems, including the tremble dance, the stop signal and the shaking signal, whose roles in coordinating worker behaviour are not yet fully understood. Here, we firstly bring together the large but disparate historical body of work that has investigated the “meaning” of such signals for individual bees, before going on to discuss how network-based approaches can show how such signals function as a complex system to control the collective foraging effort of these remarkable social insect societies.
  • Peptide mass fingerprinting of preserved collagen in archaeological fish bones for the identification of flatfish in European waters

    Dierickx, Katrien; Presslee, Samantha; Hagan, Richard; Oueslati, Tarek; Harland, Jennifer; Hendy, Jessica; Orton, David; Alexander, Michelle; Harvey, Virginia L.; University of York; University of Lille (The Royal Society, 2022-07-27)
    Bones of Pleuronectiformes (flatfish) are often not identified to species due to the lack of diagnostic features on bones that allow adequate distinction between taxa. This hinders in-depth understanding of archaeological fish assemblages and particularly flatfish fisheries throughout history. This is especially true for the North Sea region, where several commercially significant species have been exploited for centuries, yet their archaeological remains continue to be understudied. In this research, 8 peptide biomarkers for 18 different species of Pleuronectiformes from European waters are described using MALDI-TOF MS and LC-MS/MS data obtained from modern reference specimens. Bone samples (n=202) from three archaeological sites in the UK and France dating to the medieval period (c. 7th–16th century CE) were analysed using ZooMS. Of the 201 that produced good quality spectra, 196 were identified as flatfish species, revealing a switch in targeted species through time and indicating that ZooMS offers a more reliable and informative approach for species identification than osteological methods alone. We recommend this approach for future studies of archaeological flatfish remains as the precise species uncovered from a site can tell much about the origin of the fish, where people fished and whether they traded between regions.
  • Collagen fingerprinting of Caribbean archaeological fish bones: Methodological implications for historical fisheries baselines and anthropogenic change

    Harvey, Virginia L.; LeFebvre, Michelle J.; Sharpe, Ashley E.; Toftgaard, Casper; DeFrance, Susan D.; Giovas, Christina M.; Fitzpatrick, Scott M.; Buckley, Michael; University of Manchester; University of Florida; Smithsonian Tropical Research Institute; National Museum of Denmark; Simon Fraser University; University of Oregon. (Elsevier, 2022-08-22)
    The Caribbean Sea is the most species-rich sea in the Atlantic, largely due to its vast coral reef systems. However, its high biodiversity and endemism face unprecedented anthropogenic threats, including synergistic modern pressures from overfishing, climate change and bioinvasion. Archaeological data indicate initial human settle- ment of the Caribbean ~7000 years before present (yr BP), with regionally variable human impacts on fisheries through time based on standard morphological identification of fish bone. Such studies, however, are challenged by the low taxonomic resolution of archaeological fish bone identifications due to high species diversity and morphological similarity between members of different families or genera. Here, we present collagen finger- printing (Zooarchaeology by Mass Spectrometry; ZooMS) as a method to overcome this challenge, applying it to 1000 archaeological bone specimens identified morphologically as ray-finned fish (superclass Actinopterygii) from 13 circum-Caribbean sites spanning ca. 3150–300 yr BP (years before present). The method successfully identified collagen-containing samples (n = 720) to family (21%), genus (57%), and species (13%) level. Of the 209 samples that were morphologically identified below superclass, collagen fingerprinting verified the taxo- nomic identity of 94% of these, but also refined the identifications to a lower [more precise] taxon in 45% of cases. The remaining 6% of morphological identifications were found to be incorrectly assigned. This study represents the largest application of ZooMS to archaeological fish bones to date and advances future research through the identification of up to 20 collagen biomarkers for 45 taxa in 10 families and 2 orders. The results indicate that refinement of ZooMS archaeological fish identifications in this study is limited not by the quality of the preserved collagen but by the extent of the available modern collagen reference collection. Thus, efforts should be directed towards expanding collagen fingerprint databases in the first instance. Significantly, the high- resolution taxonomic identifications of archaeological bone that ZooMS can offer make ancient fisheries data highly relevant to modern sustainability and conservation efforts in the Caribbean. Additionally, more precise identifications will allow archaeologists to address a variety of questions related to cultural fishing practices and changes in fish stocks through time. This study supports the use of ZooMS as an effective biochemical tool available for mass-taxonomic identification of archaeological fish bone samples spanning century to millennial time scales in the circum-Caribbean.
  • Baseline Behavioral Data and Behavioral Correlates of Disturbance for the Lake Oku Clawed Frog (Xenopus longipes)

    Dias, Jemma E.; Ellis, Charlotte; Smith, Tessa E; Hosie, Charlotte A; Tapley, Benjamin; Michaels, Christopher J.; University of Chester; Zoological Sciety of London Outer Circle
    Animal behavior and welfare science can form the basis of zoo animal management. However, even basic behavioral data are lacking for the majority of amphibian species, and species-specific research is required to inform management. Our goal was to develop the first ethogram for the critically endangered frog Xenopus longipes through observation of a captive population of 24 frogs. The ethogram was applied to produce a diurnal activity budget and to measure the behavioral impact of a routine health check where frogs were restrained. In the activity budget, frogs spent the vast majority of time swimming, resting in small amounts of time devoted to feeding, foraging, breathing, and (in males) amplexus. Using linear mixed models, we found no effect of time of day or sex on baseline behavior, other than for breathing, which had a greater duration in females. Linear mixed models indicated significant effects of the health check on duration of swimming, resting, foraging, feeding, and breathing behaviors for all frogs. This indicates a welfare trade-off associated with veterinary monitoring and highlights the importance of non-invasive monitoring where possible, as well as providing candidates for behavioral monitoring of acute stress. This investigation has provided the first behavioral data for this species which can be applied to future research regarding husbandry and management practices.
  • Long term analysis of social structure: evidence of age-based consistent associations in male Alpine ibex

    Brambilla, Alice; von Hardenberg, Achaz; Canedoli, Claudia; Brivio, Francesca; Sueur, Cédric; Stanley, Christina R.; University of Zurich; University of Chester; University of Milano Bicocca; University of Sassari; University de Strasbourg; Institut Universitaire de France (Wiley, 2022-06-28)
    Despite its recognized importance for understanding the evolution of animal sociality as well as for conservation, long term analysis of social networks of animal populations is still relatively uncommon. We investigated social network dynamics in males of a gregarious mountain ungulate (Alpine ibex, Capra ibex) over ten years focusing on groups, sub-groups and individuals, exploring the dynamics of sociality over different scales. Despite the social structure changing between seasons, the Alpine ibex population was highly cohesive: fission–fusion dynamics lead almost every male in the population to associate with each other male at least once. Nevertheless, we found that male Alpine ibex showed preferential associations that were maintained across seasons and years. Age seemed to be the most important factor driving preferential associations while other characteristics, such as social status, appeared less crucial. We also found that centrality measures were influenced by age and were also related to individual physical condition. The multi-scale and long-term frame of our study helped us show that ecological constrains, such as resource availability, may play a role in shaping associations in a gregarious species, but they cannot solely explain sociality and preferential association that are likely also to be driven by life-history linked physiological and social needs. Our results highlight the importance of long-term studies based on individually recognizable subjects to help us build on our understanding of the evolution of animal sociality.
  • An Examination of the Social and Physiological Experience of Captive Livingstone’s Fruit Bats (Pteropus livingstonii)

    Stanley, Christina; Smith, Tessa; Hosie, Lottie; Edwards, Morgan J. (University of Chester, 2022-02-01)
    This thesis presents a series of empirical studies designed to quantify the complex social and physiological experiences of individuals within the captive population of a critically endangered bat species, the Livingstone’s fruit bat (Pteropus livingstonii). The ultimate goal of this work was to apply leading-edge methodologies and technology to gain novel, evidence-based insights into the behaviour and welfare of this species in captivity. This work has not only informed the captive management of P. livingstonii, but has also developed techniques that can be applied to maximise the captive welfare of a range of other species. A brief summary, explaining how each chapter is embedded within the overall thesis and summarising its major findings, precedes each chapter. Chapter One, the introductory chapter, will start by evaluating our current understanding of the natural history and behavioural ecology of P. livingstonii, with a focus on captive behaviour. The following sections of this chapter will then provide necessary background information to the methodologies applied in subsequent data chapters, including social network analysis, space use assessment, hormone analysis and radio-frequency identification technology. The introductory chapter is intended to provide the reader with sufficient scientific context to interpret the results of each data chapter. Chapter Two outlines the implementation of social network analysis to characterise individual social experiences in the largest captive population of P. livingstonii, housed at Jersey Zoo. Variation in network complexity and significant individual variable-based assortment is identified in this chapter. Chapter Three presents principal component analysis as a novel compliment to traditional enclosure use assessment methodologies, quantifying the individual spatial preferences of P. livingstonii. This chapter also quantifies the relationship between high-value resource location within the enclosure at Jersey Zoo and population-level space use. Chapter Four outlines the validation and application of an enzyme immunoassay to non-invasively measure faecal cortisol in the P. livingstonii population. This chapter examines the relationship between cortisol titres, individual social roles and behavioural frequencies performed by individuals in the captive population. We find that males, older individuals and lactating females have higher concentrations of cortisol than non-lactating females and younger individuals and that social roles related to conspecific affiliation were linked to decreased cortisol titres. Lastly, Chapter Five demonstrates the application of unique radio-frequency identification technology to autonomously collect individual locational data. The resulting dataset was then utilised to interrogate the foraging network displayed by P. livingstonii and Pteropus rodricensis (a cohabitating heterospecific) populations housed at Jersey Zoo, elucidating the relationship between individual bat characteristics and social foraging patterns. Finally, the discussion chapter evaluates the significance of the main findings of each chapter of this thesis, highlighting the wider applicability of results and methodologies to the assessment of captive animal welfare. This section also critically discusses recent challenges to hypothesis testing in the field of animal social network analysis, to evaluate the validity of methods utilised throughout this thesis. Finally, future research directives leading on from this work which may provide further benefit to the management of captive populations are proposed.
  • Pre- and peri-operative clinical information, physiological observations and outcome measures following flexible ureterorenoscopy (FURS), for the treatment of kidney stones. A single-centre observational clinical pilot-study in 51 patients

    Hughes, Stephen F.; Moyes, Alyson J.; Jones, Kevin; Bell, Christopher; Duckett, Abigail; Moussa, Ahmed; Shergill, Iqbal (BioMed Central, 2022-07-14)
    Abstract: Background: Kidney stone disease contributes to a significant proportion of routine urological practice and remains a common cause of worldwide morbidity. The main aim of this clinical-pilot study was to investigate the effect of flexible ureterorenoscopy (FURS) on pre- and peri-operative clinical information, physiological observations and outcome measures. Methods: Included were 51 patients (31 males, 20 females), who underwent elective FURS, for the treatment of kidney stones. Pre-operative and peri-operative clinical information, and post-operative physiological observations and outcome measures were collected using a standard case report form. Pre-operative clinical information included age, gender, BMI, previous history of stone formation and hypertension. Pre-operative stone information included the size (mm), Hounsfield units (HU), laterality and intra-renal anatomical location. Peri-operative surgical details included surgical time in minutes; Laser use; Duration and energy of laser; and post-operative stenting. The physiological outcomes measured included systolic and diastolic blood pressure (mmHg), Likert pain score, temperature, heart rate (bpm) and respiration rate (bpm). Following initial descriptive analysis, a series of Pearson’s correlation coefficient tests were performed to investigate the relationship between surgical factors other variable factors. Results: A series of significant, positive correlations were observed between; age and surgical time (p = 0.014, r = 0.373); stone size and Hounsfield unit (p = 0.029, r = 0.406); surgical time and duration of laser (p < 0.001, r = 0.702); surgical time and BMI (p = 0.035, r = 0.322); baseline heart rate and Hounsfield unit (p = 0.026, r = − 0.414); base line heart rate and BMI (p = 0.030, r = 0.307).; heart rate at 120-min post FURS and age (p = 0.038, r = − 0.308); baseline pain score and BMI (p = 0.010, r = 0.361); baseline respiration rate and BMI (p = 0.037, r = 0.296); respiration rate at 240-min post FURS and BMI (p = 0.038, r = 0.329); respiration rate at 120 min post FURS and age (p = 0.022, r = − 0.330). Four patients developed post-operative complications (3—UTIs with urinary retention, 1–urosepsis). Conclusions: We report that following FURS there is an association between various physiological, clinical and surgical parameters. Although these correlations are weak, they warrant further investigation as these may be linked with untoward complications, such as infection that can occur following FURS. This data, however, will need to be validated and reproduced in larger multi-centre studies.
  • Social roles influence cortisol levels in captive Livingstone's fruit bats (Pteropus livingstonii)

    Edwards, Morgan J.; Stanley, Christina R.; Hosie, Charlotte A.; Richdon, Sarah; Price, Eluned; Wormell, Dominic; Smith, Tessa E.; University of Chester; Bristol Zoological Society; Durrell Wildlife Conservation Trust (Elsevier, 2022-06-27)
    A critical component of conserving and housing species ex situ is an explicit scientific understanding of the physiological underpinnings of their welfare. Cortisol has been repeatedly linked to stress, and therefore used as an indicator of welfare for many species. In order to measure cortisol in the Livingstone's fruit bat (Pteropus livingstonii; a critically endangered keystone species) without disturbing the captive population, we have developed and validated a non-invasive, novel hormone extraction procedure and faecal glucocorticoid assay. A total of 92 faecal samples, 73 from the P. livingstonii breeding colony at Jersey Zoo, Channel Islands and 19 samples from P. livingstonii housed at Bristol Zoological Gardens, UK, have been collected and analyzed. Mixed-effect modelling of the influence of physiological state variables on cortisol concentration revealed that lactating females had higher cortisol levels than non-lactating females, indicating that our assay is measuring biologically relevant hormone concentrations. Males and older bats also had higher cortisol than non-lactating females and younger individuals. Further analysis applied social network methodology to compare the cortisol levels of bats with different social roles. We found that individuals that linked social groups possessed higher than average cortisol levels and conversely, individuals with high-quality, positive relationships had lower cortisol levels. These results demonstrate, for the first time in a bat species, social mediation of stress hormones. Lastly, the frequency of vocalisation was found to positively correlate with cortisol concentration in males, suggesting that this behaviour may be used by animal management as a visual indicator of a bat's hormonal status. Hence, this research has provided unique insights and empirical scientific knowledge regarding the relationship between the physiology and social behaviour of P. livingstonii, therefore allowing for recommendations to be made to optimise bat welfare at the individual level.

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