MANUAL OF BEHAVIOR edited by ANDREW U. LUESCHER

Manual of Parrot Behavior

Manual of Parrot Behavior

Andrew U. Luescher, Editor Andrew U. Luescher, DVM, PhD, is Director of the Authorization to photocopy items for internal or per- Behavior Clinic at Purdue University. He sonal use, or the internal or personal use of specific established the Animal Behavior Clinic in 1997 and is clients, is granted by Blackwell Publishing, provided certified as an applied animal behaviorist by the that the base fee of $.10 per copy is paid directly to the Animal Behavior Society and is a diplomate of the Copyright Clearance Center, 222 Rosewood Drive, American College of Veterinary Behaviorists. He has Danvers, MA 01923. For those organizations that have been treating with behavioral problems for been granted a photocopy license by CCC, a separate more than 20 years. system of payments has been arranged. The fee code for users of the Transactional Reporting Service is © 2006 Blackwell Publishing ISBN-13: 978-0-8138-2749-0; ISBN-10: 0-8138- All rights reserved 2749-3/2006 $.10.

Blackwell Publishing Professional Printed on acid-free paper in the United States of 2121 State Avenue, Ames, Iowa 50014, USA America

Orders: 1-800-862-6657 First edition, 2006 Office: 1-515-292-0140 Fax: 1-515-292-3348 Library of Congress Cataloging-in-Publication Data Web site: www.blackwellprofessional.com Manual of parrot behavior / edited by Andrew U. Blackwell Publishing Ltd Luescher.— 1st ed. 9600 Garsington Road, Oxford OX4 2DQ, UK p. cm. Tel.: +44 (0)1865 776868 Includes bibliographical references and index. ISBN-13: 978-0-8138-2749-0 (alk. paper) Blackwell Publishing Asia ISBN-10: 0-8138-2749-3 (alk. paper) 550 Swanston Street, Carlton, Victoria 3053, Australia 1. —Behavior. I. Luescher, Andrew U. Tel.: +61 (0)3 8359 1011 SF473.P3.M27 2006 636.6Ј865—dc22

2005028547 The last digit is the print number: 9 8 7 6 5 4 3 2 1 Contents

Contributors vii

Preface ix

01 Classification and the Status of Wild Populations of Parrots 3 Dominique G. Homberger

02 Behavior of Wild Amazona and Rhynchopsitta Parrots, with Comparative Insights 13 from Other Psittacines Ernesto C. Enkerlin-Hoeflich, Noel F.R. Snyder, and James W. Wiley

03 Parrot Conservation, Trade, and Reintroduction 27 Charles A. Munn

04 Sensory Capacities of Parrots 33 Jennifer Graham, Timothy F. Wright, Robert J. Dooling, and Ruediger Korbel

05 Social Behavior of Psittacine 43 Lynne M. Seibert

06 Captive Parrot Nutrition: Interactions with Anatomy, Physiology, and Behavior 49 Kevin David Matson and Elizabeth A. Koutsos

07 Comfort Behavior and Sleep 59 Laurie Bergman and Ulrike S. Reinisch

08 Parrot Reproductive Behavior, or Who Associates, Who Mates, and Who Cares? 63 Tracey R. Spoon

09 Nest Box Preferences 79 Scott George Martin and April Romagnano

10 Hand-Rearing: Behavioral Impacts and Implications for Captive Parrot Welfare 83 Rebecca Fox

11 Behavioral Development of Psittacine Companions: Neonates, Neophytes, and Fledglings 93 Phoebe Greene Linden with Andrew U. Luescher

12 Handler Attitude and Chick Development 113 Brenda Cramton

v vi Contents

13 Grey Parrot Cognition and Communication 133 Irene M. Pepperberg

14 Behavior Analysis and Parrot Learning 147 S.G. Friedman, Steve Martin, and Bobbi Brinker

15 Behavior Classes in the Veterinary Hospital: Preventing Problems Before They Start 165 Kenneth R. Welle

16 Clinical Evaluation of Psittacine Behavioral Disorders 175 Kenneth R. Welle and Liz Wilson

17 Diagnostic Workup of Suspected Behavioral Problems 195 Susan E. Orosz

18 Aggressive Behavior in Pet Birds 211 Kenneth R. Welle and Andrew U. Luescher

19 Parrot Vocalization 219 Laurie Bergman and Ulrike S. Reinisch

20 Parrots and Fear 225 Liz Wilson and Andrew U. Luescher

21 Problem Sexual Behaviors of Companion Parrots 233 Fern Van Sant

Color Plates

22 Mate Trauma 247 April Romagnano

23 Feather-Picking Disorder in Pet Birds 255 Lynne M. Seibert

24 Psittacine Behavioral Pharmacotherapy 267 Kenneth M. Martin

25 Behavior of Captive Psittacids in the Breeding Aviary 281 G. Heather Wilson

26 Housing and Management Considerations for Problem Prevention 291 Andrew U. Luescher and Liz Wilson

27 Captive Parrot Welfare 301 Cheryl Meehan and Joy Mench

Index 319 Contributors

Numbers in brackets refer to chapters

Laurie Bergman, VMD, DACVB [7,19] Ruediger Korbel, Prof. Dr. med. vet., Dr. med. Co-ordinator Clinical Animal Behavior Service vet. habil. [4] University of California Veterinary Medical Director Institute of Avian Diseases, Ludwig- Center, San Diego Maximilians-University Munich Cert. Spec. Avian Medicine, Cert. Spec. Vet. Bobbi Brinker [14] Ophthalmol., Dipl. ECAMS. Univ.–Institut Parrottalk.com fuer Gefluegelkrankheiten

Brenda Cramton, MS, JD [12] Elizabeth A. Koutsos [6] Arroyo Veterinary Hospital Department of Animal Science Denair, CA University of Missouri, Saint Louis

Robert J. Dooling, PhD [4] Phoebe Greene Linden, MA [11] Department of Psychology Santa Barbara Farm University of Maryland, College Park Santa Barbara, CA

Ernesto C. Enkerlin-Hoeflich [2] Andrew U. Luescher, DVM, PhD, DACVB www.conanp.gob.mx/ [Editor, 11,18,20,26] Director of the Animal Behavior Clinic Rebecca Fox [10] Purdue University, West Lafayette, IN Department of Animal Science University of California, Davis Kenneth M. Martin, DVM [24] Veterinary Behavior Consultations S.G. Friedman, PhD [14] New Orleans, LA Department of Psychology Utah State University, Logan Scott George Martin, MS, DVM [9] Animal Health Clinic Jennifer Graham, DVM, Diplomate, ABVP, Jupiter, FL Avian [4] Affiliate Assistant Professor, Department of Steve Martin [14] Comparative Medicine,School of Medicine, Natural Encounters, Inc. University of Washington Winter Haven, FL Veterinary Specialty Center of Seattle, Lynnwood, WA Kevin David Matson [6] www.seattleveterinaryspecialists.com Department of Biology University of Missouri, St. Louis Dominique G. Homberger [1] Professor of Zoology, Dept. of Biological Cheryl Meehan, PhD [27] Sciences Associate Director, Center for Animal Welfare Louisiana State University, Baton Rouge University of California, Davis

vii viii Contributors

Joy Mench [27] Tracey R. Spoon [8] Professor and Director of the Center for Animal Department of Biology Welfare, Department of Animal Science University of Massachusetts, Boston University of California, Davis Fern Van Sant, DVM [21] Charles A. Munn, PhD [3] For the Birds Chairman of the Board, Tropical Nature San Jose, CA Arlington, VA www.tropicalnature.org Kenneth R. Welle, DVM, Diplomate, ABVP, Avian [15, 16, 18] Susan E. Orosz, PhD, DVM, Diplomate, All Creatures Animal Hospital ABVP,Avian, and Diplomate, ECAMS [17] Adjunct Assistant Professor, University of Perrysburg Animal Care, Perrysburg, Ohio Illinois College of Veterinary Medicine Adjunct Professor, The University of Tennessee, Urbana, IL College of Veterinary Medicine, Knoxville Consultant, Lafeber Company, Cornell, Illinois James W.Wiley [2] USGS-BRD Irene M. Pepperberg [13] Maryland Cooperative Fish and Wildlife Research Associate Professor, Dept. of Research Unit, Princess Anne, MD Psychology, Brandeis University Research Scientist, MIT School of Architecture G. Heather Wilson, DVM, Diplomate, ABVP, and Planning Avian [25] Assistant Professor Exotic Animal, Wildlife, and Ulrike S. Reinisch, DVM [7,19] Zoological Medicine, Department of Small Resident–Clinical Animal Behavior Service Animal Medicine, College of Veterinary University of California, Davis Medicine University of Georgia, Athens April Romagnano, PhD, DVM, ABVP (Avian Practice) [9,22] Liz Wilson, CVT [16,20,26] Animal Health Clinic Parrot Behavior Consultant Jupiter, FL Levittown, PA

Lynne M. Seibert, DVM, MS, PhD, Dipl Timothy F.Wright, PhD [4] ACVB [5,23] Genetics Lab, National Museum of Natural Veterinary Specialty Center of Seattle History, Smithsonian Institution, Smithsonian Lynnwood, WA National Zoo Washington, DC Noel F.R. Snyder [2] Portal, AZ Many have forgotten this truth, but you must not forget it. You remain responsible, forever, for what you have tamed. —Antoine de Saint-Exupery Preface

The untamed beauty of parrots has fascinated neglected, covered with a towel to keep them humans for centuries and keeps us in its spell to quiet, are much too common. Even normal parrot the present time. Parrots are beautiful, they can behavior such as vocalization, chewing, and being fly, they are different from us, they are intelligent, messy does not fit well with people’s lifestyles and they remain mysterious. However, our rela- and can result in a broken human-animal bond. tionship with parrots has changed greatly over This book is written by authors who understand time. Once considered a plentiful natural resource and love parrots in order to help foster a mutual- worth exploiting, we now make great efforts to ly beneficial and enjoyable relationship between protect their dwindling natural populations. At the parrots and their humans. We hope it can set up same time we have come a long way in how we new parrot-human relationships for success and keep parrots in our homes. They no longer are but rekindle the joy that should be inherent in such brilliant exhibition pieces chained to a T-stand but relationships in cases where it has been lost. We have become members of our families whose sen- intend to promote a deepened understanding and sitivities, cognitive abilities, and emotions we responsible attitude toward parrots in the wild as respect and try to understand. well as in captivity. We hope this will contribute Yet parrot-keeping is a challenging endeavor. to the welfare of parrots and help develop a We admire their wildness, yet we bring them into respect for and appreciation of these fascinating a very unnatural captive environment for which beings. they have not evolved. We admire their flight, yet Although scientific interest in parrot behavior in most cases where we keep parrots as pets we is growing, knowledge in this area is still limited. need to clip their wings. We like them because This is especially true for behavior problems of they are social creatures, yet we frequently keep pet birds and their treatment. The information in them as solitary birds so they will redirect their this book is based on scientific principles and affection toward us, and in most cases we leave available publications but, where specific and them alone for extended periods of time. We rec- proven information is not available, may reflect ognize their intelligence, yet maintain them in a the opinion and the personal experience of the very restricted and confining environment. authors. Therefore, there may be some degree of No wonder behavior problems in parrots are contradiction or difference in interpretation plentiful and the numbers of abandoned parrots between chapters. This inconsistency was inten- ending up in sanctuaries is increasing. Stories of tionally maintained to offer the reader different parrots relegated to small cages in the basement, perspectives.

ix

Manual of Parrot Behavior

1 Classification and Status of Wild Populations of Parrots

Dominique G. Homberger

THE ORDER PSITTACIFORMES AND ITS ous avian orders. For example, in the curved beak RELATIONSHIPS WITHIN THE CLASS of owls (Strigiformes) and raptors (Falconi- AVES formes), the mandible points straight forward, and The roughly 350 in about 74 genera of the hooked maxilla serves to get a grip when parrots and (Forshaw 1989; Collar grabbing or tearing apart prey. In the zygodactyl 1997; Rowley 1997; Juniper & Parr 1998) are feet of woodpeckers (Piciformes) and cuckoos grouped within the Psittaciformes, one of the (Cuculiformes), the limb musculature differs most distinctive and largest of the 28 avian orders from that of Psittaciformes, and the scaly skin dif- (Brooke & Birkhead 1991). Parrot and fers in the shape and number of the scales. These species are usually easily recognized as psittaci- differences indicate that the zygodactyl feet form (or “psittacine”) birds because of their reflect an adaptation to an arboricole lifestyle, curved beaks, in which the tip of the maxilla proj- which has evolved separately in the ancestors of ects beyond the shorter mandible, and their zygo- each order, rather than one that has evolved in a dactylous feet, in which the second and third toes common ancestor of all three orders. point forward and oppose the first and fourth toes, which point caudally. Other characteristics THE EVOLUTIONARY ORIGIN OF include a usually colorful plumage; a very large PSITTACIFORMES brain; curiosity, lifelong capacity for learning, The evolutionary origin of the Psittaciformes can and adaptability to changing environmental con- be reconstructed from a combination of function- ditions; distinctive vocalizations; a feeding ecolo- al morphological, ecological, phylogenetic, bio- gy as seed predators; versatile feeding mecha- geographical, geological, and paleoecological nisms; a complex social behavior; lifelong pair data (Cracraft 2001; Homberger 1991, 2003). The bonding; nesting in cavities; white eggshells; and zygodactylous feet that are especially adept at nidicolous young. climbing tree trunks and the predominant nesting In the past, there have been some attempts at in tree cavities suggest that the Psittaciformes identifying the avian orders that are most closely originated as forest birds. The white color of the related to the Psittaciformes by looking for com- eggshells indicates that the ancestral species incu- mon features, but it has become clear that any bated their eggs in cavities (probably of trees), such commonalities reflect traits that have where they would not need camouflaging color evolved in adaptation to similar environmental pattern to escape the attention of predators. conditions and not traits that have been retained The functional morphology of their feeding from a common ancestor. Furthermore, most of apparatus provides additional support for a the common features at the ordinal level resemble psittaciform origin from an ancestor that was one another only superficially and are easily rec- adapted to living in forests (Homberger 2003). ognized as having evolved independently in vari- The quadratomandibular, or jaw, joint is uniquely

3 4 Manual of Parrot Behavior shaped to allow lateral movements of the lower may have originated in a psittaciform ancestor mandible relative to the upper maxilla. However, first to extract wood-boring or gallicole insect lar- parrots and most cockatoos, such as the White vae and subsequently been applied with few, if and Pink Cockatoos ( spp., Eolophus any, modifications, to extract seeds from fibrous- roseicapillus, Lophochroa leadbeateri, Plictolo- woody fruits. phus spp.), the (Nymphicus hollandi- In the “psittacid” feeding apparatus of parrots cus), the Yellow-tailed and White-tailed Black and most cockatoos (except the Red-tailed Black Cockatoos ( [Zanda]), and the Cockatoos, Calyptorhynchus lathami and most (Probosciger aterrimus), use this C. banksii subspecies, and the Gang-gang capacity only during bouts of bill honing and for Cockatoo, Callocephalon fimbriatum), in con- minor adjustments when positioning food items trast, the structure and function of the jaw joint between their mandible to bite into them. It is does not fit the bill shape and feeding behavior. unlikely, therefore, that the psittaciform jaw artic- The psittacid feeding apparatus relies on special- ulation was evolved in conjunction with the bill ized surface structures, such as the transverse movements observed in these species. It has long step and filing ridges on the inside of the upper been suspected that it was a feature that originat- bill tip, to provide grip for seeds that are cut open ed in a psittaciform ancestor as part of a feeding with the cutting edge of the lower mandible behavior that differed from that which is common (Homberger 1980a, 1980b, 2003). Psittaciforms among extant parrots (Homberger 1981). with a psittacid bill (except the Pesquet’s Parrot, In contrast, the lateral deflection of the lower Psittrichas fulgidus) remove the shells of all mandible is an integral part of the feeding mech- seeds before swallowing them, and they do so anism in most Red-tailed Black Cockatoos with a stereotypical seed-shelling mechanism (Calyptorhynchus banksii subspecies), the Glossy that does not require lateral movement of the (C. lathami), and the Gang-gang mandible. During this seed-shelling procedure, Cockatoo (Callocephalon fimbriatum) (Homber- the tip of the tongue places and holds a seed ger 2001, 2003). They align one of the paired, against the corrugated upper bill tip and its trans- projecting corners of their V-shaped lower bill tip verse step, while the cutting edge of the mandible with their upper bill tip. They do this in order to cuts open the seed-shell. The bony suborbital use their beak as pincer-like pliers to tear apart arch is generally absent so that the transverse woody branches to extricate wood-boring or component of the jaw muscles is much reduced gallicole insect larvae or to break apart woody- in favor of the longitudinal and vertical force fibrous capsules to extract seeds (Homberger components. If a suborbital arch is present, as in 2001, 2003). These species also possess a bony many South American species, it is less massive suborbital arch that juts out on the sides of their and fused only with the postorbital process of the skull and is firmly buttressed against the postor- cranium (see Smith 1975). This functional disso- bital and zygomatic processes of the cranium. The ciation of the various structural and functional jaw muscles that attach to this suborbital arch features indicates that the shapes of the jaw joint, assume an orientation that emphasizes transverse- skull, and bill of parrots and cockatoos with a ly directed force components, which are instru- psittacid feeding apparatus have changed under mental for the lateral deflections of the mandible the influence of a variety of selective regimes during feeding in these species. In this “calyp- arising from environmental conditions that differ torhynchid” feeding apparatus, the shapes of the from those to which the psittaciform ancestor jaw joint, skull, and bill are structurally and func- was adapted. tionally integrated with the feeding mechanism to The most significant selective advantage of the tear apart food sources that are made of fibrous psittacid feeding apparatus over the calyp- wood, which are prevalent in a wooded or forested torhynchid feeding apparatus is that the former environment (Homberger 2003). The tight func- can use both sides of the jaw musculature simul- tional integration of the features of the calyp- taneously to maximize the bite force of the man- torhynchid feeding apparatus also indicates that dible. This selective advantage, however, can be they are part of an ancestral condition for Psittaci- utilized only in environments in which plants with formes. The calyptorhynchid feeding apparatus seeds enclosed in fruits that are not woody- 1 / Classification and Status of Wild Populations of Parrots 5 fibrous predominate (Homberger 2003). Most of through the disintegration of the Mesozoic south- these fruits have a sclerotic endocarp (i.e., ern continent called Gondwana and their subse- “stone”) that can be split, or cracked open, by quent migration northward toward the equator applying a focused pressure, such as by the cut- (Frakes & Vickers-Rich 1991; Schodde & ting edge of the mandible, onto their preformed Tidemann 1986; Stevens 1991). weak points or sutures that facilitate the germina- Gondwana’s climate in the Cretaceous was tion of the seeds. The selective advantage of a generally temperate to subtropical, and Gond- psittacid feeding apparatus appears to be consid- wana itself was covered mostly with evergreen erable because it has evolved multiple times in mesic forest and rain forest (White 1990). As the separate lineages of parrots and cockatoos, continents moved northwards, they tended to including among them some of the populations become more arid with the rising temperatures and subspecies of Red-tailed Black Cockatoos (Frakes & Vickers-Rich 1991; Stevens 1991; (Calyptorhynchus banksii). This convergent evo- White 1994). The original plant communities that lution of the psittacid feeding apparatus is made included southern gymnosperms (e.g., Arau- evident by the great variability of the individual caria), Casuarinas, Proteaceae (e.g., Banksia, components and features, such as the pattern and Protea, Grevillea), Myrtaceae (e.g., ancestors of configuration of the filing ridges and corneous Eucalyptus), Podocarpaceae, Nothofagaceae palate, the shape and expression of the transverse (e.g., Southern beeches—Nothofagus), and so step, the shape of the cutting edge of the forth, adapted to the changing conditions, were mandible, and the configuration and degree of the replaced by other plant communities, or retreated reduction of the suborbital arch (Homberger to refugia in which the original Gondwanan con- 1980a, 1980b, 2003). ditions were retained or changed but little. Such The large brain of the Psittaciformes earned Gondwanan refugia are found today in Australia them the epithet “avian primates.” As in primates, along its eastern coast, the southeastern and it is correlated with curiosity and exploratory southwestern corners, and in Tasmania; in New behaviors and a lifelong capacity for learning Zealand, New Caledonia, and Fiji; in the central (e.g., Mettke-Hofmann et al. 2002; Pepperberg highlands of New Guinea; in the Drakensbergs of 2002). This high degree of encephalization sup- eastern South Africa; and in the Valdivian and ports the hypothesis that the Psittaciformes origi- Patagonian rain forests along the eastern coast of nated from ancestors that were feeding on station- southern South America and the cooler Atlantic ary food items that were hidden from sight (i.e., rain forests in Southern Brazil. wood-boring or gallicole insect larvae and seeds In Australia, several of these seed plants (e.g., within fruits) and, therefore, need to be located Casuarinas, Proteaceae, Myrtaceae) occur pre- through indirect evidence and learning from dominantly in the Gondwanan refugia (Schodde experienced individuals. These arboreal food & Tidemann 1986) and bear complex inflores- items further support the hypothesis that Psit- cences that mature into multi-seeded, fibrous- taciformes originated in a forested environment. woody infructescences, called cones, cobs, or Psittaciformess are concentrated in the conti- capsules. Several species have also become nents and islands of the Southern Hemisphere serotinous (i.e., they retain their mature fibrous- with only limited expansions into the adjacent woody fruits for several years in their canopy northern regions. Contrary to general impres- instead of shedding their mature seeds), presum- sions, Psittaciformes are not restricted to tropical ably in adaptation to their fire-prone environment regions, as several species occur in the colder (Homberger 2003). That the psittaciform species regions of China, New Zealand, New Guinea, that possess a calyptorhynchid feeding apparatus Tasmania, and South America. Such a distribu- (most Red-tailed Black Cockatoos, Calyptorhyn- tion pattern can be understood only on the basis chus banksii subspecies; the Glossy Black of past geological events. Biogeography has been Cockatoo, C. lathami; and the Gang-gang Cock- suggestive of a psittaciform origin in the atoo, Callocephalon fimbriatum) not only occur Southern Hemisphere (Boetticher 1959; Forshaw in these refugia but also have a feeding apparatus 1989) even before geological data could demon- that is specifically adapted to exploiting these strate that the southern continents were formed plants supports the hypothesis that the calyp- 6 Manual of Parrot Behavior torhynchid feeding apparatus is the ancestral con- hypothesis that needs to be tested continuously as dition for Psittaciformes. new data emerge and earlier interpretations are In the other southern continents and islands, re-evaluated in light of new observations. the Gondwanan refugia are dominated by Changes in the nomenclature of taxa and in the Gondwanan plants whose seeds are enclosed in hierarchical levels of taxonomic subdivisions are, thinner seed-shells (e.g., Araucariaceae, Notho- hence, reflective of intense scientific activity but fagaceae, some Podocarpaceae) or sclerotic endo- are not an end in themselves. carps with preformed weak points and sutures Numerous classifications have been proposed (e.g., some Podocarpaceae). The psittaciform over the last 200 years, but all have faced consid- species that feed on these seeds and are restricted erable difficulties. One of the underlying reasons to Gondwanan refugia can be surmised to have for this situation is that the Psittaciformes repre- evolved their psittacid feeding apparatus already sent a very old group that had to adapt to numer- in adaptation to these plants before the breakup of ous environmental changes in the course of its Gondwana and were able to retain it because their long history dating back to the early Tertiary (ca. environment changed little, if at all. This is prob- 60 million years ago). Because similar environ- ably the situation, for example, of the Austral and mental changes (e.g., aridification, tropicaliza- Slender-billed Conures (Enicognathus ferrug- tion, colonization of volcanic islands, etc.) have ineus and E. leptorhynchus) in southern South occurred in different regions, many derived fea- America; the Vinaceous Amazon (Amazona tures have been acquired independently and con- vinacea) in southern Brazil; the Cape Parrot vergently by different psittaciform lineages in (Poicephalus r. robustus) in southeastern Africa; adaptation to these new environments. This preva- and the non-cacatuid psittaciforms with a psit- lence of convergent (i.e., homoplastic) features tacid feeding apparatus in the Australo-Pacific among the Psittaciformes as a group has ham- region. pered earlier efforts in classifying this avian The greatest diversity of Psittaciformes at the order, mainly because many convergent and other familial and subfamilial levels is found in the non-homologous features have been misidenti- Australo-Pacific region (see Figure 1.1). This fied as homologous ones that would indicate evo- indicates that this part of Gondwana may have lutionary relationships (for discussions, see contained the greatest psittaciform diversity even Homberger 1980a, 1991; Güntert 1981). before its separation from the remainder of The distinction between homologous and con- Gondwana and further breakup into what is vergent features is one of the most challenging known today as Australia, New Guinea, New tasks for evolutionary biologists, because the first Zealand, New Caledonia, and Fiji. step in this procedure requires the analysis of both the structure and function of the features, as well THE SUBDIVISION AND as their biological role in the natural environment. CLASSIFICATION OF THE Two examples will illustrate the basic approach. PSITTACIFORMES The first example will use the bony suborbital The very ease with which psittaciforms can be arch to demonstrate the possible pitfalls in ana- identified as such is compensated by the difficul- lyzing features in isolation. A recent functional- ties that are encountered trying to subdivide this anatomical analysis of the bony suborbital arch in large order into smaller, hierarchically arranged cockatoos revealed that it is a component of the taxonomic units that are united by common char- feeding apparatus and as such cannot be used as a acteristics (i.e., families, subfamilies, tribes, gen- feature in isolation. It also revealed that its most era). Such a classification creates order within the complete configuration is intimately connected multitude of species, which is needed for scientif- with lateral mandibular movements during feed- ic research (e.g., systematics, comparative mor- ing in Black Cockatoos that possess a calyptor- phology, evolutionary biology) and applied biolo- hynchid feeding apparatus. Various configu- gy (e.g., evaluation of susceptibility to certain rations of less complete suborbital arches in diseases, choice of foster parents for the manage- different psittaciform lineages that possess a psit- ment of endangered species). However, it must be tacid feeding apparatus can, therefore, be inter- kept in mind that every classification is only a preted as derived remnants of the ancestral condi- Figure 1.1. Phylogram of psit- taciform genera based conserva- tively on established criteria.

7 8 Manual of Parrot Behavior tion that is still present in psittaciforms with a taken from the Cacatuidae may illustrate such a calyptorhynchid feeding apparatus. This reinter- case. Among birds in general, a large body size is pretation of the evolutionary history of the bony a derived character, because flight has a much suborbital arch is contrary to the original inter- greater safety margin in small birds than in larger pretation by Hofer (1950, 1953) and Zusi (1993), birds and, therefore, has probably originated in both of whom did not have access to observations small avian ancestors whose flight apparatus may of psittaciforms in their natural environment. not have been perfected yet (Homberger & de The second example will use the oral plate of Silva 2000; Homberger 2003). According to this the upper rhamphotheca (i.e., corneous sheath of criterion, the Cockatiel (Nymphicus hollandicus) the maxilla) to demonstrate that a particular struc- could be considered the most ancestral cockatoo. ture may be composed of several features that This interpretation could be supported by its dark provide different insights for the reconstruction of plumage color and pattern, which are similar to the evolutionary history of the Psittaciformes. those of the Black Cockatoos (Calyptorhynchus The oral plate of the upper rhamphotheca consists spp.) and clearly more ancestral than the plumage of three parts: The inside of the upper bill tip, the colors and patterns of the White and Pink transverse step, and the corneous palate. The Cockatoos. But the Cockatiel’s psittacid feeding inside of the upper bill tip of parrots that possess apparatus and its ecology in Australia’s more arid a psittacid feeding apparatus is corrugated by fil- woodlands indicate that it has also acquired ing ridges. These filing ridges, however, are derived characters in adaptation to the aridifica- arranged in patterns and are formed by the under- tion of Australia. In contrast, the Red-tailed Black lying soft tissues in a manner that is highly vari- Cockatoos and the Gang-gang Cockatoo are char- able among, but generally characteristic of, acterized by ancestral plumage colors and pat- species. The inside of the upper bill tip of psittaci- terns and by the ancestral calyptorhynchid feed- forms that possess a calyptorhynchid feeding ap- ing apparatus. At the same time, the Red-tailed paratus is smooth and lacks any surface structure Black Cockatoos are among the larger cockatoos, (Homberger 2003). The evolutionary transition whose body size may have evolved in conjunction from the ancestral to the derived condition of the with their more massive bills to handle their diet inside of the upper bill tip is modeled by the var- of large fibrous-woody fruits (Homberger 2003). ious populations and subspecies of the Red-tailed At this point in time, the best classification of Black Cockatoo (Calyptorhynchus banksii) and is the Psittaciformes may be one that is based on a clearly correlated with the derived seed-shelling large number of features, whose biological and behavior of psittaciforms with a psittacid feeding evolutionary significance has been analyzed and apparatus (Homberger 2003). In contrast, the sur- is well understood. Unfortunately, we are still far face structure of the corneous palate, which is the from this goal. The proposed classification (see feature with the greatest diagnostic value for the Figure 1.1) is presented as a pragmatic proposal identification of genera in psittaciforms, does not that combines simplicity and familiarity and have any functional significance (Homberger avoids some of the errors of earlier classifications. 1980a). Mosaic evolution, that is, the presence of prim- THE STATUS OF WILD POPULATIONS itive and derived characters in a single species as OF PARROTS a result of asynchronous evolutionary changes, Over the millions of years since their origin in the has been another source of difficulties for the early Tertiary, many psittaciform species have classification of the Psittaciformes. Because of it, survived and continued to adapt successfully to a phylogeny that is based on a particular set of changing environmental conditions, as we can features, such as the feeding apparatus, may not conclude from their present geographical distri- simply correspond to another phylogeny that is bution and the number of existing species and based on a different set of features. As a conse- individuals. Other species have not been able to quence, the evolutionary history of each lineage do so and have become extinct, as we know from and species needs to be reconstructed by careful- historical records or from fossils in regions, such ly analyzing, weighing, and integrating a variety as Europe, in which psittaciforms have been of data and observations. A simplified example absent in historical times. Rates of extinction are 1 / Classification and Status of Wild Populations of Parrots 9 difficult to estimate from the fossil record, transported to colonies in North America, because fossilization is a rare event in any case Australia, and New Zealand by homesick Euro- and especially so for organisms, such as the an- pean emigrants, the successful psittaciform expa- cestral and many other Psittaciformes, that are triate populations in Germany, England, and relatively small and live in microorganism-rich North America may eventually become genetical- forest environments with their characteristically ly distinct from their source populations. But rapid degradation of organic materials. Neverthe- modifications of external features will take many less, the large number of species that are known generations to become noticeable, as they did in to have existed at least until the more recent rash the various domesticated psittaciforms, and these of extinctions testifies to the success and proba- changes may reflect adaptations to the new envi- bly net increase in number of species and individ- ronments or the lack of specific selection pres- uals of the Psittaciformes over the course of their sures (e.g., in cases of variable plumage colors), evolutionary history. unless these mostly urban populations will be Although extinctions of species are a normal repeatedly swamped by new escapees and acci- part of biological evolution, extinction must be dental releases. The possibility of such artificial counterbalanced by speciation, that is, the appear- speciation events may be a consolation, but hard- ance of new species, if a taxon, or group of ly a compensation for the current progressive loss species, as a whole is to survive. The appearance of the amazing diversity of psittaciform species in of new species, however, is presently not occur- their natural environment. ring any longer, at least not naturally. This process There is no denying that the single-most threat normally starts when a certain portion of a popu- to natural populations is the capture of individu- lation becomes separated from the rest of the pop- als for aviculture and the pet market. Captive ulation by the appearance of a geographical barri- breeding of parrots by private individuals for con- er, such as a river having changed direction, an servation purposes should be recognized as the area having been divided by the uplifting of a smoke screen that it is (Beissinger et al. 1991; mountain or the formation of a desert, or a num- Beissinger 2001; Snyder et al. 1997; Wright et al. ber of individuals having migrated permanently 2001). Only a single psittaciform species, the to an island. This separation, or isolation, pre- Puerto Rican Amazon (Amazona vittata) (Wilson vents the exchange of genetic materials between et al. 1994, Wunderle et al. 2003) has been the separate populations and provides the condi- brought back from the brink of extinction, which tions for the two populations to accumulate dis- was made possible only through the lavish invest- tinctive mutations, undergo distinctive selective ment of governmental funding. The success of processes, and, thereby, acquire distinctive traits other governmental rescue programs for the Kaka simply by themselves or in adaptation to distinct (Nestor meridionalis) and Kakapo (Strigops environmental conditions. habroptilus) in New Zealand (Beggs & Wilson The main reason for natural speciation not to 1991; Lloyd & Powlesland 1994) and the Orange- be initiated any longer is the accelerating and bellied Parrot (Neophema chrysogaster) in well-documented shrinking of the natural habi- Australia (Drechsler 1998) is still uncertain. Such tats, so that psittaciform populations cannot massive financial investments for the rescue of expand and subsequently be subdivided into non- single species are beyond the possibilities of even interbreeding populations. However, the recent very wealthy persons. Furthermore, although successful establishment of self-sustaining parrot there have been successful reintroductions of cap- populations from aviary and transport escapees in tive individuals into the wild provided that these various urban and suburban places in regions that could be integrated with natural populations of had been devoid of natural populations of the same species (Brightsmith et al. 2003), simple psittaciforms may be considered an experiment in releases of captive-bred psittaciforms into natural human-induced speciation. As we can extrapolate environments, whose resources are characteristi- from earlier such experiments in the late 18th and cally seasonal and unpredictable, have not been early 19th centuries, during which European successful (Snyder et al. 1994). The reason for songbirds (e.g., House Sparrows, Starlings, Chaf- these difficulties may well be based in the evolu- finches, Blackbirds, European Goldfinches) were tionary origin of the Psittaciformes with their spe- 10 Manual of Parrot Behavior cialized diet of wood-boring and gallicole insect of Australasia, ed. P. Vickers-Rich, J.M. Monghan, larvae, which could be detected only through R.F. Baird, and T.H. Tich, pp. 111–146. Melbourne: indirect evidence and through learning from Monash University Publications Committee. experienced individuals. Güntert, M. 1981. Morphologische Untersuchungen zur adaptiven Radiation des Verdauungstraktes bei ACKNOWLEDGMENTS Papageien (Psittaci). Zool Jahrb Anat 106:471–526. Hofer, H. 1950. Zur Morphologie der Kiefermusku- I thank Andrew Luescher for his kind invitation to latur der Vögel. Zool Jahrb Anat 70 (4):427–556. contribute to this volume and his excellent editor- Hofer, H. 1953. Die Kiefermuskulatur der Papageien ship. I also thank David Ray for designing the als Evolutionsproblem. Biol Zentralbl 62 (5/6): phylogram. 225–232. Homberger, D.G. 1980a. Funktionell morphologische REFERENCES Untersuchungen zur Radiation der Ernährungs und Beggs, J.R., and P.R. Wilson. 1991. The kaka Nestor Trinkmethoden der Papageien (Psittacidae). [Func- meridionalis, a New Zealand parrot endangered by tional morphological studies on the radiation of the introduced wasps and mammals. Biol Conserv 56 feeding and drinking methods of the parrots]. Bonner (1):23–38. Zoologische Monographien, No. 13, pp. 192. Beissinger, S.R. 2001. “Trade of live wild birds: Poten- Homberger, D.G. 1980b. “Functional morphology and tials, principles and practices of sustainable use.” In evolution of the feeding apparatus in parrots, with Conservation of exploited species, ed. J.D. special reference to the Pesquet’s Parrot, Psittrichas Reynolds, G.M. Mace, K.H. Redford, and J.G. fulgidus (lesson).” In Conservation of new world Robinson, pp. 182–202. Cambridge: Cambridge parrots, ed. R.F. Pasquier, pp. 471–485. Interna- University Press. tional Council for Bird Preservation Technical Paper Beissinger, S.R., N.F.R. Snyder, S.R. Derrickson, F.C. No. 1. Washington, DC: Smithsonian Institution James, F.C., and S.M. Lanyon, S.M. 1991. Interna- Press. tional trade in live exotic birds creates a vast move- Homberger, D.G. 1981. Morphological foundations of ment that must be halted. Auk 108 (4):982–984. the bill honing behavior in parrots (Psittacidae). Boetticher, H. von. 1959. Papageien. Wittenberg Amer Zool 21 (4):1039. Lutherstadt, Germany: A. Ziemsen Verlag. Homberger, D.G. 1991. “The evolutionary history of Brightsmith, D., J. Hilburn, A. del Campo, J. Boyd, M. parrots and cockatoos: A model for evolution in the Frisius, R. Frisius, F. Guille, and D. Janik. 2003. Australasian avifauna.” Acta XX Congr Int Ornithol, “Survival and reproduction of hand-raised scarlet pp. 398–403. macaws (Ara macao) in the wild.” In Abstracts of VII Homberger, D.G. 2001. “The case of the cockatoo bill, Neotropical Ornithological Congress, Termas de horse hoof, rhinoceros horn, whale baleen, and Puyehue, Chile: Program and book of abstracts, p. turkey beard: The integument as a model system 106. Chile: Neotropical Ornithological Society. to explore the concepts of homology and non- Brooke, M., and T. Birkhead. 1991. The Cambridge homology.” In Vertebrate functional morphology: encyclopedia of ornithology. Cambridge: Cam- Horizon of research in the 21st century, ed. H.M. bridge University Press. Dutta and J.S. Datta Munshi, pp. 317–343. Enfield, Collar, N.J. 1997. “Family Psittacidae (parrots).” In NH: Science Publishers Inc. Handbook of the birds of the world. Volume 4: Homberger, D.G. 2003. “The comparative biomechan- Sandgrouse to cuckoos, ed. J. del Hoyo, A. Elliott, ics of a prey-predator relationship: The adaptive and J. Sargatal, pp. 280–477. Barcelona: Lynx morphologies of the feeding apparatus of Australian Edicions. black cockatoos and their foods as a basis for the Cracraft, J. 2001. Avian evolution, Gondwana biogeog- reconstruction of the evolutionary history of the raphy and the Cretaceous-Tertiary mass extinction Psittaciformes.” In Vertebrate biomechanics and event. Proc R Soc Lond B 268 (1466):459–469. evolution, ed. V.L. Bels, J.-P. Gasc, and A. Casinos, Drechsler, M. 1998. Spatial conservation management pp. 203–228. Oxford: BIOS Scientific Publishers. of the orange-bellied parrot Neophema chryso- Homberger, D.G., and K.N. de Silva. 2000. Functional gaster. Biol Conserv 84 (3):283–292. microanatomy of the feather-bearing avian integu- Forshaw, J.M. 1989. Parrots of the world, 3rd ed. Mel- ment: Implications for the evolution of birds and bourne: Lansdowne Editions. avian flight. Amer Zool 40 (4):553–574. Frakes, L.A., and P. Vickers-Rich. 1991. “Palaeocli- Juniper, T., and M. Parr. 1998. Parrots: A guide to par- matic setting and palaeogeographic links of Austra- rots of the world. New Haven: Yale University Press. lia in the Phanerozoic.” In Vertebrate palaeontology Lloyd, B.D., and R.G. Powlesland. 1994. The decline of 1 / Classification and Status of Wild Populations of Parrots 11

the kakapo Strigops habroptilus and attempts at con- White, M.E. 1994. After the greening: The browning of servation by translocation. Biol Conserv 69:75–85. Australia. Kenthurst, NSW: Kangaroo Press. Mettke-Hofmann, C., H. Winkler, and B. Leisler. 2002. Wilson, M.H., C.B. Kepler, N.F.R. Snyder, S.R. The significance of ecological factors for explo- Derrickson, F.J. Dein, J.W. Wiley, J.M. Wunderle, ration and neophobia in parrots. Ethology 108 A.E. Lugo, D.L. Graham, and W.D. Toone. 1994. (3):249–272. Puerto Rican parrots and potential limitations of the Pepperberg, I.M. 2002. Alex studies: Cognitive and metapopulation approach to species conservation. communicative abilities of grey parrots. Cambridge, Conserv Biol 8 (1):114–123. MA: Harvard University Press. Wright, T.F., C.A. Toft, E. Enkerlin-Hoeflich, J. Rowley, I. 1997. “Family Cacatuidae (cockatoos).” In Gonzalez-Elizondo, M. Albornoz, A. Rodríguez- Handbook of the birds of the world. Volume 4: Sand- Ferraro, F. Rojas-Suárez, V. Sanz, A. Trujillo, S.R. grouse to cuckoos, ed. J. del Hoyo, A. Elliott, and J. Beissinger, V. Berovides A., X. Gálvez A., A.T. Sargatal, pp. 246–279. Barcelona: Lynx Edicions. Brice, K. Joyner, J. Eberhard, J. Gilardi, S.E. Koenig, Schodde, R., and S.C. Tidemann. 1986. Reader’s S. Stoleson, P. Martuscelli, J.M. Meyers, K. Renton, Digest complete book of Australian birds. Sydney: A.M. Rodríguez, A.C. Sosa-Asanza, F. Vilella, and Reader’s Digest. J.W. Wiley. 2001. Nest poaching in Neotropical par- Smith, G.A. 1975. Systematics of parrots. Ibis rots. Conserv Biol 15:710–720. 117:18–68. Wunderle, J.M., Jr., N.F. Snyder, S.R. Beissinger, J.M. Snyder, N.F.R., S.R. Derrickson, S.R. Beissinger, J.W. Meyers, and J.W. Wiley. 2003. “Struggling out of the Wiley, T.B. Smith, W.D. Toone, and B. Miller. 1997. bottleneck: Puerto Rican parrot recovery from 1973 Limitations of captive breeding: Reply to Gippoliti to 2000.” In VII Neotropical Ornithological Con- and Carpaneto. Conserv Biol 11 (3):808–810. gress, Termas de Puyehue—Chile, October 5–11, Snyder, N.F.R., S.E. Koenig, J. Koschmann, H.A. Sny- 2003: Program and book of abstracts, p. 155. Chile: der, and T.B. Johnson. 1994. Thick-billed parrot Neotropical Ornithological Society. releases in Arizona. Condor 96:845–862. Zusi, R.L. 1993. “Pattern of diversity in the avian Stevens, G.R. 1991. “Geological evolution and biotic skull.” In The skull. Volume 2: Patterns of structural links in the Mesozoic and Cenozoic of the southwest and systematic diversity, ed. J. Hanken and B.K. Pacific.” Acta XX Congr Int Ornithol, pp. 361–382. Hall, pp. 391–437. Chicago: University of Chicago White, M.E. 1990. The flowering of Gondwana; The Press. 400 million year story of Australia’s plants. Prince- ton: Princeton University Press.

2 Behavior of Wild Amazona and Rhynchopsitta Parrots, with Comparative Insights from Other Psittacines

Ernesto C. Enkerlin-Hoeflich, Noel F.R. Snyder, and James W. Wiley

Research on the behavioral characteristics of on intensive studies of (1) the Puerto Rican Parrot selected wild psittacines may be important in es- (Amazona vittata) by Snyder et al. (1987); (2) tablishing management and conservation guide- various subspecies of the Cuban Parrot (Amazona lines for these species, both in the wild and in leucocephala) by Gnam (1991), Wiley (unpub- captivity. An understanding of such behavioral lished), and others; (3) the Hispaniolan Parrot characteristics may also have wider significance (Amazona ventralis) by Wiley (unpublished); (4) in aiding the interpretations of behavioral and the Jamaican Black-billed and Yellow-billed natural history parameters in other psittacine Parrots (Amazona agilis and collaria) by Koenig birds. Prior to the 1970s, intensive biological (1999); (5) the St. Lucia Parrot (Amazona versi- studies of wild Neotropical parrots were nearly color), the Imperial Parrot (Amazona imperialis), nonexistent. This gap in ornithological knowl- the Red-necked Parrots (Amazona arausiaca) of edge is now being rapidly remedied with numer- the Lesser Antilles by Snyder, Koenig, and many ous species under investigation throughout Cen- others (unpublished); and (6) three species of tral and South America and the West Indies. Yet amazons in northeastern Mexico by Enkerlin- to date there have been few attempts to integrate Hoeflich (1995, unpublished)—the Red-crowned the information from various studies into coher- Parrot (Amazona viridigenalis), the Yellow- ent frameworks of biological understanding. In headed Parrot (Amazona oratrix), and the Red- this offering, we provide a number of preliminary lored Parrot (Amazona autumnalis). Studies of hypotheses about parrot behavior, based largely Rhynchopsitta pachyrhyncha and terrisi have on studies of a variety of species, mainly in the been primarily carried out by Enkerlin-Hoeflich genera Amazona and Rhynchopsitta. These hy- (unpublished), Cruz-Nieto et al. (1998), Snyder et potheses appear to have wide explanatory power, al. (1999), Lanning and Shiflett (1981, 1983), and yet need to be tested in additional genera and Lawson and Lanning (1982). species before their validity can be considered The particular behavioral features we consider firm. here are (1) the values of intraspecific sociality in Our basic approach is the comparative one, various species, (2) timing of nesting seasons, (3) looking at features of behavior that vary among site and pair fidelity, and nest reuse, (4) feeding species and attempting to correlate these differ- behavior and rates, (5) relationships of species ences with underlying ecological imperatives conspicuousness and nest accessibility to exploi- faced by the species under consideration. As raw tation in the pet trade, and (6) deficits in breeding materials for these comparisons, we rely heavily effort.

13 14 Manual of Parrot Behavior

BACKGROUND parrots are distinct species and not simply races As generally understood, the Amazona of a single species, as they were considered by includes 31 extant species limited largely to trop- Forshaw (1990). ical areas of the Western Hemisphere. The various VALUES OF SOCIALITY AMONG species occur from Argentina and Chile north AMAZONA AND RHYNCHOPSITTA through virtually all of mainland South America PARROTS and Central America to northern Mexico (Juniper & Parr 1998). Feral populations of several species In general, Amazona parrots tend to be highly also exist in a number of southern cities of the social in foraging and roosting habits and some- United States, Mexico, and Puerto Rico what social in nesting habits, but some conspicu- (Enkerlin-Hoeflich & Hogan 1997; Mabb 1997). ous differences exist among species in these The West Indies have a particularly good tendencies. Four species that stand out in their dis- Amazona fauna with nine extant species about inclination to travel in groups larger than family evenly divided between the Greater Antilles and groups are the large amazons of the Lesser Lesser Antilles. Many Amazona species are now Antilles—the St. Lucia Parrot, the St. Vincent endangered, and most all are declining, threat- Parrot (A. guildingii), the Imperial Parrot, and the ened mainly by bird trade and habitat changes, Red-necked Parrot. Although these species some- but also in some cases by hunting, introduced times assemble in groups larger than family units exotic species, and other factors (Snyder et al. at roosts and at rich food sources, they normally 2000). The various species of Amazona are far nest in relatively dispersed arrays and travel only from monolithic in their behavior and ecology. as singles, pairs, or small family groups in moving Species vary in clutch and brood sizes, diets, from nests or roosts to foraging areas. In contrast, feeding rates, degrees of sociality, reproductive other amazons, including most of those in the effort, and reproductive success, to name just a Greater Antilles and Mexico, show clear tenden- few facets of interest. cies toward clumped nesting, often travel in much The genus Rhynchopsitta has only two living larger groups, and typically feed in large aggrega- species, both distributed in the highlands of tions. Low sociality in the Lesser Antillean species northern Mexico in more or less “island-like” for- is also reflected in the fact that male and female est habitats. The Thick-billed Parrot (R. pachy- adults often separate in foraging activities in the rhyncha) is a tree-cavity nester inhabiting the breeding season and often feed their young inde- Sierra Madre Occidental in western Chihuahua pendently. Such independent provisioning of nests and eastern Sonora south through the mountains is virtually unknown in amazons of the Greater of Durango, Sinaloa, Nayarit, and Jalisco to Antilles and the mainland Neotropics. Colima and Michoacan. It was also formerly a Are there any obvious ecological correlates to regular inhabitant of extreme southeastern Ari- explain the relatively low sociality of the large zona and probably bred there until the early 20th amazons of the Lesser Antilles? One promising century, although no historical records of nests possibility is the fact that these species, essential- exist for this region. The Maroon-fronted Parrot ly alone among species in the genus, live in habi- (R. terrisi) is a cliff-cavity nester that occurs in tats that are effectively free of predation threats the Sierra Madre Oriental of northeastern Mexico from large raptors. Whereas most Greater Antil- in southeastern Coahuila, central western Nuevo lean amazons and essentially all mainland León, and southwestern Tamaulipas (Juniper & Amazona have to deal with threats from large rap- Parr 1998). Like many of the Amazona, both tors such as Red-tailed Hawks (Buteo jamaicen- extant species of Rhynchopsitta are globally sis), Peregrine Falcons (Falco peregrinus), and threatened. In addition, on the basis of fossils, various Accipiter species, no large accipiters or Rea (1997) recently described a third species of buteos occur in the Lesser Antilles, and the Pere- Rhynchopsitta (R. phillipsi), now extinct, that was grine Falcons of these islands are largely winter- apparently sympatric with both pachyrhyncha and ing birds utilizing coastal areas separate from the terrisi in the Sierra Madre Oriental in the late rain forest habitats occupied by the Lesser Pleistocene. The former sympatry of pachyrhyn- Antillean parrot species. cha and terrisi makes it quite clear that these two The largest raptor in parrot habitats of most of 2 / Behavior of Wild Amazona and Rhynchopsitta Parrots 15 the Lesser Antilles is the Broad-winged Hawk, themselves give strong evidence for the impor- which is too small to represent a credible threat to tance of avian predators in producing social ten- the parrots and for which there are no records of dencies among Amazona parrots. parrot predation. The Red-tailed Hawk, on the We also call attention to the especially well- other hand, is not a species to be underestimated developed sociality of the Thick-billed and in its capacities to take Amazona parrots. Records Maroon-fronted Parrots of Mexico. These Rhyn- exist of it successfully dispatching a variety of chopsitta species are similar to the amazons in Amazona and Rhynchopsitta species in the size and face predation risks from the same sorts Greater Antilles and on the mainland. of avian predators. In particular, these species Thus, to the extent that conspicuous flocking face significant predation threats from both Red- behavior has often been suggested as primarily an tailed Hawks and Peregrine Falcons, and in the adaptation to reduce risks of avian predation, the case of the Thick-billed Parrot, also from Apache Lesser Antillean amazons might be expected to Goshawks (Accipiter gentilis apache). In our gain little by flocking behavior and the tendency experience, sociality in the Rhynchopsitta species may never have evolved or may have disappeared is even more highly developed than in any in the evolutionary history of these species Amazona species for which we have data. In fact, because of very low predation threats. Flocking pairs of the Thick-billed Parrot often nest very behavior has often been envisioned as primarily a close together, sometimes with more than one means to reduce predation via the increased vigi- pair in the same tree, while Maroon-fronted lance possible when the combined sensory capac- Parrots typically nest in dense colonies in cliffs. ities of multiple individuals are available and Moreover, observations indicate that breeding when specific individuals can serve as sentinels males of the Thick-billed Parrot typically associ- for groups (see discussions in Snyder et al. 1987 ate in combined flocks for foraging, often waiting and Yamashita 1987). for one another to leave the nesting areas as a Only one of the Greater Antillean amazons group. Such coordinated male behavior has not shows social behavior similar to that of the Lesser been regularly recorded for any Amazona species. Antillean species, the race of the Cuban Parrot on Other explanations for the flocking and social- Cayman Brac (Amazona leucocephala hesterna). ity of amazon parrots—for example, traditional Like the Lesser Antillean species, the Cayman arguments for advantages in food finding in birds Brac Parrot rarely travels in groups larger than (see Krebs 1974)—have difficulty in accounting family groups, and its male and female adults for the variations in sociality seen in various often feed their young independently (Wiley, Amazona species. That there might be any basic unpublished). And like the Lesser Antillean differences in food availability for the Cayman species, and as one might predict from the pre- Brac Parrot and the Lesser Antillean species that ceding discussion, this parrot lives in an environ- could explain their low sociality is undocumented ment free of significant avian predators. No Red- and does not seem intuitively likely. Available evi- tailed Hawks or large accipiters occur on Cayman dence suggests that they feed on much the same Brac, and the Peregrine Falcons that are seen foods that are taken by other more social species there occasionally are mostly on the coast, posing in the genus. no significant risks to the parrots. Regardless of what factors are truly most The associations of low sociality with low pre- important in producing the relatively high degree dation risks and high sociality with high preda- of sociality found in most Amazona and Rhyn- tion risks strongly suggest a causal connection of chopsitta, this characteristic is generally consid- these features. Further reinforcing this conclusion ered to be adaptive in the lives of these species. is the fact that the race of the Cuban Parrot on Modern circumstances, however, can produce sit- Grand Cayman (Amazona leucocephala cayma- uations where this is clearly not true. We call nensis) shows the typical Amazona tendency attention to a recent instance of mass drowning of toward large flocks and apparently feeds its young Rhynchopsitta terrisi in an artificial water catch- as pairs. Significantly, there are Red-tailed Hawks ment where the species suffered a major popula- on Grand Cayman, unlike nearby Cayman Brac. tion stress precisely because of its high degree of Thus the parrots of the various Cayman Islands in sociality. In this instance, in 1994, at least 52 R. 16 Manual of Parrot Behavior terrisi perished when they were unable to exit March usually the peak month. This timing is in from an artificial cement water tank that they had general correlated with the dry season, and could apparently entered for drinking and/or bathing be related primarily to minimizing risks of nest purposes. When one considers that the total pop- loss to flooding, although it could alternatively be ulation of this species is only about 3,000 birds keyed to seasonal aspects of food availability. and the annual recruitment of young is only about Strongly suggesting the latter is the abnormally 200 individuals, this event was nothing short of late egg-laying period seen in the Bahama Parrots catastrophic (Macías-Caballero et al. 2001). of Abaco, which do not normally lay until late As an aside, Rhynchopsitta parrots, like many May and early June, just before onset of the rainy species of Australian parrots, but unlike most season in that region (Gnam 1991). Here, laying Neotropical parrots inhabiting humid environ- appears to be timed to take advantage of the abun- ments and consuming foods high in water con- dance of poisonwood (Metopium toxiferum) tent, come to water sources, such as waterfalls, to fruits, wild guava (Tetrazygia bicolor) fruits and drink on a daily basis. This behavior has been appropriate-aged pine (Pinus caribea) seeds in documented in both species of Rhynchopsitta midsummer, the most important known foods for (Snyder et al. 1999; Macías-Caballero et al. the species in provisioning young. The Bahama 2001), and, like the parrot assemblages at clay Parrots on Inagua Island apparently lay at a more licks of the Amazon basin, constitutes a mar- typical time in the early spring, in line with other velous spectacle. Unfortunately, man-induced amazons of the West Indies (Snyder et al. 1982). changes in the environment have both reduced the Pine is absent from Inagua, and poisonwood is availability of springs and waterfalls in the land- not nearly as conspicuous an element of the flora scape and increased the presence of artificial on this island as on Abaco. water catchments that can pose inadvertent risks Breeding seasons of mainland amazons have of mortality to the species. been especially closely studied in northeastern Another species for which high sociality may Mexico (Enkerlin-Hoeflich 1995) and are similar have led to major population stress from human to most West Indian amazons, with peak laying sources is the extinct Carolina Parakeet (Conu- in late March and early April (Table 2-1). The ropsis carolinensis). Flocks of this species were sympatric Red-crowned Parrot, Yellow-headed exceedingly vulnerable to shooting, and the ten- Parrot, and Red-lored Parrot have similar egg- dency of the species to roost together in large laying dates. Food is abundant during spring and groups in hollow trees made it susceptible to summer for Mexican Amazona. There is no clear- heavy harvest for the pet trade, both of which fac- cut dry season, although spring and summer usu- tors were of presumed importance in the species’ ally show peaks in rain and winter is normally decline (Snyder & Russell 2002). The high social- dry. Their breeding season is earlier as one moves ity of this species may also have rendered it high- south and would indicate that it is more related to ly susceptible to the spread of exotic diseases. photoperiod or temperature than to food avail- Finally, as another aside, we note that the ability (Enkerlin-Hoeflich 1995, unpublished absence of any strong tendency for flocking in the data). Lesser Antillean and Cayman Brac Amazona is a Breeding seasons of the Rhynchopsitta species factor that makes censusing of these species espe- are extremely delayed relative to the Amazona cially difficult. Although counts of large flocks species, and this delay is almost surely keyed to entering and leaving roosts have proven an effec- their specialized diets, primarily of various tive way to census many other Amazona species— conifer seeds, which do not normally become for example, the Puerto Rican Parrot and the abundantly available until midsummer, with early Bahama Parrot (A. leucocephala bahamensis)—it June being the low point in seasonal availability is not a practical option for species with low of seeds for the conifer species in the ranges of flocking tendencies. the species. The mean egg-laying date of the Thick-billed Parrot in Chihuahua has been mid- TIMING OF NESTING SEASONS July, with most chicks fledged by the first or sec- In the West Indies, most amazon parrots begin ond week of October (Snyder et al. 1999). The egg laying in the late winter and early spring, with Maroon-fronted Parrot starts somewhat later with 2 / Behavior of Wild Amazona and Rhynchopsitta Parrots 17

Table 2.1. Clutch initiation, incubation periods, feeding visits, and fledging age for Amazona parrotsa A. autumnalis A. oratrix A. viridigenalis Descriptive statistics (n = 24) (n = 6) (n = 26) Week (number of nests) 1 = 19–24 March 3 1 1 2 = 25–31 March 4 3 7 3 = 1–7 April 10 1 10 4 = 8–14 April 5 1 2 5 = 15–21 April 1 0 5 6+ = after 22 April 1 0 1 “Mean” (week of initiation)b 3.00 2.33 3.23 Range (week of initiation) 1 to 6 1 to 4 1 to 6 Standard deviation 1.22 1.03 1.27 Coefficient of variation 0.41 0.44 0.39 Average initiation of clutch (date)c 2 April 31 March 5 April Mean duration of incubation (days) 28d 28d 27 (n = 7) Mean daily feeding visits to the nestse 2.09 2.18 2.08 Range of daily visits to the neste 0–3 0–3 0–4 Mean age at fledging (days) 55 (n = 4) 57 (n = 2) 53 (n = 9) aBased on nests inspected with a burrow probe in the 1993 and 1994 breeding seasons. For A. oratrix, two additional nests from the 1992 season were included to increase sample size; although no burrow probe was available in 1992, these two nests were shallow enough to be inspected directly. bAn index calculated from six categories (weeks) assigned based on day of initiation. A test using Kruskal-Wallis on this index showed no difference among species (KW = 2.5, df = 2, p < 0.281). cCalculated from actual date of initiation for each nest. dAs reported in the popular captive breeding literature. eEstimated by multiplying the average number of visits per observation session by two as justified in Enkerlin-Hoeflich 1995. The range of visits also refers to the observation sessions only.

most egg-laying in late July to early August and NEST SITE AND PAIR FIDELITY, AND chicks fledging at the end of October through the CAVITY REUSE first week of November. In general, nest site and pair fidelity tend to be Thus, the evidence for importance of diet in high for psittacine birds (Snyder et al. 1987; determining the timing of breeding is highly sug- Rowley & Chapman 1991), although there are gestive both in the Bahama Parrot and the variations to be seen among species. High pair Rhynchopsitta parrots, and diet may be the most fidelity, for example, has been found in two important factor with the other Amazona as well, species of Amazona in northeastern Mexico— although this is less clear from available data. the Red-crowned and Yellow-headed Parrots Future studies focused on crop sampling of nest- (Enkerlin-Hoeflich 1995), and as with nest fideli- lings of a variety of species to rigorously deter- ty, may often be associated with improved pro- mine dietary relationships (Enkerlin-Hoeflich et ductivity as the years of experience accumulate. al. 1999), combined with studies of seasonal In many studies, cases of divorce have been large- availability of primary foods, may help solidify ly limited to instances of reproductive incompe- knowledge of the most important factors deter- tence of one of the pair members (Snyder et al. mining the timing of breeding. 1987; Rowley & Chapman 1991). 18 Manual of Parrot Behavior

Maroon-fronted Parrots nest in colonies rang- switch nest sites after failures to fledge young and ing from one or two to more than 100 pairs. Pairs a tendency to stay with nest sites after success in seem to have strong site fidelity, at least to the fledging young (Saunders 1982). One pair of same colony, if not the same nest hole, as demon- Puerto Rican Parrots studied over many years fol- strated by returns of birds carrying radio trans- lowed this pattern religiously, while other pairs mitters over periods of several years. Similarly, exhibited strong nest-site fidelity regardless of established pairs of most Amazona exhibit a success or failure in the sites over the years (Sny- marked degree of philopatry. For example, in der et al. l987). As an aside, until it was learned northeastern Mexico in 1993, four pairs of visual- that the latter pattern was the more typical one for ly distinctive Amazona that switched nest sites this species, efforts to multiple-clutch wild pairs moved to new nests within a 50 m radius of their were held in abeyance because of concerns that previous nests. In 1994, five pairs had new nests such efforts would drive pairs into using new nest within a 50 m radius of their previous nests and sites for replacement clutches that might be vul- two pairs moved within a radius of only 100 m. nerable to predation by Pearly-eyed Thrashers The attachment to specific nesting areas can be (Margarops fuscatus). But once the strong ten- something that occurs rapidly: a female Red- dency of pairs to stick with nest sites, despite crowned Parrot released with a radio collar estab- failure in the sites, was established, multiple- lished her nest sites in two successive nesting clutching efforts were initiated with considerable periods in trees within 200 m of the release cage success and without causing pairs to abandon sites. (Enkerlin-Hoeflich 1995). Even with relatively low levels of nest reuti- At least six pairs of Red-crowned Parrots and lization, pairs of Red-crowned and Yellow-headed five pairs of Yellow-headed Parrots individually Parrots have exhibited greater tendencies to reuse recognizable by feather characteristics showed sites in which they have succeeded than sites in mate fidelity between successive nesting periods, which they have failed. Similarly, studies of and at least three of each species exhibited fideli- Maroon-fronted Parrot nesting colonies indicate ty for three nesting periods. Such high mate that cavities producing fledglings are generally fidelity has also been documented in the Puerto the cavities most frequently reused over several- Rican Parrot by Snyder et al. (1987) and may be year periods. generally true in the genus Amazona. Thus there are reasons to suspect that poaching Fidelity to specific nest sites, however, is more of entire broods from nests of many species may variable. Enkerlin-Hoeflich’s (1995) studies of not only remove immediate reproduction but may Red-crowned and Yellow-headed Parrots in 1993 also affect future reproduction by stimulating and 1994 revealed that fidelity to specific sites pairs to move to new and untested nest sites, both was low compared to that reported in other because poachers frequently destroy nest sites in Amazona (Snyder et al. 1987; Gnam 1991; Rojas- harvesting them and because they often stimulate Suárez 1994). In large measure, this difference the birds to move even if they do not harm the may reflect species differences in cavity availabil- nest sites. If instead parrot trappers were to allow ity, with suitable cavities being considerably more at least one young to fledge per nest and were not abundant for the Red-crowned and Yellow-headed to harm nest sites in harvesting young, both par- Parrots than for other amazons, although addi- rots and trappers might ultimately benefit from tional factors may well have been involved as greater overall parrot populations and nest suc- well. Nest switching is standard in many cavity- cess in the populations. Instituting such relatively nesting birds (e.g., Boreal Owls, Aegolius prudent harvesting procedures, unfortunately, is funereus, and California Condors, Gymnogyps unlikely in areas subject to unregulated harvest, californianus—see Hayward & Hayward 1993 because maximization of short-term benefits and Snyder & Schmitt 2002), and may offer gen- tends strongly to overbalance maximization of eral advantages, such as reductions in parasite long-term benefits. infestations, that need to be balanced against advantages that may result from maintaining site FEEDING BEHAVIOR AND RATES fidelity, especially in cavity-poor environments. Amazon parrots of the mainland, such as Red- In many species, there is a tendency for pairs to crowned Parrots of northeastern Mexico, almost