Investigating the behaviour and welfare of captive flamingos (Phoenicopteriformes) Submitted by Paul Edward Rose to the University of Exeter as a thesis for the degree of Doctor of Philosophy in Psychology In February 2018 This thesis is available for Library use on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. I certify that all material in this thesis which is not my own work has been identified and that no material has previously been submitted and approved for the award of a degree by this or any other University. ABSTRACT When a species is housed in captivity there are facets of the managed environment that can impact on individual and population welfare. A key component of an individual’s environment is its social environment, which can have important implications for animal health and welfare. Highly social species may experience impoverished welfare if kept in captive groups that differ in size, structure and demographic to that experienced by free-living animals. Amongst the most common of social animals to be housed in captivity are the flamingos (Phoenicopteridae). The unique evolutionary biology of these birds means that key aspects of their behaviour depends upon group living. A positive relationship between breeding success and increasing flock size has previously been noted, but how flamingo flocks are structured socially remains mysterious. All six species of flamingo are currently found in captive collections. The three more generalist species, greater (Phoenicopterus roseus), Caribbean (P. ruber) and Chilean (P. chilensis) flamingos are found commonly in zoos and can, under the right conditions, breed well. The other flamingo species are much more specialised in their habitat and dietary requirements and have proved more challenging with regards to their captive management. These three species are the Andean (Phoenicoparrus andinus), James’ (P. jamesi) and lesser (Phoeniconaias minor) flamingos. All six species are included in the experimental work presented in this thesis. This research aimed to evaluate specific elements of flamingo group living using social network analysis (SNA). It also aimed to assess influences of the captive environment (i.e. enclosure style and visitor number) and climate on enclosure usage, time-activity budgets and behavioural diversity to provide, as far as possible, a complete insight into how to measure, assess and evaluate captive flamingo welfare. A synthesis of the relevance of SNA to zoo animal management, and a review of current literature to identify research needs that could evidence good flamingo husbandry form the basis of the first two chapters. These two overview chapters support the questions asked in the following data-based sections of the thesis. Flamingos were observed at WWT Slimbridge Wetland Centre from March 2012 to July 2016 with data on patterns of social associations being collected four times daily (depending upon weather and bird husbandry). Associations were defined as birds within one neck length of each other and, using photos, the affiliations of each bird in the group were recorded. For assessment of bond strength, network position and identification of preferred/avoided partners a Half-Weight Index was applied to these data. Permutation testing was applied to association matrices to determine the difference between the number of observed preferential bonds (and avoided bonds) and Mantel tests were used 1 to compare matrix correlations to assess differences between seasons, species, years and enclosures (where appropriate). The SNA programmes Socprog, UCInet and Netdraw were used to analyse network data. These network data form the basis of three chapters and show that flamingos associate preferentially with non-random bonds occurring in all flocks observed. Influences of social bonds on courtship display were also examined, and temporal changes in association were considered across time, season and year. Finally, to see any influence of animal health on bond preferences, scores of foot condition (used to identify and evaluate the presence and severity of pododermatitis on an individual bird) were analysed alongside of network measures for three flocks of flamingos. To measure enclosure usage, each species’ exhibit was measured and zones accessible to the birds were defined. As exhibit use can be based on resource use (and these resources can form differently-sized areas within an exhibit) a modified Spread of Participation Index (SPI) was used to provide an outcome between 1 (one area or resource used more than others) and 0 (equal use of all resource zones). Time-activity budgets were calculated for all flocks over daytime, and for one flock (measured using remote camera traps) over night. These data are presented in two chapters and demonstrate that captive flamingos can change their activity patterns in a similar manner to that noted in wild birds. Interestingly, flamingos are very active during the night and this provides useful data for zoo personnel to consider when re-assessing husbandry and management plans for these most ubiquitous of zoo birds. 2 TABLE OF CONTENTS ABSTRACT .................................................................................................................. 1 TABLE OF CONTENTS ................................................................................................ 3 LIST OF TABLES ......................................................................................................... 8 LIST OF FIGURES ..................................................................................................... 10 ACKNOWLEDGEMENTS ........................................................................................... 12 DECLARATION .......................................................................................................... 15 ABBREVIATIONS ....................................................................................................... 17 THESIS OVERVIEW................................................................................................... 18 CHAPTER 1 ............................................................................................................... 28 1.1. Abstract ........................................................................................................ 29 1.2. Introduction ................................................................................................... 30 1.2.1. Understanding social behaviour in zoo populations ............................... 31 1.3. What is social network analysis? .................................................................. 32 1.3.1. Quantifying social interactions / associations ......................................... 33 1.3.2. Describing patterns in a network ............................................................ 38 1.4. Applications of SNA in the zoo ...................................................................... 43 1.4.1. Providing evidence for positive welfare .................................................. 43 1.4.2. Managing breeding programmes ........................................................... 45 1.4.3. Manipulating social groups .................................................................... 47 1.4.4. Determining resource use in enclosures ................................................ 51 1.4.5. Disease transmission ............................................................................. 52 1.5. Conclusions and chapter summary ............................................................... 53 CHAPTER 2 ............................................................................................................... 55 2.1. Abstract ........................................................................................................ 56 2.2. Introduction ................................................................................................... 57 2.3. Current knowledge ........................................................................................ 59 2.3.1. Flock size .............................................................................................. 60 2.3.2. Social behaviour and group displays ..................................................... 61 2.3.3. Foraging and activity patterns ................................................................ 62 3 2.3.4. Enclosure design ................................................................................... 64 2.3.5. Diet and plumage colour ........................................................................ 64 2.3.6. Flight restraint ........................................................................................ 65 2.3.7. Sociality and association patterns .......................................................... 66 2.4. Future directions ........................................................................................... 67 2.4.1. Flock size .............................................................................................. 68 2.4.2. Associations, social activity and group displays ..................................... 69 2.4.3. Foraging and activity patterns ................................................................ 69 2.4.4. Enclosure design ................................................................................... 70 2.4.5. Diet and plumage colour ........................................................................ 71 2.4.6.