Features of psittacine birds in captivity: focus on diet selection and digestive characteristics Isabelle Kalmar 2011 Promotor Prof. dr. Geert P.J. Janssens Ghent University, BE Guidance Committee Prof. dr. An Martel Ghent University, BE Prof. dr. Geert P.J. Janssens Ghent University, BE dr. Christel P.H. Moons Ghent University, BE Other members Prof. dr. Marcus Clauss Examination Committee University of Zürich, CH dr. Andrea L. Fidgett Chester Zoo, UK dr. Joeke Nijboer Rotterdam Zoo, NL Dr. Petra Wolf University of Hannover, DE Dr. Guy Werquin Versele-Laga Ltd., BE Features of psittacine birds in captivity: focus on diet selection and digestive characteristics Isabelle Kalmar Thesis submitted in fulfilment of the requirements for the degree of doctor in Veterinary Science (PhD) Faculty of Veterinary Medicine Ghent University 2011 Department of Animal Nutrition, Genetics and Ethology, Faculty of Veterinary Medicine Heidestraat 19, B-9820 Merelbeke, Belgium Kalmar, I.D. (2011) Features of psittacine birds in captivity: focus on diet selection and digestive characteristics PhD thesis, Ghent University, Belgium. With references, with summaries in English and Dutch. ISBN 978-90-5864-250-9 . Soon you will not see us in the forest if you look, the library is where we‟ll be inside a picture book. (Plight of the Parrot - Terri L. Doe) TABLE OF CONTENTS LIST OF ABBREVIATIONS 1 CHAPTER 1 General introduction 3 1.1. Background information on psittaciform birds 5 1.2. Housing and environmental enrichment 15 1.3. The use of parrots as laboratory animals 21 1.4. Digestive characteristics and nutrition 34 CHAPTER 2 Scientific aims 61 CHAPTER 3 Effect of dilution degree of commercial nectar and provision of fruit 65 on food, energy and nutrient intake in two rainbow lorikeet subspecies CHAPTER 4 Effects of segregation and impact of specific feeding behaviour and 83 additional fruit on voluntary nutrient and energy intake in yellow-shouldered amazons (Amazona barbadensis) when fed a multi-component seed diet ad libitum. CHAPTER 5 Apparent nutrient digestibility and excreta quality in African grey 105 parrots fed two pelleted diets based on coarsely or finely ground ingredients. CHAPTER 6 General discussion 123 SUMMARY 135 SAMENVATTING 141 ACKNOWLEDGEMENTS 147 SCIENTIFIC PUBLICATIONS 151 CURRICULUM VITAE 165 List of Abbreviations | 1 aD apparent digestibility H Trichoglossus h haematodus (green-naped lorikeet) AF as fed (on fresh matter basis) M Trichoglossus h mitchelli AWA Animal Welfare Act (red-breasted lorikeet) BW bodyweight MBW metabolic bodyweight Ca calcium ME metabolizable energy1 CF crude fibre N nectar CITES Convention on International Trade of Endangered Species NfE nitrogen free extract CP crude protein NSP non-starch polysaccharides C-pellets coarse particle pellets OM organic matter D dilution degree P phosphorous DM dry matter S subspecies ECI excreta consistency index St starch EE ether extract (crude fat) F-pellets fine particle pellets Su sugar F fruit VAM extruded pellets enriched with vitamins, amino acids and minerals 1 Due to the lack of established equations to calculate ME for psittacine species, distinct equations are applied in the species-specific literature. In order to facilitate comparison of data to the available literature, corresponding equations were used in the different chapters: Chapter 3: equation developed for poultry [Larbier and Leclerck (1992)] -1 MElorikeets (MJ ME kg ) = 0.1551 CP (%) + 0.3431 EE (%) + 0.1301 Su (%) + 0.1669 St (%) Chapter 4 and 5: modified equation originally developed for poultry [Schoemaker and Beynen (2001)] -1 MEgranivorous parrots (MJ ME kg ) = 0.18 CP (%) + 0.39 EE (%) + 0.17 NfE (%) CHAPTER 1 GENERAL INTRODUCTION In part after: Kalmar ID, Janssens GPJ and CPH Moons. 2010. Guidelines and ethical considerations for housing and management of psittacine birds used for research purposes. Institute for Laboratory Animal Research (ILAR) Journal 51, 409-423. Kalmar ID, Moons CPH, Meers L and GPJ Janssens. 2007. Psittacine birds as laboratory animals: reflections on welfare. Journal of the American Association for Laboratory Animal Science 46, 8-15. General Introduction | 5 1.1. BACKGROUND INFORMATION ON PSITTACIFORM BIRDS The Psittaciformes or parrots form a large order of land birds comprising over 350 species in about 83 genera (Collar, 1997). In Belgium and the rest of Europe, the total number of parrots kept in captivity is estimated to be 3 and 45 million, respectively (Ghysels, 2005). In the United States they are the third most popular companion animal, estimated at 10.1 million individuals in 2002 (AVMA, 2002). SYSTEMATICS Psittaciform birds have distinct morphological traits, such as a stout curved beak topped by a cere (the bump where the nostrils are located), zygodactyl feet (two toes pointing forward and two backward), and colourful plumage. Traditionally, psittacines are phylogenetically placed between the Columbiformes (pigeons) and Cuculiformes (cuckoos). Using molecular techniques, Sibley and Ahlquist (1990) suggested a closer relationship with Apodiformes (swifts), but this would be inconsistent with the plesiomorphic or primitive distal centriole in swift sperm (Jamieson and Tripepi, 2005). Within the order of Psittaciformes, two distinct groups are generally recognized as separate families: Cacatuidae (cockatoos) and Psittacidae (parrots) (Collar, 1997; Forshaw and Cooper, 2002). External morphological features of cockatoos that distinguish them from other parrots include an erectile crest and lack of Dyck texture 2 in feathers. As a result of the latter, cockatoos never display blue or green colours in their plumage. An internal difference includes the presence in cockatoos of a gallbladder, which is absent in other parrots (Rowley, 1997). Recent phylogenetic data (Tokita et al., 2007) suggest a third family in the order of Psittaciformes, the Nestoridae, which includes the New Zealand parrots: kakapo (Strigops habroptilus), kea (Nestor notabilis), and kaka (Nestor meridionalis). Lories and lorikeets form another separate group of parrot species. These birds are distinguished by certain anatomical features and feeding preferences, but their classification into a subfamily within the Psittacidae (Loriinae) or into a separate family (Loriidae) remains controversial (Russell, 1987; Forshaw and Cooper, 2002). The most prominent anatomical characteristic of lories is their long, brush-tipped tongue and slender beak, which reflect a high degree of diet specialization towards nectar and pollen (Cornejo and Clubb, 2005). 2 Blue feather colour is formed by nanostructures in the feather called Dyck texture (Dyck 1971a,b). 6 | C h a p t e r 1 GEOGRAPHIC DISTRIBUTION Most psittacines are native to the southern hemisphere and are predominantly, but not exclusively, found in tropical regions. Lories, lorikeets, and cockatoos occur naturally only in Australia and surrounding Indonesian islands. Genera in the family of Psittacidae, on the other hand, are indigenous to Asia, Central and South America, Africa, and the Australian continent. There are only two genera of Asiatic parrots: hanging parrots (Loriculus spp.) and ring-necked parakeets (Psittacula spp.). Pionus parrots (Pionus spp.), macaws (Ara, Cyanopsitta, and Anodorhynchus spp.) and conures (e.g., Aratinga, Cyanoliseus, and Pyrrhura spp.) are native to South America, and the amazons (Amazona spp.) originate from Central and South America. African greys (Psittacus spp.), poicephalus parrots (Poicephalus spp.), and lovebirds (Agapornis spp.) originate from Africa; whereas grass parakeets (Neophema spp.), budgerigars (Melopsittacus spp.), and rosellas (Platycercus spp.) are indigenous to Australia (Russell, 1987). Irrespective of geographical origin, descendents of escaped cage birds have been establishing self-sustaining populations in regions other than their native habitat. For instance, monk parakeets (Myopsitta monachus), which are indigenous to South America, have formed feral populations on four other continents (Russello et al., 2008), and in the United States the American Ornithologists‟ Union has identified seven parrot species as self-sustaining exotics, with another seven likely to be recognized as such in the near future. The two native US parrot species, the Carolina parakeet (Conuropsis carolensis) and the thick-billed parrot (Rhynchopsitta pachyrhyncha), on the other hand, disappeared during the 20th century (Butler, 2005). Efforts to re-establish the latter, however, have not resulted in self-sustaining wild populations. Still, release experiments with wild-caught birds from Mexico, where the species is still extant, have resulted in a limited number of surviving, trans-located birds and some reproductive success in Arizona (Snyder et al., 1994). CONSERVATION STATUS Unlike most taxa, parrots are vulnerable to multiple sources of extinction risk, which include a.o. habitat loss, introduction of predators and competitors, and human persecution such as trade (Juniper and Parr, 1998; Owens and Bennett, 2000). As a result, a higher proportion of species within the order of psittacine birds is threatened with extinction compared to most other bird orders (Bennett and Owens, 1997; Owens and Bennett, 2000). General Introduction | 7 Almost all parrot species are listed by the Convention on International Trade in Endangered Species (CITES). This is an international treaty that regulates the import and export of endangered wild flora and fauna, based on their classification into one of three Appendices. These regulations