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Evaluating Captive-breeding Techniques and Reintroduction Success of the California Condor (Gymnogyps californianus)
Amy C. Utt
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Recommended Citation Utt, Amy C., "Evaluating Captive-breeding Techniques and Reintroduction Success of the California Condor (Gymnogyps californianus)" (2010). Loma Linda University Electronic Theses, Dissertations & Projects. 852. https://scholarsrepository.llu.edu/etd/852
This Dissertation is brought to you for free and open access by TheScholarsRepository@LLU: Digital Archive of Research, Scholarship & Creative Works. It has been accepted for inclusion in Loma Linda University Electronic Theses, Dissertations & Projects by an authorized administrator of TheScholarsRepository@LLU: Digital Archive of Research, Scholarship & Creative Works. For more information, please contact [email protected]. LOMA LINDAUNIVERSITY School of Science and Technology In conjunction with the Faculty of GraduateStudies
Evaluating Captive-breeding Techniques and Reintroduction Success of the California Condor (Gymnogyps californianus)
by
Amy C. Utt
A dissertationsubmitted in partialsatisfaction of the requirements forthe degree of Doctor of Philosophy in Biology
June 2010 C 2010
Amy C. Utt All Rights Reserved Each person whose signature appears below certifies that this dissertation in his/her opinion is adequate, in scope and quality, as a dissertation for the degree Doctor of Philosophy.
, Chairperson William K. Hayes, Professor of Biolos6C
Ronald L. Carter, Provost
Stephen G. Dunbar, Associate Professor of Biology
(1.4 Floyd E. Hayes, Professor of Biology, Pacific Union College
than R. Wall, Assistant Professor of Biochemistry, School of Medicine
111 ACKNOWLEDGEMENTS
I would like to thank the many people and organizations for their
assistance in making my dreams a reality.
First, I would like to thank my committee members for their undying support, good advice, and most of all, believing in me. I have learned so much while working on this project, and I have Dr. William K. Hayes (Loma Linda University), Dr. Stephen G.
Dunbar (Loma Linda University), Dr. Nancy Harvey (previously with CRES; Zoological
Society of San Diego), Dr. Ronald Carter (Loma Linda University), Dr. Floyd Hayes
(Pacific Union College), Dr. Laurence McCloskey (La Sierra University), and Dr. Nathan
Wall (Loma Linda University) to thank.
I would like to thank the Zoological Society of San Diego for allowing me to study the California Condors at the Wild Animal Park. In addition, I appreciated the condor keepers at the Wild Animal Park for their interest and cooperation in my research and data collection. I would especially like to thank Don Sterner and Tom Levites for going above and beyond and sharing their experiences with the California Condor recovery project, making sure I had access to whatever information I needed, and taking me behind the scenes to witness newly hatched California Condor chicks. I am forever grateful for the time, attention, and friendships of the condor keepers.
I would also like to thank the Ventana Wilderness Society, Pinnacles National
Monument with the National Park Service, and Hopper Mountain Wildlife Refuge
Complex with the U.S. Fish and Wildlife Service, for allowing me to observe California
Condors at their respective release sites. The time I spent in the field has been valuable to
iv me in so many ways. Several people I would like to single out include Joe Burnett, Bruce
Palmer, Kelley Sorenson, Jessica Koning, Rebecca Leonard, Tom Leatherman, Greg
Austin, and Mike Stockton. There are so many other people I have had the honor of working with while in the field, thank you.
I want to share my gratitude with Los Angeles Zoo, Susie Kasielke, and Mike
Clark for their cooperation with my research. My discussions with Mike at the Los
Angeles Zoo offered me new insights into California Condor behaviors, and will be forever appreciated.
I would like to thank the Department of Earth and Biological Sciences of Loma
Linda University for helping to fund my research, along with a Grant in Aid of Research from the National Academy of Sciences (Administered by Sigma Xi, the Scientific
Research Society), and a privately funded grant through the Zoological Society of San
Diego. In addition, data collection would not have been possible without research permits from the National Park Service and the U.S. Fish and Wildlife Service. I am grateful that there are so many people and organizations supporting conservation and behavioral research.
I would like to thank my husband, Jonathan J. Rickard, who married me in the midst of this project. He supported my efforts, put up with me not being home for weeks at a time during our early years of marriage, and trusted in my ability to finish this project. He believed in me even when I didn't.
Finally, I would like to thank my son, Benjamin, for sharing the first two years of his young life with mommy and her dissertation work. Your zest for life and intense curiosity in all things renewed my own child-like wonder in the natural world. There is nothing like experiencing the world though the eyes of a toddler! Thank you my sweet baby boy. I love you!
vi For my son, Benjamin Reid Utt Rickard
You are my sunshine...
- vii CONTENTS
Approval Page iii
Acknowledgements iv
List of Tables xii
List of Figures xiv
List of Abbreviations xv
Abstract xvi
Chapter
1. Life History and Conservation of the California Condor 1
Species Description and Taxonomy 1 Habitat and Distribution 3
Historical Distribution 4 Current Distribution 5
Reproduction & Development 6
Courtship 6 Parental Care 10 Chick Development 11
Causes for Decline 11
Past Threats 11 Current Threats 13
Conservation Efforts 13
Conservation Controversy 13 Conservation Measures 17
In Situ Conservation 17 Ex Situ Conservation 18
Reintroduction 20 Objectives 21
viii References 23
2. The Effects of Rearing Method on Social Behaviors of Mentored, Captive- reared Juvenile California Condors 28
Abstract 29 Introduction 31 Materials and Methods 35
Cohort 1 (2003) 36 Cohort 2 (2004) 43 Social Behaviors 47 Dominance Relationships 49 Statistics 50
Results 51
Juveniles: Rearing Method versus Mentoring Phase 51 Adult Mentors: Rearing Method versus Mentoring Phase 55 Dominance Rankings 55
Discussion 60
Future Considerations 64
Conclusions 65 Acknowledgments 66 References 67
3. Predictors of Behavioral Problems and Survival Following Release of Captive-reared California Condors 72
Abstract 73 Introduction 75 Materials and Methods 80
Data Compilation 80 Statistical Analyses 83
Results 86
Behavior Problems 86 Survival 90
Discussion 94
ix
Sex 96 Facility 98 Rearing 99 Mentoring 100 Release Site 102 Age at Release 103 Population Size 104
Conclusions 105 Acknowledgements 106 References 107
4. Evaluating Captive-breeding and Reintroduction Methods in Avian Conservation: A Review 117
Abstract 117 Introduction 118 Multiple Clutching 131 Parent Rearing 134 Foster Parent Rearing 136
Intraspecific (Conspecific) Rearing 137 Interspecific (Cross-foster) Rearing 140
Puppet and Hand Rearing 144
Imprinting and Development Phase 147 Puppet Rearing 152 Hand Rearing 154 Group versus Isolate Housing 156
Behavior Management 157 Pre-Release Training 160
Mentoring 162 Predator Avoidance 166 Obstruction Avoidance 170
Release Methodologies 171
Hard Release 171 Soft Release 172
Acclimation 173 Predator Control 173 Supplemental Feeding 175 Monitoring 176 Hacking 177
In Situ versus Ex Situ Conservation 178 The Future of Captive Breeding 181
Defining Success 183
Conclusions 184 Acknowledgements 185 References 186
5. General Conclusions 208
Future Considerations and Implications 211 References 217
Appendices 221
A. Data Summarization 221
B. Order of Observations 226
C. Research Permits 229
D. IACUC Certification Certificate 233
E. Release Site Questionnaire and Results 235
F. Graph of Release Age California Condors (1996-2005) 239
xi TABLES
Table Page
1. Definitions of mutually exclusive behaviors quantified in California Condors 48
2. Mean acts per hour for each of 17 social behaviors exhibited by juvenile California Condors 53
3. Mean acts per hour for each of 17 social behaviors exhibited by adult puppet-reared and parent-reared California Condors 56
4. Dominance rankings of individuals from cohort 1 and cohort 2 57
5. Relationship diagnostics from dominance hierarchy analysis of "combined dominance" 58
6. Dominance matrix indicating frequency of "combined dominance" interactions for cohort 1 and cohort 2 59
7. Established population size (number of free-flying individuals) of California Condors (Gymnogyps califomianus) by year and release site 84
8. Summary of results for juvenile California Condors exhibiting behavioral problems at 1 and 2 yr after release into the wild 88
9. Logistic regression results for analyses of behavioral problems in juvenile California Condors 89
10. Summary of results for juvenile California Condors survival at 1 and 2 yr after release into the wild 91
11. Logistic regression results for analyses of survival in juvenile California Condors at 1 and 2 yr after release into the wild 93
12. Summary of red list categories of avian orders 119
13. Diagnostic features of Nice's avian developmental classes, including continuum of imprinting tendencies 123
14. Taxonomy, development, life history, rearing, and release of birds 124
15. Cross-fostering examples in avian conservation 138
16. Differences and implications of life history traits on various captive- breeding and release strategies 146
xii 17. Developmental classes and corresponding representative avian families 151
18. Pre-release training methods and outcomes 168
••• FIGURES
Figure Page
1. Prehistoric range of the California Condor 7
2. Topographic map of California Condor range in 1980s 8
3. Release sites for California Condors in 2010 9
4. Adult California Condor mentor in proximity of a juvenile prior to release 34
5. Overhead view of Zoological Society of San Diego's Wild Animal Park California Condor remote pens 37
6. Side view of condor remote pens ai the San Diego Wild Animal Park 38
7. Overhead view of flight pen in the Ventana Wilderness Area 39
8. Side view of flight pen in the Ventana Wilderness Area 40
9. Overhead view of flight pen at Pinnacles National Monument 42
10. Overhead diagram of condor flight pen at the San Diego Wild Animal Park 44
11. Overhead diagram of hospital quarantine pen at San Diego Wild Animal Park 45
12. Overhead view of flight pen at Hopper Mountain National Wildlife Refuge Complex 46
13. Interactions between rearing method (puppet-reared and parent-reared) and mentoring phase (SDWAP and flight pens at release) 54
xiv ABBREVIATIONS
ANOVA Analysis of Variance
CRES Center for Reproduction of Endangered Species
• CRP Condor Remote Pen
CRT Condor Recovery Team
DDT Double Door Trap
EM) Exotic Newcastle's Disease
EPA Environmental Protection Agency
LA ZOO Los Angeles Zoo
LAZ Los Angeles Zoo
NPS National Park Service
PNM Pinnacles National Monument
SDWAP San Diego Wild Animal Park
USFWS United States Fish and Wildlife Service
VWS Ventana Wilderness Society
WAP San Diego Wild Animal Park
ZSSD Zoological Society of San Diego ABSTRACT OF DISSERTATION
Evaluating Captive-breeding Techniques and Reintroduction Success of the California Condor (Gymnogyps californianus).
by
Amy Christina Utt
Doctor of Philosophy, Graduate Program Biology Loma Linda University, June 2010 Dr. William K. Hayes, Chairperson
In this dissertation, I present two original research studies on the behavior and survival of the critically endangered California Condor (Gymnogyps californianus). I also provide a comprehensive review of the role of captive-rearing to the conservation of birds.
The first study examined the behavioral differences of puppet- and parent-reared condor juveniles reared in captivity. This study further defined and examined the
behaviors of adult conspecific mentors and their interactions with juveniles. Dominance
hierarchy analyses for two cohorts of juveniles and their adult mentors indicated the
establishment of a linear hierarchy. Although puppet-reared juveniles engaged in fewer
social behaviors in captivity, they successfully integrated into a social hierarchy. The
second study examined potential predictors of behavioral problems and survival outcome
of released captive-reared California Condors using binary logistic regression and chi-
square analyses. Predictors incorporated in this study included age at release, sex,
mentoring, rearing facility, release site, and established population size. Results up to two
years post-release indicated that sex, adult conspecific mentoring, and established
population size were significant predictors of survival, whereas rearing facility and
xvi rearing method were significant predictors of behavioral problems. These results indicate that mentoring may be especially crucial to survival of captive-reared California Condors released to the wild, and that many puppet-reared birds successfully adapt to life in the wild.
The comprehensive review covered important methods used in avian captive-
breeding and reintroduction programs. The strengths and weaknesses of various rearing methods are discussed, including the importance of raising birds in an atmosphere that most closely mimics their breeding preferences, developmental mode, and life-history traits. The need to understand a species before implementing a captive-breeding program
is essential. Pre-release training is presented as a method to help prepare naive birds for
release, with emphases given to mentoring, predator training, and obstruction avoidance.
Comparisons between hard and soft releases and in situ and ex situ conservation are
examined. By establishing guidelines for determining success, emphasizing the need to
practice adaptive management, and implementing frequent independent reviews, avian
conservation programs — including the California Condor recovery program — can
become even more successful in the twenty-first century.
xvii CHAPTER ONE
LIFE HISTORY AND CONSERVATION OF THE CALIFORNIA CONDOR
Species Description and Taxonomy
The California Condor (Gymnogyps californianus) belongs to the Avian order
Falconiformes (BirdLife International, 2009). Controversy surrounding the taxonomy of this bird has lead to oscillations between the orders Ciconiiformes (old world vultures) and Falconiformes (which encompasses new world vultures, eagles, hawks, and falcons;
Avise et al., 1994; Slitkas, 1997; Snyder and Snyder, 2000; Snyder and Schmitt, 2002;
Hackett et al., 2008). The California Condor shares the family Cathartidae with one other condor, the Andean Condor (Vultur gryphus), and five species of vultures, including the
Black Vulture (Coragyps atratus), Turkey Vulture (Cathartes aura), Lesser and Greater
Yellow-headed Vultures (C. burrovianus and C. melambrotus respectively), and the King
Vulture (Sarcoramphus papa). The California Condor is one of only two surviving condor species, the other being the Andean Condor, and is the only member of the genus
Gymnogyps (Algona, 2004).
All new world vultures have several underlying characteristics, including urohydrosis (thermoregulatory behavior where bird urinates on legs for evaporative cooling), lack of nest-building behavior, true syringeal vocalizations, carrion feeding, reduction of feathers on the head, and feet adapted for walking rather than obtaining and killing prey (Snyder and Snyder, 2000; Snyder and Schmitt, 2002). Urohydrosis is very
1 unique to ayes and is shared only with storks and some boobies (order Ciconiiformes).
This connection is one of the main links used to connect cathartids to the order
Ciconiiformes in the past (Snyder and Snyder, 2000).
The California Condor is the largest flying bird found in North America and one of the largest flying birds in the world. The species feeds on carrion and is primarily dependent upon large mammalian carcasses (Snyder and Schmitt, 2002). Rarely, condors have been observed eating vegetation, which is later visible in castings which exhibit a greenish coloration (Koford, 1953; Snyder and Schmitt, 2002; personal observation). The propensity and possible benefits of vegetation remains unknown. The species is highly social while feeding, and can be seen in large numbers at carcasses and bathing sites
(Snyder and Schmitt, 2002; West, 2009). The condor can weigh up to 11 kg
(approximately 25 lb) with a wingspan reaching close to 3.3 m (10 ft), making it almost
equivalent in size to the Andean Condor. California Condors are not sexually dimorphic; thus, size is not a reliable determinant of sex (Snyder and Snyder, 2000; Snyder and
Schmitt, 2002).
Adult (approximately 6 years of age) California Condors are characterized by an
unfeathered, wrinkled, and fleshy head, with the exception of a small band of feathers
extending between both eyes and partially down the flesh-covered portion of the beak.
The distal portion of the beak is not covered by flesh and in mature adults is an ivory
color. The featherless head ranges in color from orange, pale pink, red, yellow, and gray
(Snyder and Schmitt, 2002). The bare skin of the head and neck has the ability to change
colors depending on the level of stimulus the bird is subjected to and superficial blood
circulation (e.g., color changes from pale to bright reddish color when threatened or
2 aggressive; Snyder and Schmitt, 2002; personal observation). Adult condors exhibit dark brown to black feathers over their body, except for under each wing where a band of white feathers is present. The conspicuous neck ruff of pointed dark-black feathers can be raised or lowered, covering or exposing the bare neck (Snyder and Schmitt, 2002).
Raising or lowering the neck ruff has been observed as a thermoregulatory behavior
(Snyder and Schmitt, 2002; personal observation).
Juvenile California Condors undergo a prolonged period of maturation, extending from about 5-7 years at reproductive maturity. During this time, the juvenile passes through several coloration changes (Snyder and Schmitt, 2002). Fledged juveniles
(approximately 5-6 mo.) are pure black, with even their necks covered in dark gray-black downy feathers. Over the next several years, the juvenile starts to lose the downy feathers on its head and neck and subsequently gains a mottled appearance, with patches of bare yellow-orange skin underneath. Concurrently, under-wing feathers begin to develop a mottled coloration as feathers slowly change from dark gray-black to pure white. Once the feathers are lost from the head and neck of a condor and under wing coloration changes are complete, the bird has finally acquired its adult coloration.
Habitat and Distribution
The California Condor formerly exhibited a broad range of habitat and climatic preferences. Condors (or fossil remnants) have been found as far north as British
Columbia, south into Mexico, and as far east as New York and Florida (Snyder and
Snyder, 2000; Snyder and Schmitt, 2002). Recently, Condors have been found primarily
in mountainous terrain, and nest most often in cliffs, or in cavities in large trees (e.g., Giant Sequoia, Sequoiadendron giganteum; Snyder and Schmitt, 2002). Condors are capable of traveling large distances (up to 150 km) in a day, and thus utilize an exceptionally large foraging area (Crawford, 1985). Condors have been known to feed at sea level on dead marine mammals, scavenge among grazing and crop-lands, and soar above high montane meadows (Snyder and Schmitt, 2002; Algona, 2004; Sorenson and
Burnett, 2007; Walters et al., 2008).
Historical Distribution
The California Condor formerly enjoyed a vast range. Early American explorers, such as Lewis and Clark in the late 18th and early 19th century, became the first white
Americans to reach the Pacific Ocean and record sightings of the California Condor
(McMillan, 1968; Snyder and Schmitt, 2002). Lewis and Clark observed the condor to be so plentiful in the Oregon territory that they dubbed it "the beautiful buzzard of
Columbia" (Smith, 1978). During this time, the range of the California Condor roughly extended from British Columbia to Baja California and as far east as Texas (Wetmore and Friedman, 1933; Darlington, 1991). However, fossils of the California Condor's close relatives, Gymnogyps amplus, G. kofordi, and Antillovultur varonai, are found in
New York and Florida as well (McMillan, 1968; DeBlieu 1993; Snyder and Schmitt,
2002; Figure 1). By the 1950s, the range diminished to a horseshoe-shaped area in
Central and Southern California.
The California Condor is sometimes called a relic from the ice ages. Preserved remains of these large birds and their ancestors have been found in the La Brea tar pits
(McMillan, 1968; Ehrlich, 1988). In the past they fed on terrestrial megafauna such as the
4 now extinct Mammoth and American Camel (Ehrlich, 1988; Snyder and Schmitt, 2002).
The primary food sources for prehistoric condors (proboscidians, edentates, and perissodactyls) largely became extinct near the end of the Pleistocene era, which may have had a large impact on early declines in numbers (Emslie, 1987; Algona, 2004)
Current Distribution
In the mid 1980s, when survival of the California Condor was uncertain, the range was reduced to a horseshoe-shaped area of central-southern California which closely followed the topography of the local mountains (Darlington, 1991; Snyder and Snyder,
2000; Snyder and Schmitt, 2002; Figure 2). For a brief period of time (1987-1992), the
California Condor was extinct in the wild when the last remaining Condors were brought into captivity for extensive captive breeding. Today, California Condors can be found in several locations: Southern California (with release sites from San Luis Obispo Country to Ventura County), Central California (in the Ventana Wilderness and Pinnacles
National Monument), Baja California (Parque Nacional San Pedro Martir), and Arizona extending into southern Utah (Vermillion Cliffs of the Grand Canyon).
Figure 3 provides a map of release sites and population sizes in North America.
Birds now freely intermingle between release sites in central and southern California
(Sorenson and Burnett, 2007). As of January 31, 2010, there were a total of 348
California Condors alive. Of these, 161 condors are housed in captivity between the San
Diego Wild Animal Park (SDWAP), the Los Angeles Zoo (LAZ), the Peregrine Fund
(TPF), and the Oregon Zoo. The remaining 187 condors are living in the wild (Figure 3).
5 Of the wild condors, 95 reside in California (Central and Southern California), 18 in Baja
California, and 74 in Arizona and Utah.
Reproduction & Development
Courtship
California Condors are monogamous breeders and are thought to mate for life
(Snyder and Snyder, 2000). If one bird dies, the remaining Condor has been known to re- pair (Snyder and Schmitt, 2002). Pair formation occurs in late fall to early winter.
Occasionally, abnormal pairing will occur, such as a group of three birds, but this type of behavior is considered "maladaptive" and is typically seen in reintroduced birds (Woods et al., 2007). When these abnormal pairings occur, frequently one or more of the birds encumbers the breeding and rearing process and can entirely preclude a successful breeding attempt (Mee et al., 2007).
Courtship involves three main behavioral displays: coordinated pair flights in nesting territory, mutual preening and grooming, and perching courtship displays (Snyder and Schmitt, 2002). Coordinated pair flights are often the first indicator that two condors are commencing pair formation (Snyder and Schmitt, 2002). Courtship displays are performed by the male who exhibits a posture of wing-spreading, extended and drooping head, and strutting around the female (Snyder and Schmitt, 2002). The male's bare head will often turn to a brighter shade of pink-red during this process.
Condors typically produce just one egg (chick) every other year. One egg is laid, but will be replaced if the first is lost to predation or damaged (i.e., double-clutching).
6 Figure 1. Prehistoric records of California Condors (redrawn maps and data from Snyder & Snyder, 2000; Snyder and Schmitt, 2002; Algona, 2004).
7 Tulare County
Fresno County
Kern County
San Bernardino
San Luis Obispo County
Santa Barbara County
Los Angeles County
^
Figure 2. Topographic map of California Condor range in 1980s (redrawn from maps and data from Snyder & Snyder, 2000; Snyder and Schmitt, 2002; Algona, 2004).
8 Location Wild Population Central California 52 Ventana (released) 20 Wild-fledged 6 Pinnacles (released) 25 Wild-fledged 1 Southern California 43 Hopper (released) 34 Wild-fledged 9 Baja California (released) 18 The Peregrine Fund 74 Vermillion Cliffs, AZ (released) 65 Wild-fledged 9 Total Wild Population 187 Figure 3. Release sites for California Condors, January 2010.
9 Parental Care
California Condors exhibit biparental care during the incubation and rearing process (Snyder and Schmitt, 2002). Condors are not nest builders like other large birds in North America, (e.g. bald and golden eagles), and typically lay their single egg in shallow caves on cliffs or in hollow portions of trees. Each parent takes a "shift" incubating or brooding the-cilick,_which can last for several days before the other parent returns (Snycleiand 'Schmitt, 2002). California condors typically produce one chick every other breeding year.
Parents in the early weeks post-hatching spend a great deal of time brooding and grooming hatchlings, with the frequency decreasing over time. Adults regurgitate in order to feed chicks, with the frequency decreasing with age of the chick as well (Snyder and
Schmitt, 2002).
The only natural dangers posed to California Condor eggs and juveniles is predation by Common Ravens (Corvus corax), and accidents, such as rolling or falling off of the shallow nest area on a cliff (Koford, 1953). Current dangers to juveniles now also include the ingestion of "microtrash", small pieces of trash brought to the nest by parents (Snyder and Snyder, 2000; Grantham, 2007; Mee et al., 2007). Microtrash has become the primary cause of nesting failure in southern California, with two of the recent failed breeding attempts having a direct link to microtrash (Mee et al., 2007). Microtrash has been found in 12 of the 13 total breeding attempts through 2005, further indicating the pervasiveness of this problem.
10 Chick Development
Typical incubation for the California Condor is about 53-60 days (Snyder and
Snyder, 2000; Snyder and Schmitt, 2002). Upon hatching, the semialtricial-1 chick is covered in white down, except for the head and neck, which are naked (Stark and Ricklef,
1998; Snyder and Schmitt, 2002). The eyes are open upon hatching, and the chick is completely dependent on its parents for all care.
Condor chicks grow rapidly, and by 100-110 days of age (approximately 2 months pre-fledging), a condor attains adult mass (Snyder and Schmitt, 2002). During this rapid period of growth, juveniles experience a change in feather coloration, from white to gray-black, including the beak, which is black during the juvenile stage.
Juveniles fledge from the nest between 5 and 6 months of age, but typically stay with their adult parents approximately 20 months in the wild before setting out on their own.
Causes for Decline
Past Threats
Natural predators (past and present) of the California Condor include Coyotes
(Canis latrans), Wolves (Canis lupus), Foxes (Vulpes vulpes), Mountain Lions (Felis concolor), Bobcats (Lynx rufus), Black Bears (Ursus americanus), Grizzly Bears (Ursus arctos), and Golden Eagles (Aquila chrysaetos; Koford, 1953; Snyder and Snyder, 2000).
However, no other species has had such a dramatic impact on the decline of this large bird as humans.
California Condors have been an important symbol for Native American tribes and were frequently used in ritual sacrifices (Snyder and Schmitt, 2002). When pioneers
11 arrived in the west, they saw the condor as a nuisance and believed them to be strong enough to carry off cattle and harbor dangerous diseases (Smith, 1978). Because of the misconceptions of early settlers, wanton shooting of condors was common. Later, the boom in the cattle industry brought a larger food supply to the condors, but also exposed the birds to new dangers (Algona, 2004). Large numbers of condors succumbed to poisoning after feeding on tainted carcasses meant to lure and kill predators such as bears, cougars, and coyotes that were killing sheep (Algona, 2004).
During the gold rush, miners would use condor quills to hold gold dust (Algona,
2004). With a diameter of approximately 1.3 centimeters, a quill could hold up to 10 cubic centimeters of gold, a small fortune in those days (Smith, 1978). This practice, along with the collection of condor eggs for museums ($300 an egg in the early 1900s), increased the decline of the already dwindling numbers of the California Condor population (McMillan, 1968; Smith, 1978).
In the mid-twentieth century, new threats emerged for the California Condor, including lead poisoning and fragile egg shells caused by pesticides (e.g., dichloro- diphenyl-trichloroethane [DDT]; Koford, 1953; McMillan, 1968; Kiff, 1979; Weimeyer,
1988; Snyder and Snyder, 2000; Snyder and Snyder, 2005). All of the aforementioned factors were compounded by the fact that California Condors have a low reproductive
(one chick every other year) and maturation rate (6-8 years), which over time, made it impossible for the dwindling numbers to rebound.
12 Current Threats
Current threats to the California Condor include lead poisoning, pollution (i.e. microtrash), and occasional shootings (Church et al., 2006; Grantham et al., 2007; Mee et al., 2007; Walters et al., 2008). Recent research has concluded that lead ingested from deer shot and left by hunters is a significant cause of condor mortality in the wild (Church et al., 2006). Therefore, condors are provided supplemental clean food at all release sites and extensive blood tests are taken regularly from released birds to test for dangerous levels of lead (Parish et al., 2007). If birds are found to have high levels of lead, they must undergo long chelation therapy treatments before being released again, sometimes returning to the same areas where they ingested the lead and becoming re-poisoned
(Meretsky & Mannan, 1999; Redig et al., 2003; Hall, 2007; Parish et al., 2007).
Conservation Efforts
Conservation Controversy
The condor, symbol of heaven and death. Certain Indian tribes believed it could fly to the gods; others refused it religious significance because it scavenged among corpses for food. As a symbol of rare wildlife its significance to Americans has also been mixed. In the history of endangered species work, no program has attracted such public attention, or generated such ill will. (DeBlieu, 1993:193)
As the numbers of California Condors plummeted in the early 1980s, controversy
about how to best deal with this critically endangered bird ensued (Crawford, 1986;
Walters et al., 2008). The U.S Fish and Wildlife Service, the California Department of
Fish and Game, the California Condor recovery team, and many others felt that
extinction would be inevitable if condors remained in the wild (Crawford, 1985).
13 Therefore, many proposed to bring all remaining condors into captivity to preserve the
species through breeding programs, with the stipulation that California Condors could be
re-released into the wild once the condor population was brought to a higher and more
stable number (Algona, 2004).
Organizations such as the National Audubon Society, Friends of the Earth, and
the Sierra Club argued that captive-bred condors would never be able to fend for
themselves once released back into the wild. They postulated that captive-raised
condors would lack sufficient knowledge of living in the wild and would be too
imprinted on humans, thereby reducing the condor's chances of success once released
(Crawford, 1985). In addition, they feared that if all California Condors were removed
from the wild, there would be nothing left to stop development of their already
encroached-upon habitat (Crawford, 1986).
The presence of condors in the mountains had forestalled a number of development projects, involving a generating plant with more than five hundred windmills that had been planned along a major condor flight path. Once every condor had been placed in captivity, the Audubon staff members feared there would be no limit to the development within the species' historic range (DeBlieu, 1993:209)
Thus, preservation of the California Condor's original wildness was another concern (Crawford, 1986; Algona, 2004). Many field biologists felt that enough was not known about the condors to remove all from the wild. There was still much to learn about the condor's behavior in the wild and the dangers that were posed to them (DeBlieu,
1993). Carl Koford, who many see as the original California Condor expert, stated:
Do we want to replace the wild condors with cage-bred, hand-raised birds? A wild condor is much more than feathers, flesh, and genes. Its behaviors results not only from its anatomy and germ plasm but from long cultural heritage, learned by each bird from previous generations through several
14 years of immature life...If we cannot preserve condors in the wild through understanding their environmental relations, we have already lost the battle and may be no more successful in preserving mankind (DeBlieu, 1993:199).
On a wider scope, the dwindling condor population indicated that something was drastically wrong with the environment (Darlington, 1991). People reasoned that bringing these highly endangered birds into captivity to raise population numbers would not fix the problems that caused their impending demise in the first place. Captive breeding can divert attention from the problems causing a species decline and become a technological fix that merely prolongs rather than rectifies problems (Snyder et al., 1996). It was argued that the real importance of the California Condor was an indication of what is going wrong with our environment. People should let nature take its course and if that meant the condor was doomed to extinction, so be it (Darlington, 1991; Algona, 2004).
In contrast, others such as Noel Snyder, who at the time was employed by the US
Fish and Wildlife Service, felt that without captive propagation of the species, the
California Condor was doomed (DeBlieu, 1993; Snyder and Snyder, 2005). For many,
allowing this grand and historic bird to become extinct was unacceptable. As more and
more condors died in the wild, the possibility of an adequate gene pool started to fade.
Snyder felt the only way to preserve the species was to establish a captive breeding
program immediately to preserve the gene pool that was left (DeBlieu, 1993; Snyder and
Snyder, 2005). Koford (1953) asserted that breeding condors in captivity should be
attempted only after all efforts to maintain natural populations had failed. As more and
more of the few remaining condors died in the wild, people began to see that leaving the
birds in the wild and supplying clean, lead-free food (in hopes of changing their
behavior to adapt to the many problems brought on by sprawling development and
15 pollution) would not alleviate the impending extinction of the species (Koford, 1953;
DeBlieu, 1993). John H. Baker, the President of the National Audubon Society, stated in
1952 for the Foreword of Carl Koford's book, The California Condor:
...man, both directly and as a consequence of his uses of land, has been the principal cause of the Condor's reaching the verge of extinction. This furnishes reason for believing that man, through helpful action, may contribute to its survival and restoration.
With the principle that humans (e.g., environmental pollutants and contaminants) were responsible for the majority of the problems, many felt that man should take
responsibility (Algona, 2004). Captive breeding programs appeared to be the only way to prevent these large birds from dying out.
Unfortunately, the fight over what to do with the California Condor broke down
communication among those studying the condors, propagating division within the
California Condor recovery team (Crawford, 1986; DeBlieu, 1993). Evidences of
division can still be seen today and continues to be a problem for field and research
biologists. Some branches of the Condor Recovery Team tend to isolate data pertaining to
rearing and releases, which leads to difficulty in accurately assessing captive-breeding
and reintroduction success of the California Condor (and other endangered species), as
well as the efficacy of management protocols (Jackson, 2006). This division had a
marked impact on the study in Chapter 3 by significantly reducing the sample size (>50
•birds) of one of my most important analyses because one rearing facility (the Peregrine
Fund) and release site (Vermillion Cliffs, AZ) failed to cooperate and share information.
Sadly, this is typical of the program.
The decision of what to do with the California Condor was cemented after intense
debates and legal action between the National Audubon Society and the U.S. Fish and
16 Wildlife Service (DeBlieu, 1993). All the remaining California Condors were finally brought into captivity in 1987. The California Condor became extinct in the wild.
Conservation Measures
Reintroduction programs benefit when cooperation exists between in situ and ex situ programs. In situ (on-site) conservation involves protection of an endangered species occurs in areas of original habitat, and can include habitat protection, restoration, and predator control (Snyder et al., 1996). Ex situ (off-site) conservation entails protecting threatened or endangered species outside areas of natural habitat (Snyder et al., 1996).
For critically endangered species, it may be necessary to maintain them ex situ while in situ conservation efforts focus on preserving existing habitat fragments and opportunistically reconstructing artificially diverse ecosystems into which threatened species can be reintroduced at a later date (Snyder et al., 1996; Rabb and Saunders,
2005).
In Situ Conservation
In the case of the California Condor, early conservation efforts (1930s-1980s) focused on habitat preservation (in situ conservation; Snyder and Schmitt, 2002). During this period, significant portions of land were set aside as condor sanctuaries (the Sisquoc
Sanctuary in Santa Barbara County in 1937 and the Sespe Condor Sanctuary in Ventura
County, CA in 1947; Snyder and Schmitt, 2002). Although we now know the principle
cause of the decline of this bird was not due to habitat loss, it still remains important in the long term management and reintroduction of the California Condor (Snyder and
17 Schmitt, 2002).
Other in situ conservations measures (between 1930s-1980s) included establishment of federal protection, increased education and law enforcement to reduce shooting and harassment, increased protection of nesting and roosting areas from human disturbance, study effects of poisons on surrogate species, full-time patrol of areas with high condor activity, prohibiting use of poisoned carcasses for coyote control, close of specific flyways to shooting, and prohibition of low-flying aircraft over the Sespe Condor
Sanctuary (Snyder and Schmitt, 2002).
In addition to these measures, several organizations became involved and committed to long-term research and conservation programs for the California Condor
(National Audubon Society, U.S. Fish and Wildlife Service, California Department of
Fish and Game, U.S. Forest Service, Bureau of Land Management, Zoological Society of
San Diego, Los Angeles Zoo, and the California Condor recovery team; Snyder and
Schmitt, 2002). Despite the increased awareness, habitat preservation, and protection of the California Condor, their numbers continued to plummet.
Ex Situ Conservation
Once it became clear the California Condor would not be able to survive without intensive ex situ management, the controversial captive-breeding program for California
Condors began in 1982 with the removal of an egg from the wild (Stoms et al., 1993;
Snyder and Schmitt, 2002). From 1983 — 1987 many additional condors and eggs were
brought into captivity for breeding (Snyder and Schmitt, 2002). Early breeding facilities
included the San Diego Wild Animal Park and the Los Angeles Zoo (Crawford, 1986).
18 The Peregrine Fund was added as a partner in the Condor Recovery Program in 1993 and most recently, the Oregon Zoo opened a breeding facility in 2003.
The first successful breeding in captivity occurred in 1988, and the following year three pairs bred successfully (Snyder and Schmitt, 2002). Breeding facilities took advantage of the female's ability to double-clutch and started pulling the first egg of the season for artificial incubation, inducing the breeding pair to lay a second egg (Snyder and Schmitt, 2002; Harvey et al., 2003; 2004; Nielsen, 2006). Typically, the first chick was raised with a condor-like puppet (a form of hand-rearing) instead of by the natural parents (Toone, 1994; Meretsky et al., 2000; Beres & Starfield, 2001; Harvey et al., 2003;
Clark et al., 2007; Utt et at., 2008). The second egg of the season was then raised by the biological parents, conspecific foster parents, surrogate Andean Condors (cross-foster parents), or by a puppet (Toone, 1994; Wallace, 1994; Meretsky et at., 2000; Beres &
Starfield, 2001; Utt et al., 2008). Multiple clutching allowed the rapid proliferation of
Condors in captivity and their numbers grew rapidly.
In addition to producing more parent-reared California Condor juveniles for release, the condor-breeding facilities at the SDWAP and LAZ established a mentoring program in 1999, whereby one or more juveniles were housed with one or more adult (>5 yr age), non-parent condors in an isolated pen prior to release, at either the rearing facility, release site, or both (Kaplan, 2002; Bukowinski et al., 2007; Utt et al., 2008). In some social species, development of normal behavior may depend on an association with the parents or other adult birds during particular stages of maturation (Hutchins et al.,
1995; Snyder et al., 1996; Meretsky et al., 2000; Algona, 2004). Thus, using adult
19 mentors was hoped to help captive-reared juvenile condors be behaviorally prepared for life in the wild (Utt et al., 2008).
Reintroduction
Prior to the release of California Condors back into areas of original habitat,
Andean Condors were released as "test subjects" starting in 1988 (Snyder and Schmitt,
2002). Part of the experimental releases was to determine if Andean Condors would feed on "clean" (i.e., lead free) proffered carcasses, as well as other technical aspects of implementing a release program (Snyder and Schmitt, 2002). Experimental releases with
Andean Condors fared well, so recovery officials released the first California Condors back into the wild in 1992. Unfortunately, all birds released in 1992 exhibited an excessive amount of human attraction (e.g., attraction to humans and human structures, multiple birds colliding with overhead power lines). Behavioral difficulties continued until in 1994, all released birds were brought back into captivity again (Snyder and
Schmitt, 2002). Releases were attempted again in 1995, and although several birds still exhibited behavioral problems and were permanently removed from the wild, those that did not became part of the new "wild" population.
Behavioral problems of released California Condors became of paramount concern to the Condor Recovery Team and multiple approaches were implemented over the years to help captive-reared California Condors behave more like wild Condors (e.g., adult mentoring, parent-rearing, cross-fostering, more aggressive puppet-rearing; Clark et al., 2007; Utt et al., 2008; discussed in Chapter 2). In addition, condors were given pre-
release training, acclimation to release sites before releases, and intermittent hazing by
humans to instill a "healthy" fear in the birds (Grantham, 2007; Utt et al., 2008; Walters
20 In Chapter 5, I summarize the general conclusions of my work. I discuss the implications of behavioral differences in rearing types (Chapter 2), as well as the factors that influence the behavior and survival of captive-reared California Condors once released into the wild (Chapter 3). I also discuss several management alternatives to improve the success of the California Condor Recovery Program (based from Chapter 4
Finally, I discuss important issues relevant to the future of the California Condor reintroduction program, including the pervasiveness of lead poisoning and microtrash ingestion.
22 et al., 2008; Chapter 2-4). Many of the behaviors recovery team members were concerned about have become maladaptive presumably because of the inability of the species to respond to new (often human-caused) selective pressures (Reed, 1999; Snyder and
Snyder, 2005).
Objectives
In this dissertation I present two original research studies on the behavior and survival of captive-reared and reintroduced condors. I also provide a comprehensive review of the role of captive-rearing to the conservation of birds
Behavioral problems of California Condors, hypothesized causes, and potential remedies are discussed in depth in Chapters 2 and 3. In Chapter, I document behavioral differences between the two different rearing methods (parent- versus puppet-reared) used for California Condor juveniles, and present one of the only two dominance hierarchy analyses performed on the condor to date (Bukowinski et al., 2007; Utt et al.,
2008). In Chapter 3 I present the most detailed analysis to date of the success of the
California Condor reintroduction program, which included the possible influence of many factors (sex, rearing, rearing facility, population size at release, age at release, and mentoring) on the behavior and survival of birds released to the wild.
I provide an extensive review of many important aspects used in modern avian captive breeding and reintroduction programs and offer suggestions on how to select techniques best suited to an individual species. Several criteria are proposed to more accurately assess success in a captive-breeding and reintroduction program.
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Stoms DM, Davis FW, Cogan CB, Painho Marco OD, Brean WSJ, Scott, MJ. (1993) Geographic analysis of California Condor sighting data. Conservation Biology. 7(1):148 — 159. Toone WD, Wallace MP. (1994) The extinction in the wild and reintroduction of the California Condor (Gymnogyps californianus). P 411-419. In Olney PJS, Mace GM, Feistner, ATC, eds. Creative Conservation: Interactive Management of Wild and Captive Animals. London. Chapman and Hall. Utt AC, Harvey NC, Hayes WK, Carter RL. (2008) The effects of rearing method on social behaviors of mentored captive-reared juvenile California Condors. Zoo Biology. 27:1-18. Wallace MP. (1994) Control of behavioral development in the context of reintroduction programs for birds. Zoo Biology. 13:491-499. Walters JR, Derrickson SR, Fry DM, Haig SM, Marzluff.IM, Wunderle JIM, Jr. (2008) Status of the California Condor and efforts to achieve its recovery. The American Ornithologists Union and Audubon California. West CJ. (2009) Factors influencing vigilance while feeding in reintroduced California Condors (Gymnogyps californianus). [thesis] Arcata: Humboldt State University. Wetmore A, Friedman H. (1933) The California Condor in Texas. Condor. XXXV:37-38. 26 •Wiemeyer S, Scott JM, Anderson M), Bloom PH, Stafford CJ. (1988) Environmental contaminants in California Condors. Journal of Wildlife Management. 52(2):238- 246. 27 CHAPTER TWO THE EFFECTS OF REARING METHOD ON SOCIAL BEHAVIORS OF MENTORED, CAPTIVE-REARED JUVENILE CALIFORNIA CONDORS Amy C. Uttl, Nancy C. Harvey2'3, William K. Hayesl, Ronald L. Carterl iDepartment of Earth and Biological Sciences, Loma Linda University, Loma Linda, California 92350 USA 2Center for Reproduction of Endangered Species, San Diego Zoo, P.O. Box 551, San Diego, CA 92112-0551 3Present address: 6509 Harrier Rd. Nanaimo BC V9V 1V9 Canada 2008. Zoo Biology. 27: 1-18. (with some updating, including many new figures) 28 • Abstract Puppet-reared and parent-reared captive-bred California condor (Gymnogyps californianus) juveniles were studied prior to their release into the wild. Behavioral data were collected during social interactions within two cohorts of juveniles (N = 11) and their adult mentors (N = 5). The purposes of this study were to: 1) document the social behaviors of mentored juvenile California Condors and 2) compare social behaviors for two different rearing methods (puppet- versus parent-reared) during two phases of the mentoring process (San Diego Wild Animal Park versus release sites). Of the 17 behaviors examined by 2 x 2 analyses of variance (ANOVAs), two significant interactions between rearing method and mentoring phase were found: pulls feathers and feeds alone. For both behaviors, parent-reared condors engaged in these activities more often at the zoo and less often at the release pens than did the puppet- reared condors. The main effect of rearing was also significant for two behaviors: near other and receives contact aggression from other. Parent-reared birds were more likely to be near another bird and receive contact aggression, regardless of mentoring phase, than puppet-reared birds. The effect size for 16 of the 17 behaviors was greater for rearing method than for mentoring phase. Rearing method differences may persist long-term, as parent-reared adult mentors were significantly more aggressive than puppet-reared adult mentors. •••• Dominance relations were examined for both cohorts, with the first cohort exhibiting a strong linear relationship (h' = 0.86, P = 0.018), whereas the second cohort exhibited a moderate but non-significant linear hierarchy (h' = 0.63, P = 0.21). Rearing method had no effect on dominance among the juveniles, but adults were probably dominant to juveniles (P = 0.052; the difference was nearly significant). Although social 29 behaviors between the two rearing groups were similar in most respects, this study is the first to document measurable differences between puppet- and parent-reared captive-bred California Condor juveniles. 30 Introduction Within the last century, the California Condor (Gymnogyps californianus) suffered a drastic decrease in population size until, in 1987, the condor became one of the world's most endangered species. At this time, all remaining wild condors were brought into captivity for an extensive captive-breeding program (Stoms et al., 1993; Snyder and Snyder, 2000; Algona, 2004). Breeding facilities used a strategy called "double clutching" to produce as many California Condors in captivity as possible (Snyder and Hamber, 1985; Harvey et al., 2003; 2004; Nielsen, 2006). Double clutching has been highly effective in increasing production of birds reared in captivity, and involves pulling the first egg of the season to induce the breeding pair to lay another egg (Conway, 1980). Typically, the first chick, and sometimes the second chick as well, were incubated and raised with condor-like puppets instead of by the natural parents (Toone, 1994; Harvey et al., 2004; Snyder, 2005; Nielsen, 2006). Meretsky and Snyder (2000) argued that the success of captive-reared California Condors was directly related to whether or not the chick was puppet-reared or parent- reared. In 1992, when puppet-reared condors were first released, 37.9% died in the wild and 18.5% had to be recaptured for behavioral problems. in 1996, when parent-raised condors started to be released, 30.2% died in the wild and only 2.3% were recaptured for behavioral problems (Mace, 2006). Mortality rates were similar between the two groups, but recapture rates stemming from maladaptive behavior of puppet-raised condors were indicative of a problem (Woods et al., 2007). Appropriate behaviors center on a fledgling that avoids human activities and structures and integrates into the condor social structure (e.g., understands place in a dominance hierarchy, eats with others, preens others, and is 31 near to others). Maladaptive behaviors are those that preclude functioning within a condor social hierarchy and show little aversion towards human activities, structures, and potential predators (Snyder and Snyder, 2000; Nielsen, 2006). Many behaviors have become maladaptive presumably because of the inability of the species to respond to new (often human-caused) selective pressures (Reed, 1999; Snyder and Snyder, 2005). There are three reasons for the apparent maladaptive behaviors of puppet-reared California Condors. First, puppet-raised condors lack certain necessary adult influences during their development, leaving the young birds deficient in specific social skills that can only be learned from adult condors (Alagona, 2004). Second, some conservation program officials may have a bias against puppet-raised condors and, therefore, hold more stringent standards when judging the ability of puppet-raised condors to live successfully in the wild compared to parent-reared condors (Meretsky and Snyder, 2000; Snyder and Snyder, 2000; Snyder and Schmitt, 2002; Neilsen, 2006). Finally, standards to which living successfully in the wild is judged may not be consistent among release sites (Appendix E). The proportions of puppet- and parent-reared birds vary among release sites (unpublished studbook and release-site databases) and maladaptive behaviors have not been adequately defined. Some experts observed that, in species with extended parental care (such as the California Condor) the behavioral deficiencies of captive-bred stock have sometimes been overcome by conspecific fostering (Snyder et al., 1996; Snyder and Snyder, 2005). Beginning in 1999, the California Condor Recovery Program initiated a mentoring program as a way to facilitate "normal" California Condor behaviors in puppet-reared juveniles that did not have prior adult exposure (Figure 4). The condor-breeding facilities 32 (San Diego Wild Animal Park and the Los Angeles Zoo) established a mentoring program in 1999, in which juveniles were housed with an adult condor (over 5 years of age) in an isolated pen prior to release (Kaplan, 2002; Snyder and Snyder, 2005). The facilities hoped that adult mentoring would ameliorate any behavioral differences between puppet-reared and parent-reared juveniles so that, when the fledglings were released, puppet-reared condors would have the same success as those who were parent- reared. Success in the wild is defined as not only surviving, but also having appropriate condor behaviors. To assess the potential impacts of rearing method and the mentoring process on the expression of appropriate or "normal" behaviors of released condors, two types of studies are required. First, detailed studies of social behavior can offer insight on whether puppet-rearing produces condors that are behaviorally distinct from parent- reared condors. Second, quantitative analyses of the success of released birds would provide a more objective evaluation of whether parent-rearing and mentoring significantly influence behavior and survival. The purposes of the present study were to: 1) document the social behaviors of mentored juvenile California Condors, and 2) compare social behaviors for two different rearing methods and two phases of the mentoring process. A companion paper will explore the factors associated with the success of released condors. 33 Figure 4. Adult California Condor mentor in proximity of a juvenile prior to release. Ventana Wilderness, 2003. Photo by Amy C. Utt Materials and Methods Social behaviors were studied in two cohorts of juvenile condors. Within each cohort, juveniles were raised by two different methods (puppet-reared or parent-reared) until, at fledgling age (approximately 5 months (c.f. Cox et al., 1993; Snyder and Snyder, 2005), they were housed with one or more additional juveniles and a non-parent adult mentor (Figure 4). The juveniles of each cohort were also observed in two dissimilar social environments: first, in several small groups at the San Diego Wild Animal Park (SDWAP), and later, in a single large group at one or more of several release sites. Individuals were marked with colored patagial tags displaying the studbook number for identification (Wallace et al., 1980; Meretsky and Snyder, 1992; Gaunt and Oring, 1999; Woods et al., 2007). While being held at SDWAP, the condors were fed a carnivore diet of (Natural Balance) beef spleen, rabbits, rats, chicks, and rainbow trout, with all birds fasted two non-consecutive days each week. Condors at the release sites were fed a diet of stillborn calf, rabbit, and rat, and were fasted on non-consecutive days as well. The stillborn calf was often the only food item provided that gave opportunity for group feeding interactions. All decisions regarding housing, transfers, and eventual release, were made by SDWAP and key members of the Condor Recovery Team. We were only given access to observe the birds and examine their records and had no control over the number of birds in the two rearing conditions, numbers of days of mentoring, number of days observed in each caging situation, and where the birds were released. In spite of the aforementioned study limitations, we were able to acquire sufficient data to answer our primary questions. 35 Cohort 1 (2003) Three adult mentors (Ad-141, female, hand-reared; Ad-138, male, hand-reared; Ad-140; male, parent-reared) and seven juveniles (3 hand- and 4 parent-reared) were observed at SDWAP. These birds were studied from 19 February to 11 April 2003, with 24 observation days. The birds were housed in three conjoining condor remote pens, with two to three juveniles and one adult per pen (Figures 5, 6). Each pen was equipped with a water pool, a perching area, and a "hot pole" (mock electric pole delivering a mild electric shock upon contact; Kleiman et al., 1994; Snyder and Snyder, 2000; Alagona, 2004; Nielsen, 2006; Woods et al., 2007) used for pre-release aversive training. Each of the three wood and chain-link pens were 6.1 x 12.2 m, with a maximum height of 6 m (the pens were on a slope, Figure 6). On 15 April 2003, six of the seven juveniles (2 hand- and 4 parent-reared) were transported to the Ventana Wilderness Area in Monterey County, California (the seventh juvenile remained at SDWAP for eventual captive breeding). Here, the juveniles were held in a single flight pen pending transport to Pinnacles National Monument (PNM) for eventual release. The cohort was housed with their adult mentor (Ad-63, male, hand- reared) from 15 April to 10 September 2003. We recorded their behaviors on 22 days during this period. The flight pen was 12.2 x 7.6 m, with a maximum height of 9.1 m (Figure 7, 8). Most of the pen was enclosed with a durable plastic mesh, but the lowest 1 m had chain-link fencing. The upslope end included six nest boxes, a wooden ledge, and several branches for perching. A water pool and "hot pole" were also present (Figures 7, 8). 36 CRP 3 CRP 2 CRP I 6.1m Perches '71 Hot13 oles t /Water pool Nest box /71 Viewing Windows Observational Room Figure 5. Overhead view of Zoological Society of San Diego's Wild Animal Park California Condor Remote Pens (CRF's). Birds are observed through one-way glass in the darkened room at the end of their CRP, farthest away from the perch area. The double lines in CRP 2 represent two layers of chain-link fencing to separate CRP 2 from CRP 1 and CRP 3. Outside walls of CRP 1 and CRP3 are completely walled so as to prevent birds from viewing zoo staff approaching or leaving CRPs. The dimensions for each of the three pens measure 12.2m x 6.1m x 6.1m. Each nest box measures 1.5 m x 1.5 m x 2.1 m. 37 Covered Area 3m perch Observation Room 12.2m Figure 6. Side view of Condor Remote Pens (CRPs). Pens slope downhill and look across to another hill above the San Diego Wild Animal Park. Walled area of pen is shaded in gray. Each pen has a partial roof covering for protection from the elements, as well as a partial wall between CRP 1, CRP 2 and CRP 3. The sides facing the opposing hill are covered with chain-link fencing. Birds are located at a remote area from the Wild Animal Park, so as to not be accustomed to human sounds or structures. 38 7.6m Release Gate Hot pole Snag Water pool Vff Feeding Area DDT • Scale Perch DDT Perch Observation window Ii rib‘ Ledge Staging Area I Observation window 6 " is olette" nestboxes Figure 7. Overhead view of flight pen in the Ventana Wilderness Area, 2003. The dimensions of the flight pen are 12.2 m x 7.6 m x 9.1 m. The flight pen is equipped with a double door trap (DDT) which is used in capturing free-flying condors and releasing condors into the wild. In addition, the facility houses six "isolette" nest boxes of approximately 1.2 m x 1.8 m x 1.8 m where condors are placed prior to release into the flight pen, or where they are trapped prior to transfer to another facility. There are two observation windows. 39 DDT Scale Ledge Snag P erch 12.2m Figure 8. Side view of flight pen in the Ventana Wilderness Area. The side view shows where many of the favorite perches are located within the pen. The flight pen in situated on a sloping hillside overlooking the Pacific Ocean above Big Sur, California. 40 The 2003 cohort made its final move on 10 September 2003 to Pinnacles National Monument in San Benito County, California. The flight pen was situated on the side of a hill, isolated from humans. The dimensions of the pen were 15.8 m x 10.1 m, with a maximum height of 6.1 m (Figure 9). The pen was otherwise similar to that of Ventana. The condors were observed with their same mentor from 17-19 September 2003 (three observation days). The total number of observation days for this group of juveniles was 49. Individuals in this group were mentored an average of 454 days (401-499 days) before being released into the wild at PNM between 20 December 2003 and 5 January 2004. The adult mentor was not released with the juvenile California Condors and was retained to mentor future juvenile cohorts. This was the first group of California Condors to be released at PNM. 41 Snag Hot pole Scale Perch Water pool z DDT Perches Feeding Area Observation Room I Scale Perch Ledge Observation Windows Staging 6 "isolette" nestboxes Area /A Release Gate •Door Hallway Door Door Figure 9. Overhead view of flight pen at Pinnacles National Monument, 2003. Flight pen dimensions are 10.1 m x 15.8 m x 6.1 m. The observation station measures 3.7 m x 4.9 m x 2.4 m. 42 Cohort 2 (2004) Juveniles (4 hand- and 1 parent-reared) were initially placed with mentors at SDWAP between 10 September and 20 October 2003. This group was observed from 11 November through 8 December (8 observation days). We observed eight condors in two separate pens. The first pen (24.4 m x 12.2 m x 6.1 m; Figure 10) held one mentor (Ad- 141, female, hand-reared) and seven juveniles, whereas the second (3.0 m x 3.0 m x 3.0 m; Figure 11) held two adult foster parents (Andean Condors, Vultur gryphus) and one juvenile. Because of taxonomic and behavioral similarities, Andean condors have been used as surrogates in the captive-breeding program. Cross-fostering has been used successfully in captive-breeding programs for a number of endangered bird species (e.g., Conway, 1980; Hutchins et al., 1997; McLean, 1997; Sanz and Grajal, 1997; Jones, 2004; Craig et al., 2004). Observational data were collected only from the five birds scheduled to go to the Hopper Mountain release site (see below). All of the juveniles (including the three scheduled originally to go elsewhere) were transported to Hopper Mountain Wildlife Refuge Complex on 10 December 2003 and were observed with their new mentor (Ad-36, female, hand-reared) from 6 January through 29 April 2004 (22 observation days). Two of the three individuals excluded from behavior analysis were transferred to another release site on 4 March 2004. The dimensions of the flight pen were 9.1 m x 14.6 m x 6.1 m (Figure 12). The remaining six condors were transferred to Ventana on 29 June 2004, but were not studied at this latter location. Much like the first cohort in 2003, the adult mentor was not transferred to Ventana or released with the juvenile California Condors. 43 CP 91 95 96 CP 87 93 38 CP 81 3 41!,1111.. Entrance Figure 10. Overhead diagram of Condor Flight Pen at the San Diego Wild Animal Park. During season 2, most of the study birds were housed in pen #89. The measurements of this pen are: 24.4 m x 12.2 m x 6.1 m. In each adjoining pen, other California Condors were housed. The pen had numerous perching areas, an electrified power pole for aversive training, and a large water pool. 44 i- iime..Pens Figure 11. Over-head diagram of Hospital Quarantine Pen at San Diego Wild Animal Park. Three of the study birds were housed in quarantine pen # 2 because of shortage of space. The approximate measurements of this pen are: 3 mx3mx 2.4 m. The quarantine pen is small and has one perching area and a water pool the birds drink from at will. Quarantine pen 1 was empty. 45 Door Figure 12. Overhead view of flight pen at Hopper Mountain National Wildlife Refuge Complex, 2004. The dimensions of the flight pen are 9.1 m x 14.6 m x 6.1 m. Unlike Ventana and Pinnacles, the flight pen at Hopper is not built on a hill and is relatively level. 46 The total number of observation days for this group of juveniles was 30. Juveniles were released into the wild on 25 September 2004. The average duration of mentoring for individuals in this group was 340 days (287-377 days). Social Behaviors The observational method we used was the one-zero (time-sampling) method (Altmann, 1974; Bart, 2000). For consistency, all observations were made by a single investigator (ACU). The investigator observed one condor for a 20 min period before moving to another focal bird (Appendix A; Altmann, 1974; Bart, 2000). During each sample period, objectively defined behaviors were recorded for the focal bird, including other birds with which the focal bird interacted. Seventeen behaviors were recorded, as defined in Table 1; these were classified as affiliative, agonistic, solitary, or feeding (c.f. Rhine and Flanigan, 1978; Tarou et al., 2000; Schiilke and Kappeler, 2003; Appendix A). We included only one feeding behavior (feeds alone) because of inconsistency recording feeding in a group during the two years and because other recorded behaviors (particularly agonistic ones) frequently accompanied group feeding. Sample periods were randomly distributed throughout the day (0700-1700) until each bird was observed once. The sequence of focal subjects was also randomized each day (Appendix B). Data from individual birds were pooled across all days of observation to give mean frequencies (acts per hour) of each behavior for each of the two mentoring phases (SDWAP and release site). For cohort 1, observations from both the Ventana and Pinnacles release sites were combined. For cohort 2, data were collected only at Hopper Mountain. 47 Table 1. Definitions of mutually exclusive behaviors quantified in California Condors. Category Behavior Definition Affiliative Seeks/is proximate Focal bird becomes within or less than a wing's length of other to other(s) (s). Or focal bird actually is proximate (less than or equal to a wing's length) of other (s), when observation starts. Is sought by/is proximate Focal bird is the recipient of another bird becoming to other(s) proximate, with the same distance criteria as above Near to other(s) Focal bird is greater than wing's length, but less than or equal to 3.3 m from others. Example: on same perch as others, but greater than wing's length. Preens other(s) Focal bird preens other for 3 or more consecutive seconds. Is preened by other(s) Focal bird receives preening from other(s) Pulls feather, nibbles, Focal bird exhibits mild aggression or play behavior; not nudge other(s) serious Receives feather-pull, Focal bird is the recipient, same description as above nibbles, nudge from other(s) Agonistic Displaces/avoided by Displacement: Focal bird approaches and takes over another other(s) bird(s) perch, food, play object, preening partner, etc. Is Avoided: Other bird maintains a consistent distance from focal bird, therefore avoiding any actual displacement behavior. Is displaced or avoided by Focal bird is actually displaced from a perch, proximity of other(s) another bird, a food item, preening partner, play object, etc. Focal bird avoids another bird by maintaining a consistent distance to the other bird, therefore avoiding any actual displacement behavior. Non-contact-aggresses Focal bird makes threatening behavior that does not include other(s) any physical contact. Examples include: raising scapular feathers head down threat, head up treat, lunges, chases, attempts at biting, pecking, or striking with wing or foot, etc Receives non-contact Focal bird receives any threatening behavior that does not aggression from other(s) include physical contact. Examples include: raising scapular feathers head down threat, head up threat, lunges, chases, attempts at biting, pecking, or striking with wing or foot, etc. Contact-aggresses other(s) Focal bird aggresses other bird and actual physical contact is made. Examples include: biting, pecking, striking or landing on another bird, moving another bird's head away with aggressors own head or beak, etc. May precede or follow non- contact aggression Receives contact Focal bird is the recipient, same as above aggression from other(s) Solitary Leaves other(s) Focal bird leaves other (creating a distance greater than 3.3 m) Is left by other(s) Focal bird is left by other bird (s) creating a distance of greater than 3.3 m) Distant from other(s Focal bird greater than 3.3 m from others, including as far from all other birds as possible: solitary Feeding Feeds alone (no one is All other birds are 3.3 m or greater distance from focal bird proximate or near) 48 Dominance Relationships We chose to examine dominance relationships because dominance hierarchies are important in learning about sociality, priority of access to resources, and consequences of individual variation in fitness (Newmark, 2000; Hansen and Slagsvold, 2004). Dominance is defined as an attribute of the pattern of repeated, agonistic interactions between two individuals, characterized by a consistent outcome in favor of the same dyad member and a default-yielding response of its opponent rather than escalation (DeVries, 1995). Dominance relationships were evaluated among the six juveniles and one adult housed together in cohort 1 (pooling data for both the Ventana and Pinnacles release sites) and among the five juveniles and one adult housed together in cohort 2 (at Hopper Mountain). Only at the release sites were a sufficient number of birds housed together for analysis. We selected three pairs of agonistic behaviors for dominance analysis: 1) "displacement/avoidance" included focal bird displaces or is avoided by other(s) and focal bird is displaced or avoids other(s); 2) "non-contact aggression" included focal bird non-contact-aggresses other(s) and focal bird receives non-contact aggression from other(s); and 3) "contact aggression" included focal bird contact-aggresses other(s) and focal bird receives contact aggression from other(s). These three pairs of agonistic behaviors were also combined to create a fourth measure, "combined dominance." Dominance interactions resulted largely from squabbles over perch use and group feeding. For each of the four dominance measures, we created two dominance interaction matrices, one for each cohort. Dominance analyses were conducted following DeVries (1995), using MatMan 1.1 (Noldus Information Technology, 2003) with 10,000 randomizations to compute an index of linearity (Landau's h) that ranged from 0-1, with 49 a value of 1 indicating perfect linearity. Both cohorts met or exceeded the minimum number of six individuals recommended for analysis (Lehner, 1979; Appleby, 1983; Martin and Bateson, 1993). The dominance rankings from the MatMan analyses allowed us to test four hypotheses: 1) that a dominance hierarchy existed for each of the two cohorts; 2) that there was concordance among the four measures of dominance; 3) that adults were more dominant than juveniles, as observed in other similar species (Wallace and Temple, 1987; Kirk and Mossman, 1998; Snyder and Snyder, 2000; Donazar and Feij6o, 2002); and 4) that puppet-reared juveniles were equal in dominance to parent- reared juveniles. We could not test the hypothesis that male and female juveniles had equal dominance because all six juveniles in the 2003 cohort were male and four of the five juveniles in 2004 were female, thus confounding year and sex representation. In the Results, we provide Landau's h for all four measures, but present relationship diagnostics only for the fourth measure of combined dominance. Statistics For juveniles, we pooled individuals from the two cohorts and used 2 x 2 repeated-measures analyses of variance (ANOVAs) to evaluate rearing method and mentoring phase for each of the 17 behaviors. Rearing method was treated as a between- subjects factor with two levels: puppet-reared (N = 6) and parent-reared (N = 5). Mentoring phase was treated as a within-subjects factor with two levels: SDWAP and release site. All data were rank-transformed to better meet parametric assumptions. Effect sizes (partial q2 values) were computed to indicate the proportion of variance in each behavior explained by each of the two main effects and their interaction (Mertler and 50 Vannatta, 2004). To evaluate the collective effects of rearing method and mentoring phase, we used a sign test to compare the partial 112 values of all 17 behaviors. We also pooled adult mentors during the two years and used two-tailed Mann- Whitney U tests to compare behaviors of puppet- versus parent-reared adults at SDWAP and to compare behaviors at SDWAP versus release sites. Because one adult was used both years at SDWAP (Ad-141), data from this individual were averaged for the two years. We tested hypotheses regarding dominance hierarchies using non-parametric tests (Conover, 1999). Probabilities for dominance hierarchies were computed separately for each cohort by MatMan (DeVries, 1995; Noldus Information Technology, 2003), which provided a P-value for whether a significant hierarchy was detected. After dominance rankings for all individuals of the two cohorts, we assessed correspondence among the four measures of dominance with Spearman correlation coefficients. We also used Mann- Whitney U tests to compare dominance rankings between adults versus juveniles (one- tailed) and between puppet-reared versus parent-reared juveniles (two-tailed). Apart from the dominance analyses requiring MatMan, all statistical tests were conducted using SPSS v. 12.0 (SPSS, 2003) with alpha = 0.05. Results Juveniles: Rearing Method versus Mentoring Phase The 17 social behaviors recorded from juveniles are summarized in Table 2. Among the four behavioral categories (Table 1), the three solitary behaviors collectively were exhibited most often (ca. 44 acts/hr), with "distant" being the most frequent (ca. 41 51 acts/hr; Table 1). The seven affiliative behaviors were also exhibited often (ca. 28 acts/hr), with seeks, is sought, and near being the most frequent. The six agonistic behaviors were exhibited less often (<7.5 acts/hr), and the one feeding behavior (feeds alone) was the least frequent category (<2.1 acts/hr). Two behaviors revealed a significant interaction between rearing method and mentoring phase: pulls feathers (P = 0.015, partial 1/12 = 0.50) and feeds alone (P = 0.008, partial 12 = 0.57). For both behaviors, parent-reared condors engaged in these activities more often at the zoo and less often at the release pens than did the puppet-reared condors (Figure 13). The main effect of rearing method was significant for two additional behaviors: near other(s) (P = 0.01, partial i 2 = 0.52) and receives contact aggression (P = 0.03, partial I/2 = 0.42). Parent-reared birds were more likely to be near another bird and receive contact aggression, regardless of mentoring phase, than puppet-reared birds (the mean values of receive contact aggression for puppet- and parent-reared birds at the release site were equivalent in Table 2, but the rank scores were higher for parent-reared birds). Importantly, none of the behaviors showed a significant main effect of mentoring phase. All of the effect sizes for mentoring phase were remarkably small (partial 112 < 0.01; Table 2), suggesting that social behaviors were similarly expressed under the different social environments. Rearing method, in contrast, had a more measurable difference in behaviors, with the effect size of eight behaviors exceeding 0.10. When comparing effect sizes for the main effects of rearing method and mentoring phase, 16 of the 17 behaviors had more variance explained by rearing method (Table 2). A two-tailed sign test indicated that this proportion was highly significant (P < 0.001) 52 Table 2. Mean (2-c, ± 1 S.E.) acts per hour for each of 17 social behaviors exhibited by juvenile California Condors. Release sites SDWAP Rearing method Mentor phase Interaction Behaviors Puppet Parent Puppet Parent 112P SE jc± SE 5-c ± SE j-c± SE P 112 P 12 Seeks 8.28 ± 2.10 6.50 ± 2.02 7.13 ± 2.47 7.13 ± 2.47 0.341 0.101 0.945 0.001 0.457 0.063 Is sought by others(s) 5.55 ± 3.18 10.90 ± 6.61 4.22 ± 1.12 3.86 ± 0.91 0.591 0.033 0.895 0.002 0.168 0.200 Near other(s) 7.58 ± 3.13 13.45 ± 6.72 9.08 ± 5.53 13.37 ±3.20 0.012 0.521 1.000 0.000 1.000 0.000 Preens other(s) 0.60± 0.20 1.14± 1.33 0.14 ± 0.10 0.15 ±0.04 0.339 0.102 0.987 0.000 0.863 0.004 Is preened 0.64 ± 0.34 1.11± 1.48 0.14 ± 0.10 0.19 ± 0.12 0.821 0.006 0.943 0.001 0.441 0.067 Pulls feathers 1.43 ± 0.81 3.05 ± 1.45 0.74 ± 0.36 0.53 ± 0.28 0.725 0.014 0.791 0.008 0.015 0.500 Receives feather pull 1.30 ± 0.97 2.23 ± 1.2 0.76 ± 0.47 0.53 ± 0.26 0.754 0.001 0.895 0.002 0.178 0.198 Displaces other(s) 0.34 ± 0.21 0.87 ± 0.86 0.18 ± 0.23 0.16 ± 0.12 0.478 0.058 0.982 0.000 0.804 0.007 Is displaced 0.82 ± 0.80 2.45 ± 1.31 0.12 ± 0.11 0.14 ± 0.11 0.060 0.339 0.917 0.001 0.271 0.133 Non-contact aggresses other(s) 0.53 ± 0.21 1.09 ± 1.39 0.30 ± 0.19 0.22 ±0.12 0.690 0.019 0.958 0.000 0.565 0.038 Receives non-contact aggression 0.56 ± 0.30 1.31 ± 1.30 0.20 ± 0.13 0.15 ± 0.10 0.496 0.053 0.883 0.003 0.131 0.235 Contact-aggresses other(s) 0.32± 0.29 0.81 ± 0.42 0.11 ± 0.07 0.10 ± 0.02 0.172 0.197 0.886 0.002 0.139 0.227 Receives contact aggression 0.23 ± 0.23 0.87 ± 0.29 0.08 ± 0.02 0.08 ± 6.04 0.031 0.421 0.902 0.002 0.198 0.177 Leaves other(s) 1.47 ± 0.98 3.00 ± 0.95 0.67 ± 0.40 0.55 ± 0.17 0.146 0.220 0.874 0.003 0.106 0.264 Is left by other(s) 1.71 ± 1.50 3.03 ± 1.61 0.67 ± 0.30 0.75 ± 0.14 0.078 0.306 0.975 0.000 0.729 0.014 Distant 40.76 ± 4.52 43.60 ± 5.99 39.57 ± 3.55 38.37 ± 2.43 0.827 0.006 0.893 0.002 0.161 0.206 Feeds alone 0.54 ± 0.71 2.04± 1.72 0.77 ± 0.78 0.18 ± 0.19 0.667 0.021 0.762 0.011 0.008 0.566 Juveniles are compared for rearing method (puppet-reared, N = 6; parent-reared, N = 5) and mentoring phase (San Diego Wild Animal Park, SDWAP; flight pens at release sites). Analysis of variance (ANOVA) results include P-values and effect sizes (partial 172). Values in bold are significant at P=0. A. B. Figure 13. Mean (± 1 S.E.) social acts/hour by juvenile California Condors, illustrating interactions between rearing method (E = puppet-reared; E= parent-reared) and mentoring phase [San Diego Wild Animal Park (SDWAP) and flight pens at release sites]. Social behaviors include A) "pulls feather, nibbles, nudge other(s)" (P = 0.015, partial 712 = 0.500) and B) "feeds alone" (P = 0.008, partial 112 = 0.566 54 Adult Mentors: Rearing Method versus Mentoring Phase Although not compared statistically, the rates of behavioral acts exhibited by adult mentors were similar to those of juveniles. At the SDWAP, parent-reared mentors (N = 3) were more aggressive than puppet-reared mentors (N = 2) for three agonistic behaviors (Table 3). Otherwise, the rates of behavioral acts by puppet- and parent-reared mentors were similar. When the puppet- and parent-reared mentors at the SDWAP were pooled (N = 5), they exhibited similar rates of behavioral acts as the two mentors at the release sites (though several acts approached significance; Table 3). Dominance Rankings Index of linearity values among the four measures of dominance ranged from 0.17-0.86 (Table 4). Displacement/avoidance was the only measure yielding significant linearity for both cohorts (h' > 0.77, P < 0.038 in both cohorts). Contact aggression was the weakest indicator of dominance (h' < 0.48 in both cohorts). For combined dominance, linearity was significant for cohort 1 (h' = 0.86, P = 0.018) but weaker for cohort 2 (h' = 0.63, P = 0.21). Linearity was weakened by the preponderance of two-way relationships (93.3-100%; Table 5), in which both individuals of an interacting pair showed dominance in some but not all encounters (Table 6). Concordance among the four dominance measures was mixed. Two measures, displacement/avoidance = 0.82, P = 0.001) and non-contact aggression (r5 = 0.55, P = 0.050), were positively correlated with combined dominance; however, no other correlations were detected among the measures. 55 Table 3. Mean ± 1 S.E.) acts per hour for each of 17 social behaviors exhibited by adult puppet-reared and parent-reared California condors that served as mentors to juveniles. Different mentors were used during the two mentoring phases [San Diego Wild Animal Park (SDWAP) and flight pens at release sites] and results were pooled over the two cohorts. Outcomes are from two-tailed Mann-Whitney U tests. Values in bold are significant at P=0.05 Release Rearing Rearing SDWAPa sites(s)b method phase Behaviors Puppet Parent Puppet (N=2) (N=31 (N=2) ± 1 S.E.) ± 1 S.E.) (,± I S.E.) Seeks 11 .58 ± 4.06 16.48 ± 7.02 6.31 ± 3.24 0.480 0.245 Is sought 4.52±0.33 6.89 ±4.26 2.00 ± 0.38 0.724 0.121 Near 11 .13 ± 0.07 16.30 ± 4.50 9.60 ± 6.63 0.480 0.699 Preens others 0.28 ± 0.28 0.31± 0.17 0.01 ± 0.01 0.578 0.417 Is preened 0.28 ± 0.28 0.25 ± 0.07 0.00 ± 0.00 0.271 0.108 Pulls feathers 1.16 ± 0.73 1.65 ± 0.56 0.12 ± 0.03 0.077 0.053 Receives feather-pulls 2.35 ± 1.59 1.89± 0.61 0.15 ± 0.09 0.480 0.053 Displaces others 2.88 ± 0.88 1.72 ± 0.95 0.42 ± 0.01 0.724 0.245 Is displaced 0.04 ± 0.04 0.42 ± 0.28 0.01 ± 0.01 0.271 0.421 Non-contact-aggresses 1.26 ± 0.05 126 ± 0.50 0.35 ± 0.13 0.034 0.053 Receives non-contact 0.63 ± 0.19 2.04 ± 0.70 0.16 ± 0.04 0.034 0.053 Contact-aggresses other 0.54 ± 0.16 0.80 ± 0.17 0.15 ± 0.02 0.077 0.053 Receives contact 0.39 ± 0.11 0.94 ± 0.29 0.06 ± 0.04 0.034 0.053 Leaves 2.00± 1.01 3.28 ± 1.65 0.41 ± 0.00 0.154 0.053 Is left 3.09± 1.24 3.38 ± 0.65 0.58 ± 0.08 0.157 0.053 Distant 42 .62± 1.30 36.84 ± 5.96 42.29 ± 2.63 0.480 0.699 Feeds alone 1.29 ± 0.78 0.24 ± 0.24 0.16 ± 0.14 0.285 0.696 a Comparison of puppet- (N= 2) and parent-reared (N = 3) adults at SDWAP b Comparison of SDWAP (N =5) vs. release site (N = 2) 56 Table 4. Dominance rankings of individuals from (A) Cohort 1 and (B) Cohort 2 for each of the four dominance indicators. Tag identification (ID), Age (Ad = adult, Juv = juvenile), sex (d,Y), and rearing method (PP = puppet- and PT = parent-reared) are indicated for each bird. Cohort 1 (2003) Dominance behaviors Non-contact Contact- Displacement/ Combined Tag ID Individual birds aggression aggression Avoidance dominance 63 (Ads-PP) 1 4 1 1 265 (Juv c3'-PP) 2 7 5 2 266 (Juv 5-PP) 4 1 2 3 278 (Juv c3'-PT) 6 2 3 4 287 (Juv d-PT) 5 3 4 5 270 (Juv c3'-PT) 3 5 6 6 286 (Juv d-PT) 7 6 7 7 Linearity index h' a 0.68 0.48 0.77 0.86 P-value 0.064 0.34 0.028 0.018 Cohort 2 (2004) Dominance behaviors Non-contact Contact- Displacement/ Combined Tag ID Individual birds aggression aggression Avoidance dominance 301 (Juv s-PT) 2 2 1 1 36 (Ad?-PP) 3 4 2 2 311 (Juv y -PP) 1 5 3 3 303 (Juv ?-PP) 4 6 5 4 298 (Juv ?-PP) 5 1 4 5 294 (Juv 9-PP) 6 3 6 6 Linearity index lf a 0.40 0.17 0.86 0.63 P-value 0.51 0.92 0.038 0.21 a Landau's linearity index, corrected for unknown relationships. 57 Table 5. Relationship diagnostics from dominance hierarchy analysis of "combined dominance" (a measure derived by pooling three pairs of agonistic behaviors). Cohort 1 (2003) Cohort 2 (2004) Sample size (N) 7 6 Matrix total 290 240 Linearity index h' (corrected for 0.86 0.63 unknown relationships) Expected value of h' 0.38 0.43 Directional consistency index 0.43 0.37 Number (%) of unknown 0(0) 0(0) relationships Number (%) of one-way 0 (0) 1 (6.67) relationships Number (%) of two-way 21(100) 14 (93.33) relationships Total number of dyads 21(100) 15 (100) Number (%) of tied 0 (0) 1 (6.7) relationships Significance * 0.018 0.21 * Linearity index h' vs. expected, based on 10,000 randomizations (DeVries, 1995). 58 Table 6. Dominance matrix indicating frequency of combined dominance interactions for cohort 1 (observed 60.67 hours, 4.78 interactions/hr) and cohort 2 (observed 44 hours; 5.50 interactions/hr). Cohort 1 (2003) Recipient Actor 63 265 266 278 287 270 286 63 * 13 8 10 8 24 18 265 2 * 3 9 3 14 7 266 2 1 * 6 4 7 5 278 2 1 1 * 11 13 4 287 5 10 2 8 * 15 6 270 5 9 4 3 9 * 12 286 3 5 4 3 4 7 * Cohort 2 (2004) Recipient Actor 301 36 311 303 298 294 301 * 8 3 14 9 13 36 7 * 18 6 16 16 311 3 7 * 2 5 8 303 7 2 1 * 10 15 298 8 0 3 8 * 21 294 1 7 9 7 7 * 59 The two adults and 11 juveniles had similar combined dominance rankings (5-c = 1.5 and 4.2, respectively), though the difference approached significance (Mann-Whitney one-tailed exact P = 0.052). The adult mentor for cohort 1 (Ad-63) was ranked most dominant, whereas the mentor for cohort 2 (Ad-36) was second-most dominant (Table 4). The puppet-reared (N = 6) and parent-reared (N = 5) juveniles also had similar combined dominance rankings = 3.8 and 4.6, respectively; Mann-Whitney two-tailed exact P = 0.43). Discussion The most important outcome of this study was that rearing method appeared to have a small but measurable effect on the social behaviors of juvenile condors. Four of the 17 behaviors recorded had significant effects involving rearing method or an interaction between rearing method and mentoring phase. In spite of the condors experiencing very different physical and social environments during the two mentoring phases (SDWAP versus release sites), the main effect of mentoring phase explained a relatively small proportion (1% or less) of variance in all of the behaviors measured. In contrast, the main effect of rearing method consistently explained far more variance (up to 52%), and effect sizes for interactions were often substantial as well (up to 57%). Because of the small sample sizes for the analyses we employed, effect sizes (practical significance) may be more meaningful than statistical significance (Mertler and Vannatta, 2004). Some of the differences between puppet- and parent-reared juveniles suggest that the former were less social or adjusted more slowly to the social condor hierarchy. 60 Puppet-reared juveniles were less likely to be near another bird and to receive contact aggression, regardless of mentoring phase, than parent-reared juveniles. Puppet-reared juveniles fed alone more often at the release pens, where they were forced to interact with more individuals than at the SDWAP pens, which housed fewer birds together. The puppet-reared juveniles also engaged in less feather-pulling, an affiliative behavior, at the release pens. These behaviors could potentially translate to poorer social skills in the wild, including success during group feeding on carcasses. The general impression exists that parent-reared birds seem more confident when first released, but the puppet-reared juveniles seem to catch up quickly (M. Stockton, pers. comm.; Nielsen, 2006; Woods et al., 2007). However, empirical data are lacking. Differences between puppet- and parent-reared adult mentors were also detected. Parent-reared mentors at the SDWAP were significantly more aggressive, though sample sizes were small. The implication that behavioral differences may be long-term justifies the need for further study. Although the measure of linear dominance hierarchy we computed, Landau's h, proved to be significant for just one of the two cohorts, we suspect that further study would reveal formation of such a hierarchy among captive California Condor groups, as has been observed in captive and recently released Turkey Vultures (Cathartes aura; Kirk and Mossman, 1998). A study similar to ours (Bukowinski et al., 2007) concluded from MatMan analysis that a perfect linear hierarchy existed among a mentor and four juvenile California Condors (Landau's h = 1.0); however, the sample size was below the minimum recommended (N > 6) for the test to accurately test dominance (Lehner, 1979; Appleby, 1983). In our study, condor relationships may have been dynamic and not yet 61 stabilized, particularly among the juveniles. Because of their fluid nature, linear relationships seem less likely to be maintained in the wild (Kirk and Mossman 1998). Our ability to detect dominance of adults over juveniles was limited by sample size (just two cohorts), though the difference approached significance. In a third cohort of California Condors studied by Bukowinski et al. (2007), the adult was also most dominant. Unfortunately, we were unable to test for sex-based dominance. Dominance relationships are commonly reported among other scavengers (vultures and condors), and may be related to species (for interspecific interactions), sex, age, body size, kinship, prior use of carcass, satiation level, daily food expectation, and probably costs and benefits of agonistic interactions (e.g., Wallace and Temple, 1987; Kirk and Mossman, 1998; Buckley, 1999; Donazar and Feijoo, 2002). In Andean Condors, age-related dominance (older dominant) was followed by sex-related dominance (male dominant to female; Donazar and Feijoo, 2002). Unlike Andean Condors, California Condors are not sexually dimorphic, which could diminish dominance differences between sexes. Crested Caracaras (Carcara cheriway) sometimes exhibit a reversed dominance pattern, with juveniles dominating adults at carcasses, but this may result from familial relationships with parents tolerating more aggressiveness from their own offspring (Rogriguez-Estrella and Rivera-Rodriguez, 1992). We emphasize that the dominance hierarchy analyses were not the primary goal of this study, and that a more thorough examination of California Condor dominancy relationships should be undertaken, particularly with regard to age, sex, and body size. The release of relatively young captive-reared California Condors is the prevailing trend in the reintroduction program, with 13 months as the average age at 62 release (Mace, 2006). By comparison, juvenile condors in the wild can spend up to 18-20 months with their parents before cutting ties (Snyder and Snyder, 2000). Over the last nine years (1996-2005), the age of California Condor juveniles at release has increased from an average of nine to 17 months (Appendix F; Mace, 2006). Over this same period, recapture rates for behavior problems dropped (13 of the 17 behavioral incidents occurred between 1996 and 2000). This trend may be attributed to at least three factors: adult mentoring, post-release population in the wild, and older age at release (Hutchins et al., 1997; Woods et al., 2007). In a companion study relying on binary logistic regression (Chapter 3), we identified adult mentoring and post-release population size in the wild as being important factors for juvenile condor survival within the first two years after release. Age at release did not influence outcome. Based on Griffon Vulture, Gyps fulvus, studies in Southern France, Sarrazin and Legendre (2000) suggest that, for species in which sociality may play a role in foraging and breeding, the effect of release strategy on age structure may be important. Often, in reintroduction programs, young individuals (which have a higher mortality rate when reintroduced) are believed to be less affected by captivity, whereas adults (who have a better survival rate) have a more marked effect from the long-term captivity (Sarrazin and Legendre, 2000). It has been suggested that animals that are removed from the wild and reared in captivity can change behaviorally and become significantly different from wild populations and may have problems with foraging, avoiding predators, and competing with conspecifics (Hutchins et al., 1997; Gippoliti, 2004; Snyder and Snyder, 2005). Results of the study on Griffon Vultures concluded that the release of adults may be the most efficient strategy for long-lived 63 species having low expected release costs (reduced survival and reproduction; Sarrazin et al., 1994; Sarrazin and Legendre, 2000). Future Considerations Understandably, some feel that the longer a California Condor spends in captivity, the more acclimatized it becomes to human activities, structures, and sounds (i.e., becomes domesticated; Snyder et al., 1996; Snyder, 2005). Snyder et al. (1996) proposed having rearing facilities built in situ (in areas of original habitat) and separate from multi- species facilities (zoos), although this may not be practical for endemic species in developing countries (Gippoliti and Carpaneto, 1997). However, it has been shown that other reintroduction programs have succeeded through captive-bred animals born in zoos (e.g., the Bearded Vulture, Gypaetus barbatus, released in the Alps; Gippoliti and Carpaneto, 1997; Gippoliti, 2004). Furthermore, zoos have a very important role in wildlife conservation through public education and awareness, research, and in situ conservation programs (Gippoliti and Carpaneto, 1997). Future comparisons of the success of condors from different breeding facilities may shed further light on the influence of rearing conditions. Two of the facilities are at public zoos (San Diego Wild Animal Park and Los Angeles Zoo), where their close proximity to exhibit areas exposes the young birds to considerable human noise, structures, and activities, which may influence the birds' behavior (Hutchins et al., 1997; Gippoliti, 2004; Snyder and Snyder, 2005). The two other facilities (Oregon Zoo's Jonsson Center for Wildlife Conservation, near Portland, Oregon, and The Peregrine Fund's World Center for Birds of Prey, near Boise, Idaho) are further removed from 64 human activities and may be appropriate to evaluate the "single species, closed facility" approach—a facility in natural habitat that is closed to the public (Gippoliti and Carpaneto, 1997). However, proper comparison between the two rearing conditions (strong versus minimal human influence) would require that juveniles from each category be released at the same site. Although there may be differences between rearing facilities and rearing conditions, the bigger problem with releasing captive-reared individuals into the wild is that all release sites are contaminated with garbage, lead, and other potential dangers which can strongly influence the outcome of released birds (Ebenhard, 1995; Clendenen and Prieto, 2004; McKeever, 2006). Conclusions 1. Juveniles exhibited similar social behaviors under different social contexts associated with the two mentoring phases. 2. Different rearing methods (puppet- versus parent-reared) resulted in small but measurable differences in social behaviors, with puppet-reared birds exhibiting fewer social interactions (although significant for only two behaviors). 3. Adult mentors that were parent-reared exhibited more aggression than their puppet-reared counterparts. 4. Individuals within one of the two cohorts exhibited a linear dominance hierarchy. 5. Rearing method did not affect dominance relationships, although adults were possibly dominant to juveniles (the difference approached significance). 6. Behavioral problems in captive-reared California Condors released to the wild have decreased markedly since the beginning of the reintroduction program, 65 possibly due, in part, to the mentoring program. 7. This study is the first to document measurable differences between puppet- and parent-reared captive-bred California Condor juveniles. Acknowledgments I would like to thank my fellow coauthors, Dr. William K. Hayes, Dr. Nancy Harvey, and Dr. Ronald Carter. I would also like to thank the Zoological Society of San Diego for allowing me to collect data at the San Diego Wild Animal Park. 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Lancaster: Cadmus Communications. 71 CHAPTER THREE PREDICTORS OF BEHAVIORAL PROBLEMS AND SURVIVAL FOLLOWING RELEASE OF CAPTIVE-REARED CALIFORNIA CONDORS Amy C. Uttl, Nancy C. Harvey2'3, William K. Hayes1 1Department of Earth and Biological Sciences, Loma Linda University, Loma Linda, California 92350 USA 2Center for Reproduction of Endangered Species, San Diego Zoo, P.O. Box 551, San Diego, CA 92112-0551 3Present address: 6509 Harrier Rd. Nanaimo BC V9V 1V9 Canada In preparation for publication. 72 Abstract The purpose of this study was to evaluate factors that might influence the success of captive-reared California Condors (Gymnogyps californianus) released into the wild. Two questions were particularly pertinent: are puppet-reared (a form of hand-rearing) individuals less successful than parent-reared individuals, and does adult mentoring help to ameliorate the potential behavior and survival problems often associated with the puppet-rearing method? Rearing data were obtained from San Diego Wild Animal Park and the Los Angeles Zoo, while release data were extracted from the California Condor Studbook and from interviews and surveys of release-site personnel. All birds included in this study were captive-reared and subsequently released into the wild. Two dichotomous outcomes, behavior (either normal or "misbehavior" that included affiliation with humans or man- made structures) and survival were tested after one year and after two years to assess adjustment to life in the wild. The outcomes were subjected to chi square analysis and/or binary logistic regression using the following predictor variables: sex, rearing facility, rearing method, mentoring, age at release, release site, and established population size at release site. Rearing facility and rearing method significantly affected behavior during the first year after release with San Diego and puppet-reared birds exhibiting misbehavior more • often. However, after two years, no predictors significantly affected behavior. Mentoring, sex, and established population size (>5 individuals) significantly enhanced first-year survival, whereas only mentoring and established population size enhanced 2- year survival. Survival was independent of rearing facility, rearing method, and age at 73 release, but appeared to be better at some release sites than others. These data suggest that most puppet-reared juveniles can cope well following release and that mentoring may be especially crucial for the survival of captive-reared California Condors released in the wild. 74 Introduction Captive-breeding of endangered species has become a vital tool for conservation in recent decades. Captive breeding is used to bolster population numbers, with the ultimate goal to supplement wild populations or to reintroduce extirpated or extinct species into areas of previously occupied habitat (Saint Jaime, 1999; Seddon et al., 2007). Although captive-breeding has dramatically increased numbers of many species, few reintroduction programs have been considered a success (Ebenhard, 1995; Powell et al., 1997; Griffin et al., 2000; Nicoll et al., 2004; Mathews et al., 2005; Williams & Feistner, 2006; Armstrong et al., 2007), prompting the need to develop a stronger science of reintroduction biology (Seddon et al., 2007). The mixed success of reintroduction efforts has resulted from many factors. First, some species are brought into captivity for a "last-ditch" effort, without adequate time to study their natural history and breeding behavior (Conway, 1980). This can lead to reproduction difficulties in captivity (Jones et al., 1995; Snyder et al., 1996; Curio, 1998; Lticker & Patzwahl, 2000). Second, a species may breed well in captivity, but because the original causes for decline are not ameliorated, individuals released to the wild again suffer the same fates (e.g. lead poisoning of California Condors [Gymnogyps californianus], Ebenhard, 1995; Snyder et al., 1996; Church et al., 2007; Hunt et al., 2007; Mee & Snyder, 2007). This can lead to extensive long-term management, which precludes the goal of reintroduction programs of establishing self-sustaining populations (Baillie et al., 2004; Church et al., 2006; Leech et al., 2007). Third, some species can change behaviorally or genetically after a short amount of time (or a few generations in captivity), as environmental conditions and selection pressures often differ dramatically from those in the wild (Snyder et al., 1996; Griffin et al., 2000; McDougall et al., 2006; 75 Hakansson et al., 2007). Once such changes occur, these individuals often become unsuitable for release. One of the main criticisms of releasing captive-bred animals has been the tendency toward behavioral deficiencies and inability to survive in the wild (Meretsky et al., 2000; Mathews et al., 2005). Finally, many reintroduction programs are aimed at species management with little or no research element or stated objective other than to increase population numbers (Seddon et al., 2007). Most reintroduction research has been retrospective, ad hoc, and fragmented, which has hindered development of an objective approach to identifying and addressing obstacles to success (Brightsmith et al., 2005). Research and intermittent progress evaluation are essential for any endangered species program involving reintroductions (Kleiman et al., 2000; Seddon et al., 2007). Information thus acquired encourages refinement of methods to optimize the success of reintroduced individuals. Approaching captive-breeding and reintroductions as a science eliminates much of the "guesswork" out of reintroductions. Without critical evaluation of reintroduction programs, even if retrospective, officials must often rely on prior assumptions and on anecdotes from the field, which can be biased. Like many recovery programs, the California Condor recovery program has been surrounded by controversy from its inception (Algona, 2004; Brightsmith et al., 2005). A critically endangered North American bird, the California Condor became extinct in the wild in the late 1980s after the last remaining individuals were captured and brought into captivity. Despite extensive captive-breeding and some success in reintroduction to areas of previously-occupied habitat, the program still lacks an extensive quantitative assessment. Recent studies have addressed the major threat to birds released to the wild, 76 which is lead poisoning (Meretsky et al., 2000; Parish et al., 2007; Woods et al., 2007), but few have considered other factors affecting the success of released birds. Because of this, many questions remain about the use of certain captive-rearing techniques and the suitability of individuals for release. There has been bias, for example, against birds that were puppet-reared (Meretsky et al., 2000; 2001). Several studies now suggest that social behaviors differ between birds reared by puppets and others reared by biological or foster parents (Bukowinski et al., 2007; Utt et al., 2008), but these studies, unfortunately, were not initiated until more than a decade into the Condor breeding program. The California Condor, similar to other avian species having declined in the past century, was susceptible to many external limiting factors, of which the most significant were habitat loss and lead poisoning (Koford, 1953; McMillan, 1968; Kiff, 1979; Weimeyer, 1988; Meretsky et al., 2000; Snyder, 2000; Algona, 2004; Snyder ,2005). Small clutch size (one egg) and slow maturation (5-7 years) rendered population recovery unlikely (Meretsky et al., 2000). In 1987, the remnant wild condor population (N=15) was brought into captivity to become founding members of the captive-breeding program (Stoms et al., 1993; Snyder & Snyder, 2000; Algona, 2004; Nielsen, 2006). Including birds previously taken into captivity, 27 California Condors existed, and were housed between the San Diego Wild Animal Park (SDWAF') and the Los Angeles Zoo (LAZ, Stomes et al., 1993; Toone, 1994; Algona, 2004; Harvey et al., 2004; Nielsen, 2006). Breeding pairs typically produce one chick every other year in the wild. However, breeding females may lay a second egg if the first is lost or removed, a phenomenon called "double-clutching" (Snyder & Hamber, 1985; Harvey et al., 2003; 2004; Nielsen, 2006). Breeding facilities took advantage of the female's ability to double-clutch and 77 started pulling the first egg of the season for artificial incubation, inducing the breeding pair to lay a second, and sometimes a third egg (Harvey et al., 2003; 2004; Nielsen, 2006). Generally, the first chick was raised with a condor-like puppet (a form of hand- rearing) instead of by the natural parents (Toone, 1994; Meretsky et al., 2000; Beres & Starfield, 2001; Harvey et al., 2003; Clark et al., 2007; Utt et al., 2008). The second egg of the season was then raised by a puppet (particularly early in the program) the biological parents, conspecific foster parents, or by surrogate cross-foster Andean Condors (Vultur gryphus; Toone, 1994; Wallace, 1994; Meretsky et al., 2000; Beres & Starfield, 2001; Utt et al., 2008). The method of hand-rearing (not always with a puppet) has been used successfully with other endangered bird species in captive-breeding programs, including the Whooping Crane (Grus americana), Mississippi Sandhill Crane (G. canadensis pulla), Yellow-Shouldered Amazon Parrot (Amazona barbadensis), Scarlet Macaw (Ara macao), Takahe (Porphyrio mantelli), and the Kaka (Nestor \meridionalis; DeBlieu, 1993; Wallace, 1994; Maxwell et al., 1997; Sanz et at., 1998; Ellis et al., 2000; Brightsmith et al., 2005; Kreger et al., 2006). In addition, many captive- breeding programs have used cross-fostering with desirable results, including with the Chatham Island Black Robin (Petroica traversi), Mew Gull (Larus canas), Lesser White- fronted Goose (Anser eythropus), Masked Bobwhite (Colinus virginianus), Peregrine Falcon (Falco peregrinus), Whooping Crane, and the Takahe (Cade, 1977; Carpenter et al., 1991; Reed et al., 1993; Bunin & Jamieson, 1996; Sutherland, 1999; Craig et al., 2004; Reed, 2004). Meretsky et al. (2000) and Snyder & Snyder (2000) argued that the success of California Condors released to the wild can be influenced by whether or not the chick 78 was parent-reared or puppet-reared. Preliminary evidence suggested that puppet-reared juveniles released in the wild were less successful than parent-reared juveniles (Snyder & Snyder, 2000). Prior to 1995, all condors in the captive-breeding program were hand- reared by adult California Condor-like puppets (i.e., "puppet-reared"; Snyder & Snyder, 2000; Mace, 2006). However, when the success rates for the first two years of releases fared poorly, the California Condor recovery team recommended that the second egg of the season be parent-reared, which would enable the same level of egg production while producing more parent-reared birds for release (Harvey et at., 2003; 2004). In 1995, parent-rearing was instated at SDWAP and LAZ (Harvey et al., 2003). In addition to producing more parent-reared California Condor juveniles for release, the condor-breeding facilities at the SDWAP and LAZ established a mentoring program in 1999, whereby one or more juveniles were housed with one or more adult (>5 yr age), non-parent condors in an isolated pen prior to release, at either the rearing facility, release site, or both (Kaplan, 2002; Bukowinski et al., 2007; Utt et at., 2008). In some social species, development of normal behavior may depend on an association with the parents or other adult birds during particular stages of maturation (Hutchins et at., 1995; Snyder et al., 1996; Meretsky et al., 2000; Algona, 2004). Thus, condor recovery officials hoped that mentoring would ameliorate puppet-rearing effects, and improve the success of all released fledglings (Ettinger, 2005; Bukowinski et at,. 2007; Clark et al., 2007; Utt et al., 2008). The purpose of this study was to evaluate possible factors influencing the success of captive-reared California Condors released to the wild. Two primary questions were raised: 1) Are puppet-reared condors less successful than parent-reared condors, and 2) Does mentoring reduce behavioral and survival problems in the wild? We employed both univariate and multivariate analyses to examine the predictors of two important indicators of adjustment to life in the wild: behavior (either normal or "misbehavior" that included affiliation with humans or man-made structures) and survival. Although retrospective, the findings of this study provide valuable insights on the success and validity of reintroduction methods in general. They inform the California Condor recovery program in particular, providing an evidence-based rationale for refining the management, husbandry, and reintroduction practices. Materials and Methods Our analyses were based on data collected and compiled from various sources, with every reasonable effort undertaken to maintain accuracy. All decisions regarding husbandry, housing, transfers, releases, and recaptures were made by zoo officials and/or key members of the Condor Recovery Team; we had no involvement. We acknowledge that, in the absence of a formalized research program, implementing these decisions may have lacked consistency. Data Compilation We compiled a data set from 109 juvenile California Condors released during the period 1996-2004. We omitted birds released prior to 1996, which were in the early phase of the reintroduction program when only puppet-reared birds were available. Rearing data were gleaned from institutional rearing records (SDWAP and LAZ). Release data were obtained from the California Condor Studbook (Mace, 2006) and from interviews and surveys of release site officials. Juveniles were released at each of five primary release 80 sites: Hopper (including Bitter Creek, Lion, and Castle), Ventana, and Pinnacles in California, Vermillion Cliffs in Arizona, and Parque Nacional Sierra de San Pedro Martir in Baja California Norte, Mexico. An additional 50 juveniles reared at The Peregrine Fund during this period were not included in this study because records were not made available for analysis (c.f. Walters et al., 2008). Juveniles that we regarded as "parent-reared" were raised by a pair of biological parents, conspecific foster parents, or Andean Condor cross-foster parents. Although we recognize that differences may exist, we assumed that juveniles raised by each of these parent groups (hereafter "conspecific/parent-reared" and "cross-foster parent-reared") were similar (Wallace, 1994), as supported by our own analyses (see Results). "Puppet- reared" juveniles were raised by a California Condor-like puppet model (Wallace, 1994). Mentoring involved placing a juvenile with one or more adult California Condors that were not considered a parent for a variable period of time prior to release (Bukowinski et al., 2007; Utt et al., 2008). Although implemented for puppet-reared juveniles in an effort to improve their social skills, both parent- and puppet-reared juveniles were subjected to mentoring, either at the rearing facility, release site, or both. Often, both parent- and puppet-reared juveniles were placed in a group for socialization purposes with one or more adult mentors (Bukowinski et al., 2007; Utt et al., 2008). Most juveniles early in the captive-breeding program lacked mentoring, which was gradually phased in beginning in 1999. For each released condor, we determined both the presence/absence of mentoring and the duration of mentoring (in days) prior to their release. We surmised that the presence and size of an established group of condors at release sites might influence the behavior and success of newly released individuals 81 (Matson et al., 2004). From the Studbook and queries of release officials, we ascertained the number of surviving condor individuals at each release site (including birds raised by The Peregrine Fund) at the time of each release (Table 7). Two dichotomous outcomes were of interest in this analysis: behavioral problems and survival in the wild. A behavioral problem (present or absent) was defined, by proxy, as recapture of a released bird because of inappropriate behavior. Behavioral problems included attraction to and destruction of human structures, approaching humans, or allowing humans to approach without showing fear (Snyder & Snyder, 2000; Meretsky et al., 2000; Neilson, 2006). Initial roosting on the ground (a habit formed in captivity but soon discontinued in the wild) and use of power poles (typical raptor behavior) were not considered inappropriate behavior. Survival (lived or died) was defined as whether a released bird was still alive after a specified endpoint. Behavioral problems and survival were analyzed at the end of each of the first and second years in the wild. If a bird remained in the wild <3 months during the year and was removed for a reason unrelated to behavior, we excluded it from the behavioral analysis for-that year. Some birds, as a result of behavioral problems, illness, or injury, were recaptured and returned to captivity for a period of time. Birds not returned to the wild within 2 months were excluded from the survival analysis for that year. If a bird misbehaved or died during the first year, it was also coded as having misbehaved or died at the end of the second year (i.e., outcomes were cumulative). 82 Statistical Analyses We initially examined dichotomous outcomes (behavioral problems, survival) by Chi-square analysis for each of five categorical predictors: sex, rearing facility (SDWAP and LAZ), rearing method (puppet-reared, conspecific/parent-reared, cross-foster parent- reared), mentoring (present or absent), and release site (the five aforementioned sites). Effect sizes, which are independent of sample size, were computed as phi (y) or Cramer's V, with values >0.3 considered moderate to large (Cohen, 1988). Because release site had >20% of cells with expected frequency less than five, effect size better represented the importance of this variable. 83 Table 7. Established population size (number of free-flying individuals) of California Condors (Gymnogyps californianus) by year and release site when captive-reared birds were released into the wild. Zeros indicate years in which birds were released with no prior population at the site. Vermillion Baja Hoppera Ventana Pinnacles Year Cliffs California• (California) (California) (California) (Arizona) (Mexico) 1996 11 0 .._ __ -- 1997 14 6 0 __ -- 1998 15 11 5 __ -- 1999 15 18 5 __ -- 2000 16 24 8 __ -- 2001 22 22 15 .._ -- 2002 26 23 18 0 -- 2003 32 30 22 0 0 2004 31 40 18 4 5 a Includes Bitter Creek, Lion, and Castle release sites. 84 Based on the Chi-square results and other exploratory analyses, we then subjected the dichotomous outcomes (behavioral problems, survival) to binary logistic regression (Mertler & Vannatta, 2004) using six predictor variables: sex, rearing facility, rearing method (collapsed to two categories, puppet- and parent-reared, because the two parent- reared groups were equivalent), mentoring (present or absent, or duration: 13-951 d, = 210 d for those mentored), age at release (180-1110 d; = 374 d), and established population size at release site (0-30 individuals; = 8.3). For the models used, mentoring was entered as either a categorical variable (present/absent) or as a continuous variable (number of days). Age at release and established population size were always treated as continuous variables. We analyzed each of the dichotomous outcomes (behavioral problems, survival) using four logistic regression models, resulting in eight models altogether. Two of the four models examined outcomes at 1 yr after release, with one model treating mentoring as a categorical variable (absent or present) and the other as a quantitative variable (total mentoring in days). Two more models examined outcomes at 2 yr after release, treating mentoring as either categorical or quantitative. We excluded release site from all models and rearing method from models of behavioral problems because of empty or sparsely-populated cells, which logistic regression accommodates poorly (i.e., behavior models included just five of the six predictor variables). High tolerance levels (>0.20) in supplemental linear regression models justified inclusion of all the variables we selected in our logistic models. We relied on SPSS v. 12.0 (SPSS, 2003) to conduct all analyses. Because full models are preferred to stepwise, or exploratory, models in ecology (Whittingham et al., 85 2006), we used defaults for the "enter" method of logistic regression. We set alpha at 0.05 for all tests. Results Behavioral Problems Within 1 yr of release, 16 of the 109 individuals (14.7%) exhibited behavioral problems and were removed from the wild. Of these, three individuals were reintroduced to the wild in the second year, with two meeting the criteria for inclusion in the second year. In the second year, none of the juveniles—including the two that had misbehaved the previous year—were recaptured for behavioral problems. Thus, outcomes for behavioral problems were identical for the two time periods. When categorical predictors were tested individually, Chi-square analyses indicated that rearing method dramatically influenced behavior (P < 0.001), with 26.7% of the puppet-reared and none of the parent-reared individuals exhibiting behavioral problems (Table 8). Sex, facility, mentoring, and release site were not associated with behavioral problems. When categorical and continuous predictors were considered together in omnibus models (excluding rearing due to an empty cell that resulted because no parent-reared birds misbehaved), logistic regression revealed that facility was also significant (P = 0.036 and 0.028, respectively, for models treating mentoring as categorical and quantitative; Table 9). A greater proportion of condors raised at SDWAP exhibited behavioral problems compared to those reared at LAZ (20.3% and 8.0%, respectively; Table 8). Neither age at release nor population size was associated with behavioral 86 problems. The logistic regression models failed to explain significant variation in the dependent variable (P > 0.059; Nagelkerke R2 = 0.13 - 0.16). The models predicted the behavior of individual birds with good success (85.3%; Table 9), but only by predicting that all birds behaved properly. Exploratory analyses confirmed that performance of the logistic regression models was weakened by the necessary exclusion of rearing method as a predictor (i.e. if just one parent-reared bird had misbehaved, rearing could have been included and the models would have explained more variation and better predicted the behavior of individuals). Exploratory analyses also confirmed that facility was significant independent of rearing method. 87 Table 8. Summary of results, including chi-square (x2(d0) probabilities and effect sizes ((p or Cramer's V), for juvenile California Condors exhibiting behavioral problems ("problems" or "none") at I and 2 yr after release into the wild. Significant effects are in bold. At 1 yr and 2 yr (N= 109) Predictors Problems None Significance N= 9 N= 47 Sex Male (1) = 0.18 (16%) (84%) X2 P= 0.67 N=7 N= 46 Female = 0.04 (13%) (87%) San Diego Wild N= 12 N= 47 Facility X(1) = 3.29 Animal Park (SDWAP) (20%) (80%) P= 0.07 Los Angeles Zoo N= 4 N= 46 = 0.17 (LAZ) (8%) (92%) N= 16 N=44 Rearing Puppet-reared (27%) (73%) Z2(2) = 15.32 Conspecific/parent- N= 0 N= 33 P< 0.001 Reared (0%) (100%) V= 0.38 Cross-foster parent- N= 0 N= 16 reared (0%) (100%) N= 8 N= 63 Mentoring Present 2 1.89 (11%) (89%) X (1) = P= 0.17 N= 8 N= 30 Absent = 0.13 (21%) (79%) N=7 N= 41 Release site Hopper (CA) (15%) (85%) N= 5 N= 15 Vermillion Cliffs (AZ) (25%) (75%) „2(4) = 2.66 N= 3 N= 26 Ventana (CA) P= 0.62 (10%) (90%) V= 0.16 N=0 N= 2 Baja California (MX) (0%) (100%) N=1 N= 9 Pinnacles (CA) (10%) (90%) 88 •Table 9. Logistic regression results for analyses of behavioral problems in juvenile California Condors. Results were identical at 1 and 2 yr following release into the wild. Significant effects are in bold. Behavior at 1 yr and 2 yr (N = 109) Mentoring categorical Mentoring quantitative Predictors B SE Wald P B SE Wald P Facility 1.379 0.657 4.404 0.036 1.423 0.647 4.841 0.028 Sex 0.066 0.576 0.013 0.908 0.213 0.585 0.133 0.716 Mentoring -0.635 0.609 1.088 0.297 -0.005 0.003 2.734 0.098 Age at release -0.077 0.063 1.493 0.222 -0.024 0.066 0.127 0.722 Population size -0.028 0.039 0.519 0.471 -0.025 0.041 0.393 0.531 Model fit x2 = 8.60, df= 5, P = 0.126 = 10.64, df = 5, P = 0.059 -2 Log likelihood 82.326 80.29 Nagelkerke R2 0.13 0.16 % Predicted correctly 85.3% 85.3% 89 Survival For condors meeting the criteria for inclusion, first-year survival (N = 90) was 77.8%, second-year survival (N = 54) was 88.9%, and cumulative survival through two years (N= 78) was 65.4%. Of the 19 birds removed from the wild and excluded from analyses at 1 yr, 16 were removed for behavioral problems, two for transfer to another site, and one for a health issue. Of the 15 birds excluded at 2 yr, one was removed from the wild for transfer to another site, three were removed for health issues, and 11 were excluded because of incomplete data (we were unable to ascertain their fates); however, these were offset by the re-release of three birds that misbehaved the previous year, of which two survived without behavioral relapses and one died. In contrast to predictors of behavioral problems, predictors of survival differed substantially for the two time periods and depended on whether mentoring was treated as a categorical or quantitative variable. At 1 yr, Chi-square analyses (Table 10) indicated that two categorical predictors were significant: sex (P = 0.032) and mentoring (P = 0.003). Females survived better than males (87.0% and 68.2%, respectively), and mentored condors survived better than non-mentored individuals (86.9% and 58.6%, respectively). Facility, rearing, and release site were not significant; however, the effect size for release site (Cramer's V = 0.25) was larger than that of sex (q) = 0.23), suggesting that survival varied among the different locations (statistical power for release site was reduced by the greater number of categories). In spite of the behavioral problems that were unique to puppet-reared juveniles, survival was high (73.8%) for the 42 puppet-reared individuals that behaved appropriately. 90 Table 10. Summary of results, including chi-square (x2(d0) probabilities and effect sizes ((p or Cramer's V), for juvenile California Condors surviving ("lived" or "died") at 1 and 2 yr after release into the wild. Significant effects are in bold. At 1 yr (N = 90) At 2 yr (N = 78) Predictors Lived Died Significance Lived Died Significance Sex Male N = 30 N = 14 N = 25 N = 15 f(1) = 4.59 0) = 0.30 (68%) (32%) (63%) (38%) X2 P = 0.032 P = 0.58 Female N = 40 N = 6 N = 26 N = 12 9 = 0.23 9 = 0.06 (87%) (13%) (68%) (32%) Facility San Diego Wild N = 35 N = 9 N = 25 N = 10 Animal Park x2(1) = 0.16 0) = 1.03 (80%) (21%) (71%) (29%) X2 (SDWAP) P = 0.69 P = 0.31 Los Angeles Zoo N = 35 N = 11 9 -= 0.04 N = 26 N = 17 9 = 0.12 (LAZ) (76%) (24%) (61%) (40%) Rearing Puppet-reared N = 31 N = 11 N = 24 N= 16 (74%) (26%) (60%) (40%) x2(2) = 1.09 (2) = 1.29 Conspecific/parent- N = 26 N= 7 N = 20 N = 9 X2 P = 0.58 P = 0.053 reared (79%) (21%) (69%) (31%) V = 0.11 V = 0.13 Cross-foster parent- N= 13 N = 2 N = 7 N = 2 reared (87%) (13%) (78%) (22%) Mentoring Present N= 53 N= 8 N = 38 N= 10 x20) = 9.09 (1) = 10.47 (87%) (13%) (79%) (21%) X2 P = 0.003 P= 0.001 Absent N= 17 N= 12 N= 13 N= 17 = 0.32 (59%) (41%) (43%) (57%) p = 0.37 Release Hopper (CA) N = 28 N = 11 N= 17 N= 15 site (72%) (28%) (53%) (47%) Vermillion Cliffs N= 10 N = 5 N= 10 N = 7 (AZ) (67%) (33%) (59%) (41%) x2(4) = 5.44 2(4) = 6.76 Ventana (CA) N = 22 N = 4 N = 21 N = 5 X P = 0.25 P = 0.15 (85%) (15%) (81%) (19%) V = 0.25 V = 0.29 Baja California N = 2 N = 0 N = 2 N = 0 (MX) (100%) (0%) (100%) (0%) Pinnacles (CA) N = 8 N = 0 N = 1 N = 0 (100%) (0%) (100%) (0%) 91 Logistic regression models at 1 yr (Table 11) revealed that sex was significant regardless of whether mentoring was treated as a categorical or quantitative variable (P = 0.023 and P = 0.029, respectively). Mentoring was significant (P = 0.002), but only when treated as a categorical variable. Population size was also significant regardless of whether mentoring was treated as a categorical or quantitative variable (P = 0.008 and P = 0.049, respectively). The odds ratios for population size indicated that the probability of survival decreased by approximately 10. 5% (reflecting ratios of 1.13 and 1.08 for the categorical and quantitative models, respectively; Table 11) with each wild condor already present at the site upon release. Facility, rearing method, and age at release failed to account for survival. The model including mentoring as a categorical variable provided a better fit to the data than the model treating mentoring as quantitative (P < 0.001 and P = 0.044, and Nagelkerke R2 = 0.34 and 0.21, respectively), and predicted outcomes with better success (83.3% and 80.0%, respectively). Predictions were well-distributed between survival and non-survival. At 2 yr, Chi-square analyses (Table 10) indicated that sex was no longer significant, with survival similar for females and males (68.4% and 62.5%, respectively). However, mentoring remained significant (P = 0.001), with mentored condors continuing to survive better than non-mentored individuals (79.2% and 43.2%, respectively). The moderate effect size (c.f. Cohen, 1988) for release site (Cramer's V= 0.29) suggested higher survival for releases at Ventana compared to other locations. 92 Table 11. Logistic regression results for analyses of survival in juvenile California Condors at 1 and 2 yr after release into the wild. Significant effects are in bold. Survival at 1 yr (N = 90) Mentoring categorical Mentoring quantitative Predictors B SE Wald P B SE Wald P Facility -0.302 0.608 0.247 0.619 -0.290 0.576 0.253 0.615 Sex 1.434 0.632 5.144 0.023 1.259 0.576 4.770 0.029 Rearing 0.535 0.653 0.670 0.413 0.060 0.619 0.009 0.923 Mentoring -2.620 0.828 10.025 0.002 -0.005 0.003 2.542 0.133 Age at release -0.032 0.062 0.272 0.602 -0.018 0.068 0.071 0.789 Population size 0.121 0.046 6.993 0.008 0.078 0.040 3.874 0.049 Model fit X2 = 22.72, df = 6, P < 0.001 X2 = 12.94, df = 6, P = 0.044 -2 Log likelihood 72.63 82.41 Nagelkerke R2 0.34 0.21 % Predicted correctly 833% 80.0% Survival at 2 yr (N = 78) Mentoring categonca Mentonng• quantitative Predictors B SE Wald P B SE Wald P Facility -0.771 0.574 1.805 0.179 -0.691 0.583 1.647 0.199 Sex 0.318 0.547 0.337 0.561 0.346 0.499 0.480 0.488 Rearing 0.049 0.592 0.007 0.934 -0.595 0.547 1.181 0.277 Mentoring -2.253 0.674 11.116 0.001 -0.002 0.003 0.808 0.369 Age at release -0.011 0.050 0.047 0.829 -0.012 0.050 0.055 0.815 Population size 0.094 0.040 5.473 0.019 0.026 0.043 0.538 0.552 Model fit X2 = 18.16, df = 6, P = 0.006 X2 = 6.63, df = 6, P = 0.357 -2 Log likelihood 82.47 94.00 Nagelkerke R2 0.29 0.11 % Predicted correctly 70.5% 69.2% 93 Logistic regression models at 2 yr (Table 11) similarly failed to show significance for sex. Mentoring, when treated as a categorical variable, significantly influenced survival (P = 0.001). Population size was also significant when mentoring was treated as categorical (P = 0.019), with an odds ratio similar to that of the first year (1.10). Again, the model including mentoring as a categorical variable provided a better fit to the data than the model treating mentoring as quantitative (P = 0.006 and 0.59, and Nagelkerke R2 = 0.29 and 0.08, respectively), and predicted outcomes with slightly better success (70.5% and 69.2%, respectively). Predictions were well distributed between survival and non-survival. Closer inspection of the data revealed that the effect of mentoring on survival differed over time for the two sexes. Mentored males survived better than non-mentored males at both 1 yr (83.3% and 35.7%, respectively; x20) = 9.98, P = 0.002, cp = 0.48, N = 44) and 2 yr (76.0% and 40.0%, respectively; x2(1) = 5.18, P = 0.023, y = 0.36, N= 40). Survival of mentored females, in contrast, was similar to non-mentored females in the first year (90.3% and 80.0%, respectively; f(1) = 0.95, P = 0.33, y = 0.14, N = 46), but improved significantly at 2 yr (82.6% and 46.7%, respectively; x20) = 5.43, P = 0.020, (i) = 0.38, N= 38). Thus, the benefits of mentoring were more immediately apparent for males than females. Discussion Reintroduction programs have generally been hampered by the lack of an experimental approach, in part because they have often begun with so few animals (McCleery et al., 2007; Seddon et al., 2007). This was certainly the case with the 94 California Condor recovery program, with only 27 birds remaining in 1987. As numbers in captivity steadily increased and birds were reintroduced to the wild, calls were made for experiments to optimize rearing and release in' ethods (e.g., Meretsky et al., 2000). In the unfortunate absence of such experiments (Walters et al., 2008), progress evaluation remains limited to retrospective analyses such as ours and those of others (Meretsky et al., 2000; McCleery et al., 2007; Woods et al., 2007). Although the univariate and multivariate approaches we employed can identify only associations rather than cause- effect relationships, they offer novel and valuable insights on how to improve the reintroduction program for California Condors. We chose to analyze what we believed were some of the more salient factors, or predictors, that might influence behavioral problems and survival in the first two years following release to the wild. Before discussing each of these predictors, we acknowledge several important limitations to our work and sources of potential bias. First, the operational definition for behavioral problems—the recapture of a bird because of inappropriate behavior toward humans and/or their property—may have been inconsistently applied by workers and supervising officials at the release sites, and likely varied over time (See Appendix E). Personal bias regarding the release of puppet-reared birds may have influenced recapture decisions (Meretsky et al., 2000; Mike Stockton, personal communication). Second, because most of the birds removed from the wild for misbehavior were not returned, we could not evaluate whether these birds—all puppet-reared—would have survived if left in the wild. Thus, whereas our analyses examined various factors that independently influenced behavioral problems and survival, the direct effect of misbehavior tendencies on survival remains elusive. Third, factors we did not evaluate possibly influenced 95 behavior and survival, and these may not have been equally represented among all birds. Some of the condors, for example, were transferred several times between different release sites prior to eventual release, temporarily removed from the wild for behavioral or health problems and returned later, and/or recaptured and transferred to other sites. Many were also subjected to hazing in an effort to discourage affiliation with humans (Meretsky et al., 2000; Grantham, 2007; Mee & Snyder, 2007). Puppet-reared birds were presumably hazed the most, and hazing methods likely varied. Although believed by some to have been beneficial (Meretsky et al., 2000; Clark et al., 2007), unpublished data from California suggest that hazing has failed to modify behavior because of inconsistencies in release site management (Grantham, 2007; Mee & Snyder, 2007; Appendix E). Finally, because all releases involved juveniles that remained under the minimal breeding age of 5-7 years (Meretsky et al., 2000) during the two years following release, we assumed that survival attributes considered here were independent of reproduction. Sex Sex was not a significant predictor of behavioral problems. Although California Condor males average slightly larger than females (8.8 and 8.1 kg, respectively), they are otherwise monomorphic and monochromatic (Snyder & Snyder, 2000). Accordingly, there was no a priori reason to suspect one sex would be more inclined to misbehave than the other. Sexual differences in behavior, apart from reproduction, are poorly documented in California Condors (which we detail shortly), and none have been examined in relation to habituation toward humans. However, sex-based rearing effects can appear in birds, 96 particularly as a consequence of maternal and social deprivation (Kleiman, 1980; Harvey et al., 2002). In contrast to its negligible influence on behavioral problems, sex proved to be a significant predictor of survival in both univariate and multivariate analyses. Females experienced better survival than males in the first year (87.0% and 68.2%, respectively), but the difference waned by the end of the second year (68.4% and 62.5%, respectively). Our results contrasted with those of Woods et al. (2007) from the Arizona release site, who reported statistically similar survival between sexes at 1 yr and at >5 yr post-release (based on Chi-square tests; percentages and effect sizes were not provided). Sexual differences in survival are well-documented in birds, but they often relate to sexual dimorphism and unequal investment in reproduction (Liker & Siekely, 2005). The sex- based differences in our study were independent of dimorphism and reproduction, and therefore were unexpected. In a study explicitly testing the hypothesis that a long-lived monomorphic species would lack sex-based differences in survival, Egyptian Vulture (Neophron percnopterus) survival gradually increased through the first four years, but no differences emerged between the sexes (Grande et al., 2009). However, a study with translocated Mountain Quail (Oreorlyx pictus) indicated that females experienced a higher survival rates than males (Nelson, 2007). Thus, broad conclusions cannot be drawn in birds regarding sex-based survival, and should be examined on a species-by- species basis. Several studies have examined sexual differences in behavior that potentially relate to survival. Male California Condors exhibit more vigilance than females when scavenging at proffered carcasses, where condors are particularly vulnerable to predators 97 (West, 2009). In sexually dimorphic Andean Condors, older individuals are dominant at roosts, and males are more dominant than females in all age classes (Donazar & Feijoo, 2002). Age similarly influences dominance relationships in California Condors (Bukowinski et al., 2007; Utt et al., 2008; West, 2009), but sexual differences have not been examined. If higher levels of vigilance and dominance enhance survival, then these behaviors would favor male survival relative to females. Thus, our finding of lower first- year survival for juvenile males must have resulted from other factors that warrant investigation. Facility Rearing facility emerged as an unexpected predictor of behavioral problems. Birds reared at the SDWAP misbehaved more frequently than those reared at LAZ (20.3% and 8.0%, respectively), suggesting that differences in husbandry techniques may have influenced habituation to humans. Facility-based differences are seldom documented in captive-bred animals. In one study, Zidon et al. (2009) found that Persian Fallow Deer (Dama mesopatamica) reared in a heavily visited facility exhibited fewer antipredator behaviors than those reared at a more remote facility. Although we are not aware of any major husbandry or environmental differences between the two facilities in our study, further investigation is warranted. In spite of the behavioral differences, rearing facility did not significantly influence the survival of released California Condors. We are unaware of examples in which releases by different facilities resulted in marked survival differences. 98 Rearing Rearing method profoundly influenced tendencies toward misbehavior, confirming the early analyses and concerns expressed by others (Snyder et al., 1996; Meretsky et al., 2000; Utt et al., 2008). Puppet-reared condors were far more likely than conspecific/parent-reared or cross-foster parent-reared condors to exhibit inappropriate behaviors leading to their recapture (26.7%, 0.0%, and 0.0% of individuals, respectively). Detailed behavioral observations prior to release in the wild suggest that parent-reared birds are more apprehensive in novel situations and focus more attention on social interactions among conspecifics than puppet-reared juveniles (Clark et al., 2007; Utt et al., 2008). Grantham (2007) asserted that all condors in the release program participate in inappropriate behaviors, regardless of rearing type. Condors with behavioral problems are recognized more quickly now and promptly removed from the wild, often before a real problem occurs (Walters et al., 2008). Other reintroduction programs have experienced problems with hand-reared birds and post-release behavioral problems (e.g., Hawaiian Goose [Branta sandvicensis], Marshal & Black, 1992; van Heezik & Seddon, 1998; Gray Partridge [Perdix perdix], Curio, 1998; Scarlet Macaw, Brightsmith et al., 2005). In contrast to the obvious influence on behavior, rearing method had no measurable effect on the survival of released California Condors. Woods et al. (2007) likewise reported the lack of a rearing influence on survival of condors released in Arizona (percentages were not provided). As we cautioned earlier, however, we can only speculate whether the removal of inappropriately behaving birds affected our analyses of survival. Meretsky et al. (2000) suspected that puppet-reared condors were defective and should be removed from the wild, but our findings confirm that puppet-reared birds 99 which behave appropriately and remain in the wild are equally likely to survive as conspecific/parent-reared and cross-foster parent-reared birds (73.8%, 78.8%, and 86.7%, respectively, at 1 yr; 60.0%, 69.0%, and 77.8% at 2 yr). Studies of other species have found similar survival for hand-reared and parent-reared birds, including those involving the Takahe (Bunin & Jamieson, 1996), Houbara Bustard (Chlamydotis undulate; van Heezik & Seddon, 1998), Mississippi Sandhill Crane (Ellis et al., 2000), Mauritius Kestrel (Falco punctatus; Nicoll et al., 2004), and Whooping Crane (Kreger et al., 2006). Other studies found differences, including puppet-reared birds experiencing higher survival rates than parent-reared birds (Common Ravens [Corvus corax], Valutis & Marzluff, 1999; Mississippi Sandhill cranes, Ellis et al., 2000). Mentoring Exposure of juveniles to an adult mentor in captivity failed to ameliorate behavioral problems in the wild. This came as a mild but disappointing surprise, since the mentoring program was initiated in an attempt to reduce behavioral differences between the rearing types (Clark et al., 2007; Utt et al., 2008). Of course, we evaluated only one relatively crude measure of behavior (recapture for behavioral problems). Condors undoubtedly require a large suite of appropriate behaviors for survival in the wild, so mentoring may still be important for shaping social and other behaviors essential for success in the wild but not measured by us. Further study may be needed to evaluate the influence of individual mentors, as some mentors used were adults deemed unfit to the live in the wild because of behavior problems (NCH, unpublished data). Although some have questioned the value of using non-biological adults for mentoring (Mee & Snyder, 100 2007), the lack of behavioral and survival differences among parent/foster- and cross- foster-reared condors in our study supports their utility (see also Clark et al., 2007; Utt et al., 2008). Although mentoring did not ameliorate behavioral problems, it significantly improved the survival of juveniles through the first 2 yr following release in the wild. Mentored condors enjoyed improved survival compared to non-mentored birds (87.0% and 58.6%, respectively, at 1 yr; 79.2% and 43.3%, respectively, at 2 yr). However, the duration of mentoring (13-951 d, = 210 d) did not appear to influence survival, suggesting that longer mentoring periods offered no cumulative benefits. The benefits of mentoring were more immediately apparent for males, since mentoring did not improve survival of females until the second year. These sex-dependent results indicate the importance of extending our study through 2 yr post-release, because a 1-yr study would not have detected the improved survival in females due to mentoring. Considering the higher first-year mortality rates for males, mentoring may be particularly valuable for this sex. Behavioral modification has been used with other avian species and has increased survivability of released individuals (e.g., various pre-release training methods, Yellow- shouldered Amazon parrot, Sanz & Grajal, 1998; Houbara Bustard [Chlamydotis undulata], Van Heezik & Seddon, 1999; Mississippi Sandhill Crane, Sutherland, 1999; New Zealand Robin [Petroica australis], McLean et al., 1999; San Clemente Loggerhead Shrike [Lanius ludovicianus mearnsi], Farabaugh, personal communication). 101 Release Site We found no significant differences in behavioral problems of condors among the five release sites. The likelihood, recognition, and consequences of misbehavior (encounters with humans and property) probably vary among release sites, as may the implementation of hazing procedures to discourage association with humans and human property. However, our findings suggest a degree of uniformity in outcomes. Although not significant statistically, the large effect size (Cramer's V= 0.25 and 0.29, respectively, for each year; c.f. Cohen, 1988) suggests that condor survival varied significantly among release sites. Primary sources of mortality include collisions with overhead wires (including electrocutions) and lead poisoning (Meretsky et al., 2000; Mee & Snyder, 2007; Snyder, 2007). The propensity of condors to ingest "microtrash" (e.g., bottle caps and pieces of glass), or feed it to wild-born young, represents a more recently recognized source of mortality (Johnson et al., 2007; Mee et al., 2007; Mee & Snyder, 2007; Snyder, 2007). Some release sites probably carry a higher risk of potential dangers depending on the relative remoteness of the location (Mee & Snyder, 2007). One noteworthy difference between release sites is the frequency of lead poisonings (Mee & Snyder, 2007): central California (Ventana and Pinnacles) and Baja California tout lower exposures to lead than the other sites (Hopper, southern California; Vermillion Cliffs, Arizona). This difference may explain why survival at Ventana exceeded that of Hopper and Vermillion Cliffs at 1 yr (84.6%, 71.8%, and 66.7%, respectively) and at 2 yr (80.8%, 53.1%, and 58.8%, respectively). The more recent releases at Pinnacles and Baja California provided too few birds for comparison. 102 Age at Release Age at release did not influence the behavioral proclivities of released condors. There has been concern that condors released prematurely might lack the necessary behavioral skills survival in the wild (e.g., wariness; Woods et al., 2007; West, 2009), and exhibit a greater propensity to approach humans and human structures (Grantham, 2007). Juvenile condors in the wild remain dependent for 1 yr or more and spend up to 20 months with parents before severing ties (Snyder and Snyder, 2000). Birds in our data set were released at an average of just over 1 yr (374 d) with a range of 180-1110 d. More unexpected, age at release did not influence condor survival in our study. Woods et al. (2007) found improved survival at the Arizona release site for condors greater than 1 yr old versus younger individuals (95% and 73%, respectively, at 1 yr post- release; 81% and 52%, respectively, at >5 yr), though other factors were not controlled for as in our study. In long-lived species with slow maturation rates, older birds presumably benefit from increased maturity prior to release (Sarrazin et al., 1994; Sarrazin & Legendre, 2000; Utt et al., 2008). Survival in our study increased between the first and second years (77.8% and 88.9%, respectively). Survival of condors released in Arizona also increased over successive years, from 79.6% in the first year, to 89.5% in the second through fourth years, and 97.8% from the fifth year onward (Woods et al., 2007). Age-related survival differences similarly exist in the Egyptian Vulture (Grande et al., 2009). Verner (1978) and Meretzky et al. (2000) concluded that mean annual survival of California Condors must exceed 90()%0 for population persistence. Accumulating evidence suggests that condors approach this benchmark by their second year after release. 103 Population Size We found no relationship between behavioral problems and existing population size at the time of release. These results are encouraging because of the possibility that established birds can negatively influence the behaviors of newly-released individuals, or vice versa (Conway, 1980; Meretsky et al., 2000; Mee et at., 2007; Mee & Snyder, 2007; Wallace et al., 2007; Walters et al., 2008). In contrast to behavioral problems, established population size was a significant predictor of survival during both years (P = 0.008 and 0.019 at 1 and 2 yr, respectively). Survival decreased as the existing population size at the time of releases increased. This finding suggests two important possibilities in the condor release program: 1) that the presence of other successful birds in the wild does not improve survival of newly released birds, and that 2) at least some release sites may have reached their carrying capacity, resulting in reduced survival following subsequent releases. Our findings came as somewhat of a surprise. Because condors have strong social tendencies, one might expect group benefits to improve survival. Initial population size proved critical, for example, in reintroduction efforts of the Black-faced Impala (Aepyceros melampus petersi), with releases of larger groups more likely resulting in population growth (Matson et al., 2004). Year of release (time) was confounded to some extent with rearing method and population size in the wild. We assumed that changes over time would be less important than the other predictors we considered, and therefore chose to exclude year of release as a factor in analyses. The influence of rearing method on behavior problems was clearly independent of time. However, the southwest has suffered from a long-term drought during much of the study period (MacDonald et at., 2008), so it's conceivable that the 104 effects of population size on survival might reflect, instead, the consequences of drought, such as prey availability. Conclusions Our analyses were based on the largest data set examined to date. The advantage of a multivariate approach, such as logistic regression, is that many variables can be evaluated, and controlled for, simultaneously. As the reintroduction program continues, we recommend the use of more detailed survival models. The continuously distributed data from a survival analysis, the increased sample size from more recent releases, and the inclusion of rearing data from the Peregrine Fund should provide much greater statistical power than our models, and would be useful for comparison to and extending our findings. Rigorous evaluation of the factors reducing attraction to humans and human structures has been hampered by lack of an experimental approach and the confounding of rearing and aversive training techniques in releases (Meretsky et al., 2000; Mee & Snyder, 2007). Other similar species, such as the Andean Condor, similarly exhibit attraction to human activity and man-made structures, so the question of how much "misbehavior" is natural or acquired in captivity remains unclear (Wallace, 1989), as do its consequences for survival. With increasing numbers of condors in captivity and the wild, experimental approaches to rearing and release can now be more readily incorporated into the recovery program to better identify optimal approaches. We have identified several factors that potentially contribute to survival, most notably sex-based differences, mentoring, and existing population size. The relatively 105 poor fit of the logistic regression models for survival (explaining 11-34% of variance), however, suggests that other important predictors of mortality could be identified. Possibilities to consider include additional rearing considerations (e.g., single- versus group-rearing, handling trauma, human contact; Clark et al., 2007), duration of time in acclimation pens at the release site (Lockwood et al., 2005), and methods of supplemental feeding (Grantham, 2007). The apparent success of the mentoring program suggests that relatively simply measures exist to improve the survival of released birds, and justifies further study. Acknowledgments I would first like to thank my coauthors, Dr. William K. Hayes and Dr. Nancy Harvey. I would also like to thank the Zoological Society of San Diego for allowing me to collect data at the San Diego Wild Animal Park. Don Sterner, Tom Levites, and the condor keepers made available essential information for this study. I also thank the Los Angeles Zoo for allowing us to glean data at their facility, as well as Mike Clark for sharing his amazing insights and knowledge of the California Condor. 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(1986) Environmental contaminants in surrogates, food, and feathers of California Condors (Gymnogyps californianus). Environmental Monitoring and Assessment. 6(1):91-111. Wiemeyer 5, Scott JM, Anderson MP, Bloom PH, Stafford CJ. (1988) Environmental contaminants in California Condors. Journal of Wildlife Management. 52(2):238- 246. Williams TM, Feistner ATC. (2006) Reproduction of Bali Starlings Leucospar rothschildi. International Zoo Yearbook. 40:271-289. White TH, Collazo JA, Vilella FJ. (2005) Survival of captive-reared Puerto Rican Parrots released in the Caribbean National Forest. Condor. 107:424-432. Whittingham, M. J., P. A. Stephens, R. B. Bradbury, and R. P. Freckleton. (2006) Why do we still use stepwise modeling in ecology and behaviour? Journal of Animal Ecology. 75:1182-1189. Woods CP, Heinrich WR, Fury SC, Parish CN, Osborn SAH, Cade TJ. (2007) Survival and reproduction of California Condors released in Arizona. P 57-78. In: Mee A & Hall LS, eds. California Condors in the 21st Century. Lancaster: Cadmus Communications. 296 p. Zidon R, Saltz D, Shore LS, Motro U. (2009) Behavioral changes, stress, and survival following release of Persian Fallow deer from two breeding facilities. Conservation Biology. 23(4):1026-103. 116 CHAPTER FOUR EVALUATING CAPTIVE-BREEDING AND REINTRODUCTION METHODS IN AVIAN CONSERVATION: A REVIEW Abstract When habitat management and preservation (in situ conservation) fail to alleviate the decline of a species, captive breeding (usually ex situ conservation) and reintroduction techniques provide essential tools in avian conservation. In fact, many avian species would have likely gone extinct without ex situ conservation intervention. I this review I show that captive breeding is a complicated process, relying on species- specific information gleaned from research such as habitat use, developmental modes, life history, social behaviors, and breeding preferences. A multitude of breeding techniques exist, allowing a customizable propagation program to be implemented, including parent-, hand-, puppet-, foster-, and cross-foster rearing. Because some birds reared in captivity tend to have deficiencies in behavioral repertoires, which wild birds normally acquire during rearing, pre-release training is often necessary to improve the chances of survival of captive-bred individuals. A variety of training methods exist, such as predator avoidance, obstruction avoidance, mentoring, and acquisition of proper foraging techniques. Release methodologies also play an important role in the success or failure of a reintroduction program, specifically the differences between hard and soft releases. With a thoughtful combination of methods and techniques discussed in this paper, captive breeding and reintroduction of endangered birds can be quite successful. 117 Introduction The need for captive breeding and reintroduction programs has never been as important as it is today. The Red List Index for birds indicates a steady and continuing increase in the threat status (projected extinction risk) of the world's birds between 1988 and 2004 (Baillie et al., 2004). This trend has continued through 2009 (IUCN, 2009). The number of threatened bird species on the IUCN (International Union for Conservation of Nature and Natural Resources) red list has reached an astonishing 1227, representing nearly 12.3% of all bird species (1227 species; Table 12). From 1996-2009, the number of critically endangered bird species rose almost 9% (from 168 to 192 species), while endangered bird species increased by 65% (from 235 to 362 species; IUCN, 2009). Almost half (47%) of the birds listed on the IUCN Red List belong to the order Passeriformes (perching birds). Fifty-four percent of passerines, 61% of Sphenisciformes (penguins), 44.6% of Procellarliformes (seabirds), and 38.5% of Struthioniformes (ostriches, rheas, kiwis) are in jeopardy (i.e., including the statuses of vulnerable [VU], endangered [EN], critically endangered [CR], and extinct in the wild [EW]). Orders experiencing minimal threat include Coliiformes (0%, mousebirds), Gaviiformes (0%, loons), and Trogoniformes (9%, trogons and quetzals). Almost half of all threatened bird species are estimated to have declined in status during 2000-2004, regardless of whether or not they were uplisted to higher categories of threat (Baillie et al., 2004). 118 Table 12. Summary of red list categories of avian orders: values refer to number of species. EX — extinct, EW — extinct in the wild, CR-critically endangered, EN — endangered, VU vulnerable, NT — near threatened (includes lower risk/near threatened), DD — data deficient, LC — least concern (includes lower risk, least concern; IUCN, 2009 Order EX EW CR EN VU NT DD LC Totar Total" Anseriformes 6 0 6 10 12 9 0 124 43 28 Apodiformes 2 0 9 16 11 24 8 373 62 36 Caprimulgiformes 0 0 3 2 3 10 4 100 18 8 Charadriiformes 4 0 10 11 17 34 0 278 76 38 Ciconiiformes 5 0 5 11 5 6 0 88 32 21 Coliiformes 0 0 0 0 0 0 0 6 0 0 Columbiformes 15 1 9 15 35 40 1 220 115 60 Coraciiformes 1 0 4 3 17 29 3 164 54 24 Cuculiformes 2 0 2 3 6 11 0 143 24 11 Falconiformes 2 0 11 8 30 39 1 221 90 49 Galliformes 2 1 5 21 45 38 0 176 112 72 Gaviiformes 0 0 0 0 0 0 0 5 0 0 Gruiformes 21 1 5 19 32 20 4 125 98 57 Passeriformes 42 1 79 169 324 439 34 4814 1054 573 Pelecaniformes 2 0 2 4 10 7 0 42 25 16 Phoenicopteriformes 0 0 0 0 1 3 0 2 4 1 Piciformes 0 0 4 2 12 29 2 360 47 18 Podicipediformes 2 0 2 2 2 0 0 14 8 6 Procellariiformes 2 0 14 18 26 16 4 50 76 58 Psittaciformes 19 0 16 32 48 41 0 218 156 96 Sphenisciformes 0 0 0 4 7 2 0 5 13 11 Stringiformes 4 0 6 10 17 24 4 137 61 33 Struthioniformes 2 0 0 1 4 4 0 2 11 5 Tinamiformes 0 0 0 0 5 3 0 39 8 5 Trogoniformes 0 0 0 1 0 10 0 29 11 1 Total 133 4 192 362 669 838 65 7735 2198 1227 a Total number of species in corresponding avian order b Total number of threatened species in corresponding avian order; including the categories extinct in the wild (EW), critically endangered (CR), endangered (EN), and vulnerable (VU). 119 What is driving this rapid decline in biodiversity? The influence of human activities either directly or indirectly has been a major impetus. Although some species respond positively to anthropogenic pressures, the great majority show only limited tolerance to the increasingly widespread and rapid changes in ecosystems worldwide. The major human impacts on biodiversity include habitat destruction and fragmentation, invasive alien species, over-utilization of species, disease, pollution and contaminants, incidental mortality, and climate change (Baillie et al., 2004; Sekercioglu et al., 2004; Butchart et al., 2006; BirdLife International, 2008a). Recent evidence indicates that it may take decades to hundreds of years before vertebrate species facing habitat loss and fragmentation finally become extinct (Baillie et al., 2004). This time lag offers an opportunity to reverse the trend through habitat protection and, if necessary, more intense conservation programs (Baillie et al., 2004). Habitat conservation (in situ conservation) is often not enough to prevent a species from declining; thus, a more hands-on approach, such as captive breeding and management (ex situ conservation), is needed (Baillie et al., 2004). Captive breeding combined with reintroductions or population reinforcement have prevented many species from becoming extinct (Baillie et al., 2004; Butchart et al., 2006). In fact, conservation measures in the past decade (including habitat protection, captive-breeding, and reduction of threats) have directly prevented the extinction of at least 16 bird species and have allowed 18 more to be down-listed (Butchart et al., 2006; BirdLife International, 2008b). In addition to preventing extinctions, conservation measures were crucial to improving the status of 49 critically endangered bird species, either by slowing the rate of decline or 120 by down-listing to a lower category (24 and 25 species, respectively; BirdLife International, 2008b). Captive breeding involves the translocation of individuals, which can be defined in any of the following three ways: 1) introduction, movement of an organism to an area outside its native habitat/range; 2) reintroduction, movement of an organism into an area of previously occupied habitat from which it has been extirpated; and 3) restocking, movement of organisms to build up numbers of an already established population (Conway, 1980; Campbell, 1980; Sarrazin and Barbault, 1996; Millar et al., 1997; Tenhumberg et al., 2004; Sutherland et al., 2010). Organizations involved in captive propagation include zoos, private breeders, state agencies, conservation foundations, and research centers within or outside of universities (Saint Jaime, 1999; Fernandez and Timberlake, 2008). Special consideration to a species developmental mode should be taken when planning and implementing a captive-breeding program. Stark and Ricklefs (1998) developed a comprehensive classification system of Avian developmental modes (Table 13). Understanding the developmental mode and life history of a species is critical in providing the most beneficial rearing environment in captivity. Precocial-1 (P-1) defines a chick which hatches with plumage feathers and open eyes, leaves the nest, and requires no parental care. Precocial-2 (P-2) defines a hatchling covered in down and with open eyes, leaves the nest, and is brooded by parents. Precocial-3 (P-3) describes a hatchling covered in down and with open eyes, leaves the nest, and may rely on food showing by parents for a period of time. Precocial-4 (P-4) defines a hatchling covered in down, open eyes, leaves the nest area, but relies on a parent for food. Semiprecocial (SP) is a 121 hatchling covered in down, open eyes, remains in the nest area, and relies on parents for food. Semialtricial-1 (SA-1) describes a hatchling covered in down and with open eyes, remains in the nest, and relies on parents for food. Semialtricial-2 (SA-2) is defined as a hatchling covered in down and with closed eyes, stays in the nest, and relies on parent for food. Finally, an altricial (A) hatchling has no feathers (or down), hatches with eyes closed, stays in the next, and relies on parents for food. Throughout this review, developmental class will be provided after each species mentioned. Additional information on each species mentioned in this paper is provided in Table 14. Ideally, all birds should be reared by their own parents, such as in the wild; however, in captivity this is often not possible. Many innovative approaches have been used in captive-breeding programs to rear avian young which could not be cared for by their biological parents, including the use of foster-parents, cross-foster parents, hand- rearing, and puppet-rearing (discussed below; Conway, 1980; Dixon, 1986; Scott and Carpenter, 1987; Wallace, 1994; Snyder et al., 1996). To combat behavioral problems seen in certain species, mentoring, a recently implemented technique, can be used (Bukowinski et al., 2007; Utt et al., 2008). To prepare naïve birds for successful reintroduction, implementing pre-release training techniques such as predator avoidance, obstruction avoidance (e.g. high-power lines), proper foraging skills, and soft releases are also useful (McLean et al., 1999; Griffin et al., 2000; Alagona, 2004; Ward and Schlossberg, 2004; Mee and Snyder, 2007; Woods et al., 2007). 122 Table 13. Diagnostic features of Nice's developmental classes, including continuum of imprinting tendencies, modified from Stark and Ricklef (1998). Nest Parental Class Plumage Eyes Imprinting attendance care Contour Immediate Precocial —1 None feathers upon hatch Precocial —2 Leave Brooding Food Precocial —3 Open showing Precocial —4 Semiprecocial Down Nest area Parental Semialtricial — 1 feeding Semialtricial —2 Closed Stay Delayed Altricial None until fledging 123 Table 14. Taxonomy, Development, Life History, Rearing, and Release Techniques in Avian Conservation Order Family Genus species Common name DM a LHb Breede State Reard Rlsf References Anseriformes Anatidae Anas nesiotis Campbell Islands Teal P-2 ✓ S CR - PT, McClelland and S,T Gummer, 2006 A. laysanensis Laysan Teal P-2 K S CR - T,S Reynolds and Work, 2005; Reynolds et al., 2008 Anser erythropus Lesser White-fronted Geese P-3 S, C VU CF - Momer, 1986 A. fabalis Bean Goose P-3 S, C LC CF - Morner, 1986 Aythya innotata Madagascar Pochard P-2 S CR - - BirdLife International, 2009b Branta canadensis Canada Goose P-3 ✓ C LC CF - Von Essen, 1982 B. leucopis Barnacle Goose P-3 ✓ C LC CF - Momer, 1986 B. sandvicensis Hawaiian Goose P-3 ✓ S, C VU P, H, S Marshall & Black, CF, F 1992 Apodiformes Trochilidae Amazilia Chestnut-bellied Hummingbird A ✓ S EN - - BirdLife International, castaneiventris 2009c Collocalia bartschi Guam Swiftlet A ✓ S EN - S BirdLife International, 2008d Eriocnemis mirabilis Colorful Puffleg A ✓ S CR - BirdLife International, 2009e Caprimulgiformes Caprimulgidae Caprimulgus Puerto Rican Nightjar SP ✓ S CR - - BirdLife International, noctitherus 2009f Eleothreptus White-winged Nightjar SP ✓ S EN - - BirdLife International, candicans 2008g Charadriiformes Charadriidae Charadrius melodus Piping Plover ✓ NT CF S Powell et al., 1997 C. vociferus Killdeer P-2 ✓ S LC CF - Powell et al., 1997 Haematopodidae Haematopus Eurasian Oystercatcher P-3 ✓ 5, LC LC - - BirdLife International, ostralegus 2009h Laridae Larus argentatus Herring Gull SP K C LC CF - Cade, 1977 L. canas Mew Gull SP K C LC CF - Cade, 1977 L. fuscus Lesser Black-backed Gull SP K C LC CF - Cade, 1977 Sterna nereis davisae New Zealand Fairy Tern SP K LC CR F, CF - Hansen, 2006 Recurvirostridae Himantopus Pied Stilt P-3 ✓ LC LC CF Reed and Murray, himantopus 1993; Reed, 1994 H. novaezelandiae Black Stilt 13-3 r S CR CF, F, S Reed and Murray, P, H 1993; Reed, 1994 Recurvirostra avosetta European Avocet P-3 ✓ LC LC - - BirdLife International., 2009i Table 14. Taxonomy, Development, Life History, Rearing, and Release Techniques in Avian Conservation, continued. Order Family Genus species Common name DM a LHb Breed' Staf Reard RIsf References Scolopacidae Actitis macularia Spotted Sandpiper P-2 r S LC CF Reed and Murray, 1993; Powell and Cuthbert, 1993 Ciconiiformes Ciconiidae Mycteria cinerea Milky Storks SA-1 K C VU H, P Yaacob, 1994 M ibis Yellow-billed Stork SA-1 K C LC Luthin et al., 1986 M leucocephal Indian Painted Stork SA-1 K S, C NT Luthin et al., 1986 Threskiornithidae Eudocimus ruber Scarlet Ibis SA-1 K S, C LC Luthin et al., 1986 Geronticus eremita Waldrapp Ibises SA-1 K C CR H, P S Tinter & Kotrschal, 2002 Nipponia Nippon Crested Ibis SA-1 K C EN H, P Hi et al., 2001 Columbiformes Columbidae Columba inornata Puerto Rican Plain Pigeon A r S EN U.S. Fish & Wildlife wetmorei Service, 1982 Nesoenas mayeri Mauritius Pink Pigeon A r S EN F Coraciiformes Alcedinidae Halcyon cinnamomina Guam Micronesian Kingfisher A r S EN H, P S U.S. Fish and Wildlife cinnamomina Service, 2008 Bucerotidae Anthracoceros montani Sulu Hornbill A K S CR BirdLife International, 2009k Penelopides Panini Tarictic Hornbill A K S EN P, H Buay, 1991 Cuculiformes Cuculidae Carpococcyx viridis Sumatran Ground-cuckoo A r P CR BirdLife International, 20091 Centropus sterrii Black-hooded Coucal A r P CR BirdLife International, 2009m Falconiformes Accipitridae Accipiter cooperii Cooper's Hawks SA-1 K S LC II, P Snyder and Snyder, 1994 Aquila adalberti Spanish Imperial Eagle SA-1 K S VU P, F S Gonzalez et al., 1996 Gypaetus barbatus Bearded Vulture SA-1 K S C LC Margalida et al., 2004 G. bengalensis White-rumped Vulture SA-1 K S C CR Gilbert et al., 2002 Gyps fulvus Griffon Vulture SA-1 K S C LC P, H S Sarrazin and Legendre, 2000 G. indicus Indian Vulture SA-1 K S, C CR Gilbert et al., 2002 Haliaeetus Bald Eagle SA-1 K S LC PT S Wallace, 1994 leucocephalus H vociferoides Madagascar Fish-eagle SA-1 K S CR P, H Watson et al., 1996 Neophron percnopterus Egyptian Vulture SA-1 K S, C EN Hernandez & Margalida, 2009 Pandion haliaetus Osprey SA-1 K S LC H Cade, 1980 Torgos tracheliotus Lappet-faced Vulture SA-1 K S, C VU Pennycuick, 1976 negevensis Trigonoceps occipitalis White-headed Vulture SA-1 K 5, C VU Pennycuick, 1976 Table 14. Taxonomy, Development, Life History, Rearing, and Release Techniques in Avian Conservation, continued. Order Family Genus species Common name DM a LH1' Breed' Statc Rear' RIsf References Cathartidae Cathartes aura Turkey Vultures SA-1 K S, C LC H S Kirk and Mossmen, 1998 Gymnogyps California Condor SA-1 K S CR P, F, S, Walters et al., 2008; californianus CF, H, PT BirdLife International, PT 2009a Vultur gryphus Andean Condor SA-1 K S NT P, H, S Bruning, 1983 PT Falconidae Fako femoralis Alpomado Falcon SA-2 K S, C LC H S Brown et al., 2006 septentrionalis F. peregrinus Peregrine Falcon SA-2 K S C LC H, P S Wallace, 1994 CF, PT F. punctatus Mauritius Kestrel SA-2 K S C VU H, P, S Nicoll et al., 2004 F. tinnunculus Common Kestrels SA-2 K S C LC H, P, S Brown, 1980, Craig et CF al., 2004 IN) Galliformes Megapodiidae Leipoa ocellata Malleefowl P-1 r/K S LC H, S Priddel and Wheeler, 1994 Odontophoridae Callipepla squamata Scaled Quail P-3 r S LC CF Carpenter et al., 1991 Colinus virginianus Masked Bobwhite P-3 r S CR .H, CF S Ellis et al., 1977; ridgwayi Carpenter etal., 1991 C. V. texanus Texas bobwhite P-3 r S LC CF Ellis et al., 1997; Carpenter etal., 1991 Phasianidae Gallus gallus Domestic Chicken P-3 r S LC CF Berger et al., 1977 domesticus Perdix. perdix Grey Partridge P-3 r S LC H, P, S Buner & Schaub, 2008 P. inopinatum Mountain peacock pheasant P-3 r S VU P Bruning, 2003 Gruiformes Gruidae Anthropoides paradisea Stanley Crane P-4 K S VU H S Luthin et al., 1986 Grus americana Whooping Crane P-4 K S EN H, P, S Horwich,1989; CF Nagendran et al., 1996 G. antigonie sharppi Eastern Saws Crane P-4 K C VU H, PT S Mirande, 1985; NatureServe, 2009 G. canadensis Sandhill Crane P-4 K S LC P, H, S Nagendran et al., 1996 PT G. c. pulla Mississippi Sandhill Crane P-4 K S EN PT S Nagendran et al., 1996 G. japonensis Red Crowned Crane P-4 K S EN H, CF, S Horwich, 1989; P, PT Nagendran et al., 1996 G. leucogeranus Siberian Crane P-4 K S CR H S Luthin et al., 1986 Table 14. Taxonomy, Development, Life History, Rearing, and Release Techniques in Avian Conservation, continued. Order Family Genus species Common name DM a LIP Breed' Statc Rea? RIsf References G. rubicund Australian Crane P-4 K S LC H S Mirande, 1985 G. vipio White-naped Crane P-4 K S VU H, P, S Horwich, 1989; CF Nagendran et al., 1996 Otididae Ardeotis kori Kori Bustard P-4 K S LC H, P Hallagar, 2004; Hallagar, 2005 Chlamydotis undulata Houbara Bustard P-2 K S VU P, H Van Heezik & Seddon, 1998 Otis tarda Great Bustard P-4 K VU Rallidae Porphyrio mantelli Takahe P-4 EX P, F, S, T Lack, 1968; Maxwell PT, & Jamieson, 1997 CF Rallus owstoni Guam Rail P-4 S EW H S BirdLife International, 2008m Passeriformes Acanthisittidae Acanthisitta chloris Rifleman A LC H,T Leech et al., 2007 Xenicus gilviventris Rock Wren A VU T BirdLife International, 2008g Callaetidae Callaeas cinerea North Island Kokako A EN S,T lanes et al., 1999 wilsoni Philesturnus c. South Island Saddleback A • S NT T,S Pierre et al., 1999 carunculatus Campephagidae Coracina newtoni Reunion Cuckoo-shrike A • S CR S Thiollay and Probst, 1999 Corvidae Corvus corax Common Ravens A LC P, PT Valutis & Marzluff, 1999 C. tropicus Hawaiian Crow A • S EW H, P, S Kuehler et al., 1995; PT Valutis & Marzluff, 1999; Harvey et al., 2002 Icteridae Molothrus ater Brown-headed Cowbirds A • P LC Lack, 1968 Laniidae Lanius ludovicianus San Clemente Loggerhead A • S EN P, H S,T Pruitt, 2000 mearnsi Shrike Meliphagidae Lichenostomus Helmeted Honeyeater A • LC, S CR P, CF S Smales, 1996 melanops cassidix Mimidae Nesomimus trifasciatus Floreana Mockingbird A CR Toxostoma guttatum Cozumel Thrasher A CR Monarchidae Eutrichomyias rowleyi Cerulean-Paradise Flycatcher A CR Muscicapidae Copsychus sechellarum Seychelles Magpie Robin A EN S,T BirdLife International, 2008c Table 14, Taxonomy, Development, Life History, Rearing, and Release Techniques in Avian Conservation, continued. Order Family Genus species Common name DM a LHb Breed' Statc Rear' Rlst References Petroicidae Petroica australis New Zealand Robin A r S LC CF - MeLean et al., 1999; S Griffon et al., 2000 P. traversei Chatham Island Black A r S EN CF H, Dixon, 1986; Butler Robin S,P and Merton, 1992; T Lovegrove, 1996 Paradiseaidae Paradisaea rubra Red Bird of Paradise A r S NT H, P - Worth et al., 1991; Hundgen et al., 1991 Sturnidae Leucopsar rothschildi Bali Mynah A r S, C CR H S,P Collins et al.,1998 Timaliidae Garrulax strepitans Tickell's Laughing A LC H Mace, 1991 Thrush Turdidae Myadestes palmeri Puaiohi A CR H S Tweed et al., 2003 Pelecaniformes Balaenicipitidae Balaeniceps rex Shoebill SP K S VU Luthin et al., 1986 Phoenicopteriformes Phoenicopteridae Phoeniopterus chilensis Chilean Flamingo SP K C NT P Pickering et al., 1992 P. r. ruber Caribbean Flamingos SP K C LC Pickering et al., 1992 Piciformes Picidae Campephilus principalis Ivory-billed Woodpecker A CR t\-) Procellariiformes Diomedeidae Diomedea Amsterdam Albatross SP K C CR BirdLife International, oo amsterdamensis 20090 Hydrobatidae Oceanites maorianus New Zealand Storm Petrel SA-2 K C CR S BirdLife International, 2009p Psittaciformes Psittacidae Amazona barbadensis Yellow-Shouldered SA-2 K S, C VU P, F, S Sanz & Grajal, 1998 Amazon Parrot Amazona vittata Puerto Rican Amazon SA-2 K S, C CR H S, Lacey et al., 1989; PT White et al., 2005 Anodorhynchus Hyacinth Macaw SA-2 K S, C EN H T Kuniy et al., 2006 hyacinthinus Ara macao Scarlet Macaw SA-2 S, C LC H S,H, Myers and Vaughan, PT 2004 Cacatua moluccensis Salmon-crested Cockatoo SA-2 K S, C VU H, P S Sweeny, 2000; Brightsmith et al., 2005 Nestor meridionalis Kaka SA-2 EN H T,S Moorehouse and Greene, 1998; Greene et al., 2004 Nymphicus hollandicus Cockatiel SA-2 K S, C LC H, P Myers et al., 1988 Psittrichas fulgidus Pesquet's Parrot SA-2 S, C VU P, H Buay & Thirunavukkarasu, 2000 Table 14. Taxonomy, Development, Life History, Rearing, and Release Techniques in Avian Conservation, continued Order Family Genus species Common name DM a LHb Breed' Statc Reard Rlsf References Rhynchopsitta Thick-billed Parrot SA-2 K S EN H P T, Snyder et al., 1994 pachryhyncha S, H Stringops habroptilas Kakapo SA-2 K S, C CR H, P S, T Sibley, 1993; Elliot et al., 2001 Sphenisciformes Spheniscidae Eudyptes sclateri Erect-crested Penguin SA-1 K C EN BirdLife International, 2008q Strigiformes Strigidae Athene cunicularia Burrowing Owl SA-2 r LC LC F S Poulin et al., 2006 Bubo bubo Eurasian Eagle Owl SA-2 K S LC F S,P Johnson, 1991; T Penteriani et al., 2004 Tytonidae Tyto alba Barn Owl SA-2 r S, LC LC P, H cS Durant and Handrich, 1998; Meek et al., 2003 Struthioniformes Apterygidae Apteryx owenii Little Spotted Kiwi P-2 K S VU H BirdLife International, 2008i aDevelopmental state at hatch: Precocial-1 (P-1), Precocial-2 (P-2), Precocial-3 (P-3), Precocial-4 (P-4), Semiprecocial (SP), Semialtricial-1 (SA-1), Semialtricial-2 (SA-2), Altricial (A; Ehrlich et al., 1988; Gill, 1995; Stark & Ricklefs, 1998; see Table 13). bLife history: r-selected (r) , K-selected (K; Table 16). 'Current IUCN status: Extinct (EX), extinct in wild (EW), critically endangered (CR), endangered (EN), vulnerable (VU), near threatened (NT), least concern (LC; IUCN, 2009). dRearing method: Parent (P), conspecific foster (F), cross-foster with different species (CF), hand-reared (H), puppet-reared (PT) 'Breeding ecology— Colonial nesting (C), Loose colony (LC), Group nesting territories (N), Parasitic (P), Solitary nesting (5) (Lack, 1968). Release method: Soft release, may include supplemental food, hacking, or predator control (S), hard release (H), Prerelease training (PT), translocation (T) The combination of double-clutching, fostering, and cross-fostering techniques permits a wide range of possible management systems that can allow flexibility in the design of management programs, which could be critical to the conservation of some bird species (Dixon, 1986; Wallace, 1994). In addition, artificial insemination and incubation can contribute to reproductive success and reduce the dependence of a breeding program on the existence of compatible, reproductively able, and willing parents capable of rearing healthy offspring (Mirande, 1985; Dixon, 1986: Saint Jaime, 1999). Because of the preponderance of information related to captive-breeding programs, I have narrowed the scope of this paper to focus on rearing methods, behavioral modification, and pre- release training for reintroduction. Detailed information on genetics, studbooks, artificial insemination, disease, and research on surrogate species, although important, are not covered in this paper. Reviews by Wilson et al. (1994), Saint Jalme (1999), and McDougall et al. (2006) serve as excellent resources for this additional information. • Comprehensive programs for endangered species need to encompass knowledge from field investigations as well as carefully developed captive breeding programs (Luthin et al., 1986; Wallace, 1994; Baillie et al., 2004). Thus, for the captive propagation of a species to be successful, research is often needed in a wide range of areas such as species-specific studies in husbandry, nutrition, behavior, medicine, physiology, and endocrinology (Kleiman, 1980; Wallace, 1994; Saint Jaime, 1999; Baillie et al., 2004; Farrell et al., 2000). It is imperative that much be understood about a specific species (or closely-related surrogate species) prior to attempts at captive- breeding (Conway, 1980). 130 The case of the Kakapo (Stringops habroptilus, SP) sheds light on what can occur if little is known about a species before beginning a captive-breeding program (Kear, 1977). Early in the Kakapo breeding program, birds were housed together for years without breeding. Only after the birds died was it discovered that all the birds were male. The Kakapos were trapped displaying together at a lek where females would occasionally visit. Thus, the likelihood of trapping a female was extremely low. Because of the lack of knowledge of the Kakapo's natural breeding behavior and difficulties sexing the bird, early attempts at captive-breeding failed (Kear, 1977). Modern genetics and advances in sex identification techniques allow captive breeders to form male/female pairs without having to guess if they have paired appropriately. However, similar stories are told of many neonate conservation programs, which further strengthen the notion that research must be conducted before the onset of any captive-breeding program (Tongren, 1985; He et al., 2005). • Multiple Clutching Multiple clutching hastens propagation in captivity by increasing the reproductive potential of a breeding pair, and is employed most among species with low reproductive rates (Dixon, 1986; Sheppard, 1987; Saint Jaime, 1999; Beres & Starfield, 2001). The California Condor (Gymnogyps californianus, SA-1) is an ideal example of the necessity for multiple clutching. In the late 1980s, the California Condor became extinct in the wild, with only 27 surviving individuals in captivity. Zoo officials needed a way to quickly bolster numbers of the critically endangered bird, which normally attempts to raise only once chick every other year (Snyder & Hamber, 1985; Kuehler et al., 1991; 131 Harvey et al., 2003; 2004; Nielsen, 2006; Clark et al., 2007; Utt et al., 2008). This was accomplished by employing the method of multiple clutching. Caretakers pulled the first egg of the season, and sometimes the second, to induce the breeding pair to lay another (Dixon, 1986). Typically, the first chick, and sometimes the second chick as well, was incubated and raised with species-specific puppets instead of by the natural parents (Toone, 1994; Harvey et al., 2004; Snyder, 2005; Nielsen, 2006; Utt et al., 2008). Suitable pairs were permitted to hatch and raise the last clutch of the season (Beres & Starfield, 2001). The use of multiple clutching made a drastic impact on condor numbers, with an increase to more than 350 living in 2010, and approximately 187 of these living in the wild. Multiple clutching was also successfully used with the Scarlet Ibis (Eudocimus ruber, SA-1; Luthin et al., 1986), Peregrine Falcon (Falco peregrinus, SA-2; Cade, 1977; Fyfe et al., 1977), Mauritius Kestrel (Falco punctatus, SA-2; Saint Jaime, 1999) Salmon-crested Cockatoo (Cacatua moluccensis, SA-2; Sweeney, 2000), Hawaiian Goose (Branta sandvicensis, P-3; Berger, 1977) and the White-naped Cranes (Grus vipio, P-4; Sheppard, 1987). In addition to bolstering weak population numbers, multiple clutching may also be useful in species where sibling aggression, siblicide, or infanticide occurs in the nest (Sauey & Brown, 1977; McMillen et al., 1987; Saint Jaime, 1999; Kuniy et al., 2006). For example, some cranes begin incubating as soon as the first egg is deposited, which leads to asynchronous hatching of a typical two-egg clutch (Sauey & Brown, 1977; McMillen et al., 1987; Saint Jaime, 1999). Young cranes are aggressive in the nest, and the younger siblings often die without their removal (either as egg or hatchling). This also occurs in the Hyacinth Macaw (Anodorhynchus hyacinthinus, SA-2), which lays a two- to 132 three-egg clutch, and typically, only the oldest chick survives (Lticker & Paztwahl, 2000; Kuniy et al., 2006). Multiple clutching produces an excess of eggs and young which must be cared for appropriately (Fyfe et al., 1977). Often, when eggs are pulled from a breeding pair, they are artificially incubated and hand-reared, fostered by conspecifics, or cross-fostered by a similar species (Fyfe et al., 1977; Conway, 1980; Utt et al., 2008). Many times, the surplus of eggs mean that the young must be hand-reared, which for some species may provide undesirable behavioral results (see section on hand- and puppet-rearing). However, lesser-known detriments are also associated with clutch-removal. For example, one pair of captive-breeding Milky Storks (Mycteria cinerea, SA-1) appeared to suffer weakened pair bonding after their first clutch was removed for double-clutching (Yaacob, 1994). Courtship and nest building were disrupted by the removal of the clutch, subsequently resulting in infertile eggs. Beres and Starfield (2001) addressed an important question about the decision to use multiple clutching: do captive parents transmit survival skills that will help released captive-reared birds survive in the wild, or will released birds (not reared by their own parents) develop those survival skills in the wild and pass them on to their offspring? If captive-reared birds can acquire necessary survival skills from their parents or after their release to the wild, then multiple clutching and alternate rearing techniques continue to be useful tools in the captive propagation of many bird species. Recent research with the California Condor indicates that individuals experience similar survival rates even though rearing methods differ (Utt et al., 2008; Chapter 3). Moreover, multiple clutching does not preclude the use of parent-rearing techniques (Beres and Starfield, 2001). First 133 clutches can be reared by hand, puppets, foster, or cross-foster parents (Conway, 1980; Dixon, 1986; Utt et al., 2008). The second clutch could remain in the nest, hatch, and be reared by their natural parents if found to be suitable (Beres and Starfield, 2001). Parent-Rearing Aviculturists generally encourage parent-rearing in order to prevent inappropriate imprinting and behaviors, and to increase the likelihood of successful second-generation breeding in captivity (Mirande, 1985). The inquisitive and playful nature of some hand- reared birds (such as the Pesquet's Parrot, Psittrichas fulgidus, SA-2) could compromise successful breeding (Buay & Thirunavukkarasu, 2000). In one study on the Hawaiian Goose, results showed that birds which were parent-reared were able to integrate socially, display higher levels of vigilance, and avoid predators better than those which were hand- reared or visually mentored (Marshall and Black, 1992; van Heezik and Seddon, 1998). A study of the Grey Partridge (Perdix perdix, P-3) also showed that parent-reared chicks, as opposed to cross-fostered or sibling-reared, showed longer bouts of vigilance (Curio, 1998). Myers et al. (1988) compared hand- and parent-reared Cockatiels, (Nymphicus hollandicus, SA-2), and discovered differential reproductive success, with hand-reared males exhibiting reduced fertility. These results are intriguing and suggest that, at least for some species, the necessity of parent-rearing may be sex-specific. In comparing parent- and cross-foster reared partridges, Marshall and Black (1992) found that the latter learned inappropriate responses to predators. The results of the Grey Partridge and Hawaiian Goose studies indicate that parent-rearing is the best possible method to be implemented in captive-breeding scenarios for several crucial reasons: proper species- 134 specific imprinting, learned behaviors, social integration, and appropriate predator responses. However valuable parent-rearing may be circumstances exist when this rearing method may not be the most practical (Marshall and Black, 1992; Sweeny, 2000). The use of parent-rearing as a sole breeding method for endangered birds will not produce as many hatchlings as a combination of other rearing methods (Conway, 1980; Marshall and Black, 1992; Beres & Starfield, 2001). In addition, parent-rearing in captivity can lead to problems for some young birds. For example, captive breeding pairs, such as the Hyacinth Macaw, will sometimes refuse to rear their own progeny, and removal of the chicks may be the only method for their survival (Lticker and Patzwahl, 2000). Sweeney (2000) observed problems with Salmon-crested cockatoo parents breeding in captivity, such as inconsistent feeding behavior (e.g., failure to feed the chick after hatching or part way through the rearing period), biting of the chick's emerging pin feathers (c.f. Williams and Feistner, 2006), infestation of the chick by ectoparasites (most mite infestations originate from wooden perches, nest boxes, or nesting substrate), and damage caused by adults biting the wings and feet of the chicks (Sweeney, 2000). Pesquet's Parrots sometimes mutilate and kill their own young in captivity (Buay and Thirunavukkarasu, 2000). Researchers studying the Red Bird of Paradise (Paradisaea rubra, A) were forced to abandon their objective of comparing hand- and parent-reared chicks when two hatchlings became the victims of infanticide (Hundgen et al., 1991; Worth et al., 1991). Common Kestrels (Falco tinnunculus, SA-2) have also been known to kill their own chicks shortly after hatching, perhaps due to confusion over the dead domestic chicken (Gallus gallus; P-3) chicks, that were supplied to the adults as food but superficially 135 resemble young raptors (Jones, 1981; Brown, 1983). Other documented examples of infanticide include the Mountain Peacock Pheasant (Polyplectron inopinatum, P-3; Bruning, 2003), and Prairie Falcon (Falco mexicanus, SA-2; Enderson, 1972) In some cases, pairing of genetically compatible birds, may lead to behavioral problems (Kleiman, 1980; Wilson et al., 1994; Curio, 1998). Cockatiels with free mate choice, for example, had higher breeding success than those artificially paired due to genetics or other factors (Curio, 1998). Reproductive success of the Mauritius Kestrel was also lower when artificially paired in captivity compared to wild individuals with free choice (Jones et al., 1995). Many other examples exist in the literature where inappropriate parent pairing has lead to problems in reproduction, or for the chick (Tongren, 1985; Harvey et al., 2004; Cristinacce, 2008). This problem can sometimes be repaired if the captive stock is sufficient in numbers to substitute a new individual and allow for proper pair bonding. Thus, due to the potential setbacks of artificial pairing in some species, parent-rearing must be utilized with a degree of caution and oversight in captivity. Foster-Parenting Fostering is a technique used in many avian conservation programs (Saint Jaime, 1999). The theory behind fostering is that females of the same or closely-related species would pass information to the young about feeding techniques, food choice, habitat utilization, predator avoidance, and social behaviors (Saint Jaime, 1999). Fostering can be either intraspecific (conspecific) or interspecific (cross-fostering). Fostering can involve either eggs or hatchlings, and be conducted in captivity or directly in the wild 136 (Conway, 1980; Scott and Carpenter, 1987). The success of fostering can, in part, depend on the developmental mode of the species. Birds closer to the altricial spectrum will accept young up to a week of age, possibly even more, whereas highly precocial species have a smaller window to accept non-related chicks (1-3 days at most, Table 13; Ehrlich et al., 1988). Intraspecific (Conspecific) Rearing Conspecific fostering occurs when an egg or hatchling is placed with foster parents of the same species to be cared for, either in a captive-breeding environment or by parents living in the wild (Dixon, 1986; Wallace, 1994; Table 15). Foster-parenting typically involves removing eggs or nestlings from one nest and placing them in the nest of the same or similar species (Temple, 1977; Conway, 1980; Dixon, 1986; Wallace, 1994; Bunin & Jamieson, 1996a; Groombridge et al., 2001; Utt et al., 2008). The latter technique provides a method whereby the eggs or hatchlings of captive parents can be channeled back into the wild so that the young may learn the basics of survival from wild conspecifics or cross-foster parents (Dixon, 1986). This approach allows a captive breeding program to stay in close contact with a wild population and contribute directly to its survival (Dixon, 1986). Conspecific fostering, along with its benefits and possible downsides, has typically been considered functionally equivalent to parent-rearing. Conspecific foster- parents are chosen based on pair compatibility and previous history with caring for young. In some cases, conspecific fostering may be better than rearing by biological parents who are not well-matched. 137 Table 15. Cross-fostering examples in avian conservation. Captive-bred subject Cross-foster parents Contexe Reference Greylag Goose Canada Goose Wild/eggs Von Essen, 1982 (A. anser) (B. canadensis) Lesser White-fronted Goose (A. Barnacle goose (B. leucopsis) Captive/eggs, Von Essen, 1982; Momer, erythropus) chicks 1986 Hawaiian Goose ene; Domestic Chicken (Gallus gal/us), Captive/eggs Berger, 1977 (Branta sandvicensis) Domestic Duck (Anas platyrhynchos domestica), Silky Bantam (G. gallus) Bean Goose Canada Goose Wild/eggs Von Essen, 1982; Morner, (A. fabalis) (B. canadensis)s 1986; Ridley, 1986; Ounsted, 1987 Cheer Pheasant Domestic Hen (G. gallus) Captive/eggs Ridley, 1986 (Catreus Piping Plover Killdeer Captive/eggs Powell et al., 1997 (Charadrius melodus) (C. vocferous) Masked Bobwhite Scaled Quail (Callipepla squamata), Wild/chicks Ellis et al., 1977; Carpenter et (Colinus virginianus ridgwayi) Bantam Chicken (G. gal/us), Texas al., 1991 Bobwhite (C. v. texanus) Peregrine Falcon Prairie Falcon (F. mexicanus), Wild/eggs, Cade, 1977; Fyfe etal., 1977; (Falco peregrinus) Goshawk (Accipiter gentilis), chicks Cade, 1986; Wallace, 1994; Common Kestrel (F. tinnunculus), Craig et al., 2004 Common Buzzards (B. buteo) Whooping Crane Sandhill Crane Wild/eggs Wallace, 1994; Nagendran et (Grus americana) (G. canadensis tabida) al., 1996; Leary, 1997; Reed, 2004 California Condor Andean Condor Captivity/eggs, Utt et al., 2008 (Gymnogyps californianus) (Vultur gryphus) chicks Black Stilt Pied Stilt Wild/eggs Reed & Merton, 1991; Reed & (Himantopus novaezelandiae) (H himantopus),or hybrid Murray, 1993; Reed, 1994 Helmeted Honeyeater Yellow-tufted Honeyeater Captivity/eggs Smales et al., 1991; Miller, (Lichenostomus melanops cassidix) (L. m. gippslandicus) 1994; Smales, 1996 Chatham Island Black Robin Chatham Island Tit (P. Wild/eggs Dixon, 1986; Butler & Merton, (Petroica traversi) macrocephala chathamensis 1992 Chatham Island Warbler (Gelygone albofrontata) Takahe Pukeko Wild/eggs Bunin & Jamieson, 1996b (Porphyrio mantelli) (P. Porphyrio) Prairie Falcon Ferruginous Hawk (Buteo regalis), Wild/chicks Fyfe et 1977 Red-tailed Hawk (B. jamaicensis), Swainson's Hawk B. swainsoni) Ferruginous Hawk Prairie Falcon Wild/chicks Fyfe et al., 1977 a Location (wild or captivity)/ Developmental state (eggs or chicks) Interspecific (Cross-Foster) Rearing Cross-fostering is similar to intraspecific rearing, only that the egg or hatchling is placed with a different but closely-related species to be reared. Cross-fostering has been used as a technique to rear, prepare, and release young when not practical to allow captive parents to participate in the care and fledging process of their offspring (Wallace, 1994; Hansen & Slagsvold, 2004). Where a suitable foster species exists, cross-fostering has potential for extending the range of an endangered species into new areas or for re- establishing populations where they have been extirpated (Cade, 1977). Cross-fostering has been used successfully in many avian captive-breeding programs (Table 15; Hutchins, 1995; Bunin & Jamieson, 1996a; Slagsvold, 2004; Utt et al., 2608; Utt, 2010) Cross-fostering is used to increase productivity of a captive-breeding program, sometimes in conjunction with another captive-breeding technique, such as multiple- clutching (Berger, 1977; Fyfe et al., 1977; Monier, 1986; Reed et al., 1993; Bunin & Jamieson, 1996a; Utt et al., 2008). For critically endangered species of birds, fostering appears to be a safe and effective method for increasing the productivity of local, poorly- reproducing populations and to tide them over the period required to correct whatever factors may be responsible for the decline in population numbers (Cade, 1977). Several captive-breeding programs have used cross-fostering to bolster population numbers (Table 15; Reed et al., 1993). For example, with the use of the cross-fostering technique, the Chatham Island Black Robin increased from five to over 100 birds (Reed & Merton, 1991; Reed et al., 1993). Birds cross-fostered in the wild may learn adaptive behaviors suited to current environmental conditions, such as predator avoidance, which will positively affect 140 survivorship (Cade, 1977; Dixon, 1986; Bunin & Jamieson, 1996b). A study in the late 1930's with Mew Gull eggs (Larus canus, SP) cross-fostered by Black-headed Gulls (L. ridibundus, SP) indicated that although cross-fostered individuals adapted to their foster parent's nesting preferences, (from tree-nesting to colonial marsh nesting), they were able to recognize conspecifics and breed successfully (Table 15; Cade, 1977). This study indicates that, with some species, cross-fostering does not pose a threat of improper imprinting. However, it can raise the question of potential reduction of fitness by altering nesting habits and preferences. Another study with Lesser White-fronted Geese (Anser erythropus, P-3) cross fostered by Barnacle Geese (Branta leucopsis, P-3) indicated that although the lesser white-fronted geese learned new (desirable) migration patterns from their cross-foster parents, there was no indication of cross-species sexual imprinting (Table 15; Ounsted, 1987; Sutherland, 1999). Finally, several California Condors (Gymnogyps californianus, SA-1) cross-fostered to Andean Condors (Vultur gryphus, SA-1) successfully mated with conspecifics and reproduced in the wild (Table 15; Mace, 2006). Although conservationists adhere to the philosophy that individuals may acquire the behaviors of their foster-parent(s), cross-fostering between two species or subspecies which are very similar in behavior and morphology is considered to have only negligible adverse effects on imprinting of the fostered young upon the surrogate parents (Smales et at, 1991). Despite the success of cross-fostering in some captive-breeding programs, there are species for which this method can pose a problem (Hansen and Slagsvold, 2004). For example, male Whooping Cranes reared by Sandhill Cranes failed to recognize 141 conspecific females as appropriate mates, indicating a problem with sexual imprinting (Lewis, 1996). Incorrect sexual imprinting was also seen with Black Stilts (Himantopus novaezelandiae, P-3) cross-fostered to Pied Stilts (H. himantopus, P-3; Table 15; Reed et al., 1993). Black Stilts fostered to Pied Stilts or hybrids adopted their cross-foster parents migration patterns, thereby isolating fostered Black Stilts from their own species during the season when pair-bonding normally occurs. In addition, Black and Pied Stilts sometimes breed in the wild when there is a shortage of Black Stilt females or within range overlap, creating fertile hybrid offspring (Reed and Murray, 1993). Thus, cross- fostering two species which naturally interbreed is not advised, and can lead to further problems with species recognition and breeding. An individual Chatham Island Black Robin (Petroica traversei, A) paired and nested with its cross-foster species (Reed et al., 1993). Cross-fostered Herring Gulls (Larus argentatus, SP) and Lesser Black-backed Gulls (L. fuscus, SP) that survived to breeding age mated with members of their foster species, later leading to extensive hybridization between the two species (Cade, 1977). Several studies have examined the role of imprinting on call recognition. For example, Killdeer (Charadrius vociferous, P-2) cross-fostered by Spotted Sandpipers (Actitis macularia, P-2) still recognized their own species-specific alarm call (Reed & Merton, 1991; Powell & Cuthbert, 1993; Reed et al., 1993). Similar results were found with other cross-fostered avian species (Gottlieb, 1965; Fisher, 1966). Although cross-fostering may bolster the population of an endangered avian species, cross-fostering can be considered a failure if the cross-fostered individuals 'mimic 142 certain behaviors of their foster parents (e.g. undesirable migration patterns, inappropriate mate selection), or fail to breed with their own species (see above; Reed et al., 1993; Beres & Starfield, 2001). However, there are several reasons why some birds may not be adversely-effected by acquiring these traits. First, some birds, such as California Condors and their cross-foster parents, Andean Condors, do not naturally occur in the same continent (North vs. South America, respectively) and neither is strongly migratory. Geographic isolation of the foster and cross-foster species could alleviate potential negative long-term imprinting and possible hybridization with the incorrect species. Sympatric species that overlap in habitat use with their cross-fostered species may be at a higher risk for problems once released into the wild (e.g., Galahs [Cacatua roseicapilla] SA-2) and Major Mitchells' Cockatoo [C. leadbeateri, SA-2]; Rowley and Chapman, 1986). Second, a study on cross-fostered killdeer concluded that individuals cross- fostered with their biological siblings may be less prone to imprinting errors (Powell & Cuthbert, 1993). Third, cross-fostered species which have clear, species-specific markings may be better able to recognize conspecifics (Powell & Cuthbert, 1993). Shared attributes with nest mates may help overcome imprinting upon heterospecific parents. Fourth, if cross-fostered individuals are allowed to interact with wild conspecifics, incorrect imprinting may be avoided (Powell & Cuthbert, 1993). Fifth, Cade (1977) hypothesized that cross-fostering has greater long-term effects on precocial (r-selected) species than altricial (K-selected) species (Table 13; Wallace, 1994; van Heezik & Seddon, 1998). Thus, use of cross-fostering in avian conservation requires careful evaluation of past use of cross-fostering in the same or closely-related species, including behavioral flexibility of the subject species, shared habitat, possible undesirable 143 behaviors that might emerge from incorrect imprinting, and safeguards to reduce the chances of incorrect imprinting (Reed et al., 1993). In addition, depending on the species and its degree of sociality, cross-fostering can result in maladaptive behaviors such as sexual imprinting on the foster parent species (Cade, 1977; Rowley and Chapman, 1986; Wallace, 1994; Valutis and Marzluff, 1999). To reduce negative sexual imprinting and undesirable behaviors, cross-foster parents should be chosen from a closely-related species which exhibits similar behaviors (Wallace, 1994). The degree of sociality of a species may influence the effectiveness of cross-fostering, with less social species benefiting more from this method (Wallace, 1994; Table 16). Puppet and Hand Rearing Maybe the most relied upon tool in avian captive-breeding is hand- and/or puppet- rearing. Although not always emphasized in the literature, there is a distinct difference between hand- and puppet-rearing methods. Hand-rearing refers to humans rearing chicks directly, usually with little or no effort to conceal themselves from the young bird. Puppet-rearing utilizes a species-specific puppet head that masks the caretaker's hand in order to reduce the risk of human imprinting while feeding or caring for the chick (Wallace, 1994; Saint Jalme, 1999; Valutis and Marzluff, 1999). In some cases, humans dress in a full-body costume to feed, mentor, and train some birds (e.g., Whooping Crane; Horwich, 1989; Jamle, 1999; Sutherland, 1999). Hand-rearing appears to be the most frequent rearing choice. The risk of imprinting is a concern for those involved in captive- 144 breeding of endangered birds for reintroduction, and thus determining the appropriate combination of rearing and husbandry methods is imperative. 145 Table 16. Differences and implications of life history traits on various captive-breeding and release strategies, modified from Wallace (1994). r-selection characteristics K-Selection characteristics Short life span Long life span Produce many young (large clutches) One or two eggs (small/singular clutches) Short parental dependence period Long parental dependence period Low survivorship of offspring and adults High survivorship of offspring and adults Population stabilizes near carrying Population fluctuates greatly capacity Reaches sexual maturity quickly Reaches sexual maturity slowly High intrinsic rate of population increase Low intrinsic rate of population increase Captive-breeding implications Captive-breeding implications Parent-, foster-, or puppet-rearing may not Parent-, foster-, or puppet-rearing needed be needed May benefit from conspecific group-rearing Isolation from conspecifics until fledging Mentoring may have minimal effect "Wild" mentoring may be beneficial Limited by space and funding Reintroduction implications Reintroduction implications Larger number of releases and individuals Fewer releases needed to establish needed population Short incubation and fledging period Protracted incubation and nestling period Longer parental dependence and release Shorter, less complicated release process process 146 Imprinting and Developmental Phases Considering the susceptibility to imprinting on non-parental models during the rearing process is important in selecting the appropriate rearing technique(s) used in any captive-breeding program. In addition, the importance of knowing the developmental mode of the species of interest is essential for optimum success. An avian captive- breeding program must carefully weigh the needs and implications of both of these factors if captive-reared birds are to behave appropriately, survive, and ultimately reproduce in the wild. Imprinting can occur during several stages of development. Auditory imprinting can affect the behavior of a bird while still incubating. After hatching, filial and sexual imprinting can occur. Auditory imprinting is a complex process that varies based on the developmental mode (Table 13), exposure to artificial or natural sounds, pre- and post-natal procedures, and whether or not sounds are associated with visual objects (Moore, 2004). Thus, some suggest that proper imprinting begins even before hatching, and tape playback of adult conspecifc calls prior to hatching has been tried on several species of captive-reared cranes (Luthin et al., 1986; Horwich, 1989) as well as the Takahe (Porphyrio mantelli, P- 4; Maxwell et al., 1997). Taped calls of Turkey Vultures (Cathartes aura, SA-1) have been used while incubating and hatching California Condor eggs in captivity, although it is not clear why California Condor vocalizations were not used (Don Sterner, personal communication). Despite the use of taped calls in several captive-breeding programs, the effectiveness of this technique in reducing imprinting remains uncertain. Although some species can recognize their parent's call before hatching, Moore (2004) asserted that 147 auditory imprinting prior to hatching is unlikely because visual stimulation is also necessary for auditory imprinting to occur (Ehrlich et al., 1988). Post-hatching, auditory imprinting is continues and because it may be much more effective, it has been used with many breeding programs. For example, in New Zealand, taped calls of adult conspecifics were played while feeding hand-reared Kakapo in an attempt to reduce human imprinting associated with food (Sibley, 1993). Post-hatch imprinting can occur at different phases of the development process, anywhere between the neonate stage (filial imprinting) or at sexual maturity (sexual imprinting). Filial imprinting (or follow response) allows offspring to recognize their parents, who serve as role models for important skills such as foraging, predator avoidance, social behavior, and even migratory patterns (Slagsvold and Hansen, 2001). Filial imprinting occurs at a young age and can be focused on different Objects or species (Table 13; van Heezik and Seddon, 1998; McLean, 2002). Depending on the developmental mode, filial imprinting can occur quickly (in highly precocial young) or be delayed until fledgling (in most altricial young, Table 13; Burn, 1977; Rowley & Chapman, 1986; Ehrlich et al., 1988). Ring Doves (Streptopelia roseogrisea, A), for example, develop a fear of humans when raised by parents, but are "tame" if raised by hand before they are eight days old (Curio, 1998). In addition, a study of hand-reared Scarlet Macaws (SA-2) indicated birds given affection post-fledgling showed an increase in attraction to humans compared to those not given affection post-fledgling (Brightsmith et al., 2005). These studies illustrate how important understanding the developmental class and life history of the species can be in implementing captive-breeding program (Sarrazin and Barbault, 1996). 148 Sexual imprinting occurs later in development than filial imprinting and parents serve as models for later sexual preferences (Valutis and Marziuff, 1999; Slagsvold and Hansen, 2001). Slagsvold and Hansen (2001) assert the presence of two distinct stages of sexual imprinting. The early acquisition phase occurs early in development where sexual preference is established, and the consolidation phase occurs when the early acquired preference is linked to sexual behavior and stabilizes. Although time-consuming and expensive, species-specific puppets are commonly used to avoid sexual (and even filial) imprinting in modern captive-breeding programs (McLean, 2002). Abnormal behavior displays in hand- or puppet-reared altricial birds, such as begging for food in the presence of humans or responding sexually to human handlers instead of with conspecifics, have been attributed to filial and sexual imprinting to humans (Cooper, 1977; Cade, 1980; Erickson and Carpenter, 1983; Valutis and Marzluff, 1999; Sweeny, 2000; Elliot et al., 2001). Some species appear to be more susceptible to improper imprinting and behavioral displays than others (Van Heezik et al., 1999). Susceptibility to mis-imprinting not only depends on developmental phase, but can vary among different species of the same genera (Tables 13, 16). In Gruidae, the Sandhill Crane, Red Crowned Crane (Grus japonensis, P-4), and Stanley Crane (Anthropoides paradisea, P-4) were wilder when raised in isolation from humans, whereas the Siberian Crane (G. leucogeranus, P-4) showed little difference in behavior from those reared by hand (Luthin et al., 1986). However, it appears that most birds in a taxonomic family share the same life history traits, development phase, and possibly even tendency towards imprinting (Table 17). Even if a bird does not imprint on its human caretaker, mere contact with humans can be disadvantageous (Cooper, 1977). For example, Snyder and 149 Snyder (1974) showed increased mortality in wild-reared Cooper's Hawks (Accipiter cooperii, SA-1) that were accustomed to humans. Although the risk of imprinting is high with some avian species, aviculturists should bear in mind that imprinting (filial or sexual) may not be permanent in all species and may be overridden by future experiences in an individual (McLean, 2002). 150 Table 17. Developmental classes and corresponding representative Avian families. Families in bold represent life history characteristics different from the rest of the Avian families in a given developmental class. Class Examples in Avian families Imprinting Precocial-1 Megapodiidaerfic Immediate at hatch Precocial-2 Charadriidaer, Scolopacidaer, Tytonidaer, ApterygidaeK , Anatidaer' a Precocial-3 Haematopodidaer, Odontophoridaer, Phasianidaer, Recurvirostridaer, Anatidaer Precocial-4 GruidaeK, OtididaeK, Rallidaer , Semiprecocial BalaenicipitidaeK , LaridaeK, SturnidaeK, PhoenicopteridaeK, DiomedeidaeK, _ Caprimulgylaer Altricial-1 Ciconiidae, ThreskiornithidaeK, AccipitridraeK , CathartidaeK, SpheniscidaeK Altricial-2 FalconidaeK, HydrobatidaeK, PsittacidaeK, StrigidaeilK / Altricial Trochilidaer, Columbidaer, Alcedinidaer, Cuculidaer, BucerotidaeK, Passeriformesr'b, Delayed until Picidaer fledging r-selected life history traits K-selected life history traits a exception; Laysan Teal (Anas laysanensis) exhibits K-selected life history traits b Entire order of Passeriformes, except for the family Stumidae Puppet-Rearing Several _captive-breeding programs employ puppet-rearing techniques to help prevent human imprinting during development, including those for the Takahe, California Condor, Houbara Bustard (Chiamydotis undulata, P-2), Mississippi Sandhill Crane (Grus canadensis pulla, P-4), and Mauritius Kestrel (McMillen et al., 1987; Maxwell and Jamieson, 1997; Van Heezik et al., 1999; Utt et al., 2008). Programs with puppet-rearing and isolation techniques have produced birds that are wary of humans (Luthin et al., 1986; Sheppard, 1987; Wallace, 1994; Valutis and Marzluff, 1999). Recent research on captive-reared California Condors has shown that although a bird may be hand- or puppet-reared, it does not preclude normal functioning in the wild or within a social hierarchy (Utt et al., 2008; Chapter 3). In fact, some studies indicate that puppet-reared birds had a higher post-release survival compared to those that were hand-reared (Common Ravens, Corvus corax, A, Valutis and Marzluff, 1999; Mississippi Sandhill cranes, Ellis -et al., 2000), while others indicate no survival differences between rearing methods (Houbara Bustards, van Heezik and Seddon, 1998; Mauritius Kestrel, Nicoll et al., 2004; Whooping Cranes, Grus americana, P-4, Kreger -et al., 2006; California Condors, Woods et al., 2007; see Chapter 3). Hand- and puppet-reared Kakapos exhibited no imprinting toward humans when implementing appropriate precautions (e.g., minimal human contact, use of a puppet, taped playback of adult conspecifics while feeding, and contact with other juvenile conspecifics; Sibley, 1993). Hand-reared raptors may form imprinting attachments to humans as well as to their own species, as observed in Peregrine Falcons (Jones, 1981). In this example, -many falcons showed appropriate sexual responses and became 152 reproductively competent with conspecifcs despite having some attachment (filial imprinting) to humans (Jones, 1981). Houbara Bustards (Chlamydotis undulata, P-2) became less tame when prolonged exposure to humans ceased, suggesting that, at least for some species, minimizing human contact using models and harriers is unnecessary, and all that is required to produce birds wary of humans is a period of time when exposure is minimized (van Heezik et al., 1999). Valutis and Marzluff(1.999) argued that some species only need to be raised with conspecifics to promote correct sexual imprinting, even when exposed to humans (Table 16). In some programs, researches have gone beyond the use of a model of the adults head to -ensure proper imprinting. For example, two breeding programs, for the Mississippi Sandhill Crane and the Whooping Cranes, dressed human caretakers in species-specific-crane costumes to show novice -cranes appropriate crane behavior (Horwich, 1989; Jamie, 1999; Sutherland, 1999). Integrating the full body costume at appropriate periods in -development produces cranes that are better able to recognize conspecifics, forage, and recognize predators (Horwich, 1989). Utilizing puppets during the nestling phase may not influence appropriate sexual imprinting, and it remains uncertain whether correct filial imprinting affects the success of reintroductions (Valutis and Marzluff, 1999). The appropriateness of puppet-rearing birds not only depends on when in development it is employed but also the sociality of the species (Table 1-6). 153 Hand-Rearing The method of hand-rearing has been used successfully with many endangered birds, including the San Clemente Loggerhead Shrike (Lanius ludovicianus mearnsi, A), Yellow-shouldered Amazon Parrot (Amazona barbadensis, SA-2 ), Alala (Corvus hawaiiensis, A), Scarlet Macaws (Ara rnacao, SA-2), Takahe, and the Kaka (DeBlieu, 1993; Wallace, 1994; Kuchler et al., 1995; Maxwell et al., 1997; Sanz -et al., 1998; Brightsmith et al., 2004; Farabaugh, personal communication). Other studies indicate birds reared in captivity can form unnatural bonds with their caregivers. The worst possible scenario for hand-reared birds is when a bird bonds with its human caregiver rather than its own species (Saint Jaime, 1999). Female hand- reared Eastern Sarus Cranes (Grus antigonie sharppi, P-4) were prone to human imprinting, and exhibited-dance-displays whenever human male caretakers approached their enclosures (Mirande, 1985). However, this result may not be completely unexpected since cranes are precocial-4 and sensitive to early exposure to human caretakers (Tables 13, 16). Numerous species of raptors hand-reared in captivity have reportedly become sexually imprinted on humans rather than their own species (Berry, 1972; Temple, 1972; Grier, 1973; Boyd et al., 1977; Cade and Fyfe, 1978; Cade, 1980). The Salmon-crested Cockatoo also exhibits varying levels of "inevitable" imprinting on their human caregivers (Sweeny, 2000). Hand-reared Salmon-crested Cockatoos were prone to exhibiting imprinted behavior, such as begging for food in human presence (Sweeney, 2000). Problems associated with imprinting in cockatoos included increased mate aggression, reduced frequency or improper copulation, weaker pair-bonding behavior (many imprinted birds continued to show a preference for human 154 bonding well into maturity), and delayed exhibition of breeding behaviors and reproductive maturity (Sweeney, 2000). Use of conspecific adult mentors (discussed later) may to help to alleviate or prevent improper imprinting of hand-reared birds. In fact, Mendelssohn and Marder (1983) asserted that if hand-reared birds are exposed to adult conspecifics during development (i.e., mentors), the use of puppets in the rearing process may be altogether unnecessary in some species. Often, little thought is given to possible developmental or growth delays when hand-rearing a bird. Mace (1991) found that hand-reared Tickell's Laughing Thrushes (Garrulax strepitans, A) weighed less than their parent-reared counterparts throughout development. Although no explanation was offered to explain the differential development, attention to growth rates and potential long-term effects on captive-reared birds should be investigated. The importance of rearing birds wary of humans becomes less essential if the bird is to permanently remain in captivity. In fact, some feel that a degree of tameness (or filial imprinting) can be an asset in reducing trauma, assisting induction of breeding, and facilitating egg removal and/or substitution (Erickson and Carpenter, 1983; Valutis and Marzluff, 1999). However, species that show marked human imprinting (sexual imprinting) which impacts their ability to attract a mate and reproduce should not be reared with this method. Understanding the species' breeding biology and life history traits are essential to making the correct management decision (Kleiman, 1980; Sarrazin and Barbault, 1996; Reed, 1999; Table 145). 155 Group versus Isolate Housing The sociality of the species may play an important role in determining if a bird would do well in a group of conspecifics at a pre-fledgling age (Kleiman, 1980). Tintner and Kotrschal (2002) compared group and isolate rearing of the Waldrapp This (Geronticus eremita, SA-1), a colonial-nesting species, and found that chicks raised in a group environment experienced faster -development, increased social interactions, and earlier fledging than those reared in isolation from conspecifics. Results indicated Filial imprinting (early parental recognition) is most prevalent in species where young are mobile (see above) or reared in a communal/social group environment (Ehrlich et al., 1988). Thus, it would be prudent to conclude that in avian species normally reared in a colonial breeding environment, those having a clutch size of more than 2-3 (an attribute of r-selected life history trait, Table 16), or those with a developmental phase ranging from Precocial-1 through 4, should be reared in group environments for optimal development and behavior (Tables 13, 16; Kleiman, 1980). Other birds reared in isolation from conspecifics which have been known to exhibit improper imprinting include Whooping Cranes, Shoebills (Balaeniceps rex, A), and Helmeted Honeyeaters (Lichenostomus melanops cassidix, A; Sauey & Brown, 1977; Luthin et al., 1986; Smales et al., 1991). At times, rearing environment can affect other aspects of captive-reared birds, such as breeding behavior. Hawaiian Cr-OWS normally have a-clutch size ranging from 1- 4, and chicks are typically raised in a social environment with siblings (Table 14, Harvey et al., 2002). A study comparing group versus isolate rearing of Hawaiian Crows found that although isolate-reared males were able to breed with females, they engaged in more 156 "play" behavior which frequently disturbed the female's nest preparation and incubation, sometimes leading to clutch loss (Harvey et al., 2002). These results indicate that species typically reared with siblings (or in a colonial atmosphere) should not be reared in isolation. The opposite can be said for avian species typically reared in single clutches (e.g., California Condor). Clark -et al. (2007) found that California Condors exhibited more appropriate behaviors if reared in isolation versus a group environment. In fact, early in the captive-breeding program, -condor juveniles were housed in large groups, leading to abnormal aggression and social dominance. Thus, for avian species with small clutch sizes (1-2 -eggs), it may be a better approach to raise chicks in isolation from each other until an age when birds would normally fledge and begin interacting with other non- familial birds. Ultimately, timing of fledging and grouping experience may affect initial survival upon release to the wild, such that highly social species reared in isolation may experience higher mortality (Stark and Ricklefs, 1998; Titner and Kotrschal, 2002). Behavior Management Captive breeding programs -often fail because of behavioral problems (Sutherland, 1998). Problems that arise during captive breeding can often be attributed to our lack of -knowledge of social behavior (Kear, 1977; Kleiman, 1980; Sutherland, 1998). For example, some species are unable to cope with the inability to choose their own mate (Kleiman, 1980; Sutherland, 1998; Saint Jaime, 1999). This can lead to reproductive 157 failure or, if a mismatched pair does propagate, inadequate parenting which may prove deleterious for the offspring. Maintaining animals in appropriate social groupings can facilitate growth, proper development of social behaviors, and natural breeding of birds in captivity (Kleiman, 1980; Tongren, 1985; Saint Jaime, 1999; Tintner and Kotrschal, 2002; Hallagar, 2004). Sociality and grouping tendencies of captive-bred species must be evaluated to properly provide species-specific needs (Kleiman, 1980). For example, Chilean Flamingos (Phoenicopterus chilensis, SP) and Caribbean Flamingos (P. r. ruher, SP) in zoos will often breed when maintained in large flocks, but rarely when kept in small groups (Stevens, 1991; Pickering -et al., 1992; Stevens & Pickett, 1994). This is also seen with two other colonial bird species, the Indian Painted Stork (Mycteria leucocephal, SA-1) and the Yellow-billed Stork in isolation from conspecifics showed increased solitary behaviors compared with those reared in groups (Tintner and Kitrschal, 2002). Understanding and accommodating the breeding ecology of a species may be important to facilitate successful breeding in captivity as well as to reduce the behavior problems (e.g., mis-imprinting; Table 14). Some avian species, the Whooping and Sandhill Cranes for example, need isolation for successful breeding (Tongren, 1985; Luthin et al., 1986). Pairs bond through intricate dancing displays. Consequently, paired cranes behave more aggressively towards other individuals, necessitating complete visual separation from other cranes in captivity (Tongren, 1985). Aggressive behavior in pair-bonded individuals has been observed in other avian species bred in captivity, including Salmon-crested Cockatoos (Sweeny, 2000) and Black Stilts (Reed, 1994). However, it must be stressed that group- 158 housing of hatchlings and/or juveniles may only be beneficial with species which are naturally colonial or highly social. Species which typically have an extended period of parental care and small clutches (1-2 eggs) should not be placed in communal rearing environments until a designated -developmental stage (e.g., fledgling age). For example, Andean Condors typically raise and care for one chick every other year. In one study, juvenile Andean Condors (approximately 6 months of age) were housed communally and consequently displayed aggression for periods of up to 3 weeks (Erickson and Carpenter, 1983). Placing individuals which come from an intimate rearing history with a large group of conspecifics at a young (pre-fledgling) age may elicit unnatural behaviors, such as intense aggression (leading to skewed dominance hierarchies) or other behavioral abnormalities, and should be cautioned against unless appropriate species-specific research has already been conducted (Clark et al., 2007). Abnormal levels of aggression are especially common among raptors socialized to humans (Jones, 1981; Park, 2003). The more socialized a raptor is to humans, the more dangerous it can become to humans and conspecifics alike, leading to problems such as mate aggression, which interferes with reproduction. Aggression can also be an outgrowth of an unnatural rearing or social environment (see above). It has been suggested that animals removed from the wild and reared in captivity can change behaviorally and become significantly different from wild populations (Kleiman, 1980). This can lead to problems with foraging, predator avoidance, and competing with conspecifics for resources (Hutchins et al., 1995; Snyder et al., 1996; Gippolifi, 2004; Snyder and Snyder, 2005). Some captive-reared animals may be behaviorally -unable to cope with a wild environment due to lack of important behaviors 159 normally acquired in the wild from parents (Saint Jaime, 1999). Captive breeding can select behavior and genotypes which are maladaptive in the wild (Fyfe, 1977; Kleiman, 1980; Lynch and O'Hely, 2001; McPhee, 2003; Gippoliti, 2004). The question becomes, how much behavioral change is acceptable in captivity and can captive-breeding produce birds that behave like wild birds (Beres and Starfield, 2001)? Some birds reared in captivity have shown a decrease in undesirable behaviors after becoming socialized with their own species. Conspecific fostering or mentoring may help alleviate some behavioral problems associated with captive rearing, such as improper imprinting, but may depend on when in development a bird is exposed to conspecifics or adult mentors (Utt et al., 2008). For precocial birds with an early period of imprinting and short parental dependence period (r-selected species), it is imperative to be exposed to their own species as soon as possible (within a few days post-hatching; Table 13). Altricial (SA-1 through A, Table 13) birds with an extended period of parental care and extended social development (K-selected species) may have more flexibility during the imprinting period; however, the sensitive period also may be longer (Valutis and Marzluff, 1999; Moore, 2004). These factors must be considered and addressed for •each species to potentially alleviate or prevent behavioral problems unique to captivity. Pre-Release Training Captive-breeding of threatened and endangered birds goes hand-in-hand with preparation for reintroduction (Fernandez and Timberlake, 2008). While some birds remain in captivity for breeding stock, advocates of captive breeding programs readily agree with the goal of eventual release-of-captive-bred birds (Imboden, 1987; Fernandez 160 and Timberlake, 2008). Reintroduction is generally initiated only after more conservative techniques (e.g., habitat protection, law enforcement, and public education) have been unsuccessful in restoring population levels (Scott and Carpenter, 1987). Potential benefits of reintroduction programs include increasing the number of animals in a small population, increasing genetic diversity in a small population, reducing inbreeding depression in small populations, and establishing new populations (Scott and Carpenter, 1987). Although captive breeding has the potential to increase genetic diversity and reduce inbreeding depression, typically breeding programs -do not get underway until a population is very small (e.g., Hawaiian Crow, 29-30 individuals; California Condor, 27 individuals; New Zealand Fairy Tern {Sterna nereis davisael; SA-1, 16-18 birds); Seychelles Magpie Robin [Copsychus sechellarum] A, 12-15 birds); Chantham Island Black Robin, 7 individuals), thereby limiting some of the potential benefits of captive breeding (Flack, 1975; Parrish & Honnor, 1997; Harvey et al., 2002; Snyder, 2007; Sutherland et al., 2010). Many failed reintroductions have involved releases of inexperienced captive-bred birds (Marshall and Black, 1992). With this in mind, husbandry and training techniques have been developed to prepare naïve captive-reared birds for life in the wild. Behavioral training in skills such as predator avoidance and foraging have been used to improve the success of avian reintroductions (Saint Jaime, 1999; Ward and Schlossberg, 2004). Different applications of pre-release training exist, including predator recognition and avoidance, power pole avoidance, foraging skills, soft releases, and other survival techniques (McLean et al., 1999; Griffin -et al., 2000; Alagona, 2004; Ward and Schlossberg, 2004; Woods -et al., 2007). Training captive-reared birds prior to 161 reintroduction has proven to be a critical part of many successful reintroductions, and many of the techniques -discussed in the following sections were implemented after high post-release mortality, injuries, or behavioral issues became apparent. Mentoring Mentoring, one of the newer techniques in behavioral modification may be the most useful method for preparing novice birds to behave appropriately in the wild, although its efficacy may depend on life history and developmental patterns. Mentoring is the process whereby one or more captive-reared juveniles are housed with one or more adult (of approximate breeding age) non-parent conspecifics in an isolated pen prior to release (Kaplan, 2002; Bukowinski et al., 2007; Utt et al., 2008). McLean (2002) suggests that the cultural transmission of behavioral traits may be disrupted if young individuals are isolated from their parents before acquiring such traits (Marshall and Black, 1992). Some experts observed that, in altricial species with extended parental care, the behavioral deficiencies of captive-bred stock isolated from parents or conspecific foster parents have sometimes been overcome by conspecific fostering or "mentoring" (Snyder et al., 1996; Snyder and Snyder, 2005; LAI et al., 2008). Mentoring may also be useful, though probably less affective, if a young bird is allowed to view other conspecifics in a separate enclosure without direct interaction (i.e., visual mentoring), thereby preventing incorrect imprinting on humans or siblings by being able to observe proper behaviors (Sauey and Brown, 1977; Mendelssohn and Marcler, 1983; Marshall and Black, 1992; Clark et al., 2007). 162 Perhaps the best documented example of mentoring in captivity is the California Condor (Risebrough, 2002; Bukowinski et al., 2007: Utt et al., 2008; Chapter 3). After early releases into the wild, some condors exhibited undesirable behaviors, including showing little or no aversion toward human activities, structures, or potential predators (Snyder and Snyder, 2000; Nielson, 2006). The majority of released captive-raised condors exhibiting behavioral problems were puppet-reared (Meretsky -et al., 2000; Snyder and Snyder, 2000; Chapter 3). Beginning in 1999, several California Condor breeding facilities implemented a mentoring program designed to facilitate more appropriate "condor" behavior in puppet-reared juveniles prior to their release into the wild (Kaplan, 2002; Snyder and Snyder, 2005). Contrary to the theory that mentoring would prove effective in managing behavior, results of a recent study (Chapter 3) indicated that mentoring had no measurable effect on the "misbehavior" of released, captive-reared California Condors. These results only reflect a crude measure of what was deemed "appropriate" behavior by release site officials. The mentoring presumably yielded more subtle (but unmeasured) behavioral changes because mentored birds experienced significantly improved survival. Mentoring may be beneficial to some species more than others, and its success may also depend on the temperament of the individual mentor. Vocal tutoring may benefit certain species raised in captivity for release to the wild. Freeburg (1996) paired young Brown-headed Cowbirds Wolothrus ater; A) with individual "tutors" to facilitate appropriate song learning and sexual imprinting. The tutor could be a conspecific, heterospecific, or taped playback of songs. Results indicated that adult -tutoring was -effective and that the young birds tended to adopt the breeding 163 preference of their tutor. This study demonstrates that the development of certain behaviors is open to the influence of experience when the social context is complex and interactive, not unlike the social dynamic of birds in the wild. The use of a heterospecific "tutor", the Maui Parrotbill (Pseudonestor xanthopkys, SA-2), was proposed to encourage acclimation and proper feeding in recently captured Hawaiian Honeyereepers (Melamprosops phaeosoma, SA-2; Groombridge et al., 2004) Success in visual mentoring (allowing visualization of adult conspecifics, but with no interaction with them due to adult aggression or-other factors) has been documented for the Griffon Vulture (Gyps fulvus, SA; Mendelssohn and Marder, 1983). A young hand-reared Griffon Vulture was exposed to adult conspecifics while at the same time being isolated from humans. The young vulture displayed normal courting behavior (as observed in captivity) to another Griffon Vulture in its second year, by manipulating nesting material jointly with another individual (Mendelssohn and Marder, 1983). Visual mentoring has also been used with effectiveness in young Lappet-faced Vultures (Torgos tracheliotus negevensis, SA-1) and Hawaiian Geese (Mendelssohn and Marder, 1983; Marshal and Black, 1992). If it is unsafe to allow juveniles to interact directly with adult mentors, visual mentoring may be a suitable alternative. Mentoring presumably prepares captive-reared individuals to adapt more readily to life in the wild. For example, many wildfowl are characterized by behavioral patterns learned from their parents and other conspecifics (mentors), which may enable individual members of reintroduced groups to acclimatize more easily to the wild (Ounsted, 1987). Social mentoring in the wild is important to the behavioral -development of many avian species. 164 Mentoring may be most effective if a wild mentor was used in place of a captive- reared mentor. An inexperienced mentor (i.e., captive-reared adult mentor) might be less effective teaching appropriate behaviors and social organization to young captive-reared individuals (Kleiman, 1980). Thus, proper mentoring would not only require a reproductively mature adult of the same species, but also one which has experience living in the wild (i.e., ."wild"). Mentoring may be especially useful in species with an extended period of parental care or altricial young. In altricial young, the sensitive period for imprinting is typically longer than with precocial young (Jones, 1981; Wallace, 1994). Therefore, birds exposed to adult conspecifics during this time are more likely to show appropriate predator avoidance behaviors (Jones, 1981; Wallace, 1994). Imprinting for precocial chicks occurs during a relatively short sensitive period early in the life of the individual (soon after hatching), because in the wild they must quickly follow the adult for food, protection, and warmth (van Heezik and Seddon, 1998). Thus, species with precocial chicks or shorter periods of parental care may not need mentoring, provided the young are able to imprint on their own species before exposure to humans (Jones, 1981; Wallace, 1994). The permanence and flexibility of imprinting is not only related to the developmental class of the young, but also depends upon the life-history traits of the species (see above; Table 16; Jones, 1981; Wallace, 1994). Some species have defined imprinting periods, while others are more open-ended (Lorenz, 1973). Mentoring may be useful for captive-reared chicks which cannot stay with their parents during the sensitive imprinting period, thus avoiding human exposure. 165 Predator Avoidance Predators are frequently either a major cause of species decline or represent a barrier to reestablishment of a species in an area from which it has become extirpated (Curio, 1998; McLean et al., 1999; van Heezik et al., 1999). Likewise, mortality due to predation is a major cause for many failed reintroduction or translocation programs (Priddel and Wheeler, 1994; Snyder et al., 1994; McLean et al., 1999; Griffin et al., 2000; Seddon et al., 2007). Reintroduced captive-reared animals are typically naive to potential predators as well as other aspects of their new environment (Curio, 1998; McLean et al., 1999; Lynch and O'Hely, 2001; Seddon et al., 2007). Animals that have been isolated from predators may no longer express appropriate antipredator behavior (Griffin -et al., 2000). Therefore, it is imperative that animals be able to recognize a predator the first time it is encountered and exhibit appropriate antipredator behavior. Because animals raised in captivity have adapted to life in a predator-free environment, methods were developed to reduce the typically high mortality of newly-introduced individuals, such as moving animals to predator-free environments, building predator-proof enclosures, and eradicating predators (Sutherland, 1998; van Heezik et al., 1999; Griffen et al., 2000; Waniess et al., 2002; Reynolds et al., 2008). None of these methods offer a long-term solution to predator-induced mortality. Research has shown that naive animals which initially show no fear toward predators can be conditioned to respond to live and model predators (van Heezik et al., 1999; Griffin et al., 2000; McLean, 2002). Antipredator training has been used successfully in a number of studies to improve predator recognition and survival in the wild (Table 18). For example, Ellis et al. (1977) trained Masked bobwhites (Colinus virginianus ridgwayi, P-3) to avoid humans 166 and domestic dogs (Canis familiaris) before release to improve survival, (Sarrazan and Legendre, 2000; Table 18). McLean et al. (1999) demonstrated that New Zealand Robins learned to respond fearfully to a model predator when they viewed a model conspecific in an aggressive mobbing posture beside the predator, or when chased by a model predator (Griffin et al., 2000) Care must be taken during antipredator training to avoid possible habituation to the predator model. Houbara Bustards tended to show habituation by decreased frequencies in alarm calls and attempts to avoid the predator model during training (van Heezik et al., 1999). Predator habituation may be avoided or minimized by only having exposure to the predator model a few times, which more closely resembles natural occurrences in the wild. For some species, reduction in exposure to model predators may not be enough to prevent predator habituation (van Heezik et al., 1999). Because it is difficult to simulate a realistic encounter with a predator by using a model, van Heezik et al. (1999) postulated that repeated exposure to predator models may not be associated with a negative experience. Some animals are able to quickly assess the risk posed by a predator or predator model and respond accordingly (van Heezick et al., 1999). Thus, Van Heezick et al. (1999) modified anti-predator training and used a live predator, a Red Fox (V. vulpes), which significantly improved the post-release survival of bustards. Unfortunately, even though safeguards were in place to prevent the fox from harming the bustards, three received injuries and one died. Although using a live predator was more effective in this study, implementation of this training technique should be approached with caution due to ethical and legal issues (van Heezick et al., 1999). 167 Table 18. Pre-release training methods and outcomes Species Rear' Training employed Outcome upon release Outcome' Reference Sanz & Grajal, Yellow-shouldered P, F, H Observed wild parrots from aviary Birds exhibited appropriate Down-listed to Amazon Parrot and exposed to predators, Boa predator recognition, foraging, VU 1998; IUCN, 2009 Amazona barbadensis constrictor and Parabuteo and social behaviors unicinctus Eurasian Eagle Owl Trained to catch live prey prior to Successful foraging, although LC, population Johnson, 1991 Bubo bubo release power pole avoidance training decreasing. would have been beneficial Houbara Bustard P, H Trained with a live model predator Significant improvement in Uplisted to VU, Van Heezik et al., Chlamydotis (fox) and taped alarm calls post-release survival population 1999; IUCN, 2009 [undulata] macqueenii decreasing. Masked Bobwhite CF, H Exposed to dogs (Canis familiaris) Increased post-release survival EN, slight Ellis et al., 1977; Colinus virginanus and harassed by humans and Harris' (able to hide, freeze, or flush in population Carpenter et al., ridgwayi Hawks (Parabuteo unicinctus) presence of predator) increase 1991; Marshal & Black ,1992: Hawaiian Crow P, H, PT Hacked into large predator-proof Majority of released individuals EX in wild due Kuehler et al., 1995; Corvus hawaiiensis release aviary acclimatize to natural survived through 19 mo. post- to disease and Harvey et al., 2002; habitat and learn to forage release. predation. Wesley, 2003 Hawaiian Goose P, F Released into large predator-proof Successful — birds were joined Down-listed to Berger ,1977; Branta sandvicensis release enclosures to acclimatize to with wild conspecifics post- VU. Population IUCN, 2009 natural habitat, learn to forage and release increase. fly Mississippi Sandhill H, P, PT. Observed wild cranes from outdoor Successful — birds were able to EN, population McMillen et al., Crane CF aviary, developed site fidelity, join wild conspecifics and increasing 1987; Nagenclran et Grus canadensis pulla learned to forage for natural foods, migrate, proper predator al., 1996; exposed to taped alarm calls in avoidance Sutherland, 1999; response to dangers, trained by Ellis et al., 2000 humans in crane costumes California Condor H, P, PT, Trained with electrified mock power Reduction in attraction to Wild Meretsky et al., Gymnogyps F, CF pole to deter attraction to the power poles since population 2000; Uft et al., californianus structure implementation (although increasing and 2008; Walters et al., inability to avoid power lines breeding 2008 still a problem) Table 18. Pre-release training methods and outcomes, continued. Species Rear' Training employed Outcome upon release Outcome" Reference New Zealand Robin CF Viewed model cohspecific exhibiting Avoidance of predator species, Survived McLean et a ., 1999 Petroica australis appropriate antipredator behavior, even in predator-naive birds release through chased by model cat, (Fel-is catus) or 6 months, ferret (Mustela furo) population increasing Takahe Porphyrio P, H, CF, Frightening the birds with the model Avoidance of predator species EX due to Saint Jaime, 1999; hochstetteri PT stoat, observing stoats attacking and implementation of habitat loss and IUCN, 2009 model conspecific (which emitted appropriate alarm calls possible distress calls) hunting Thick-billed Parrot H,P Diet supplemented with pine Captive-reared birds failed to EN, population Snyder et al., 1994 Rhynchopsitta cones(typical food in wild), observed join wild flocks, eat from pine decreasing pachryhyncha wild parrots from outdoor aviary cones, or display normal vigilance, while wild-caught birds fared better San Clemente P, H Released into large predator-proof Increased survival and breeding Population Farabaugh, personal Loggerhead Shrike release enclosures to acclimatize to rates in the wild increasing communication Lanius ludovicianus natural habitat, learn to forage for mearnsi live prey, supplemental food after release Puerto Rican Parrot CF, H Exposure to silhouette of Red Tailed Parrot developed aversion to CR, population Brock and White, Pt Amazona vittata Hawk, Bute° jamaicensis, observe predator, with yr survival increasing 1992; White et al., hawk attack of tethered Hispaniolan rate of 41% 2005 Parrot, Amazona ventralis aRearing methods: Parent (P), conspecific foster (F), cross-foster with different species (CF), hand-reared (H), puppet-reared (PT) bProgram outcome with current IUCN status: extinct (EX), extinct in wild (EW), critically endangered (CR), endangered (EN), vulnerable (VU), near threatened (NT), least concern (LC; IUCN, 2009). For a predator-recognition training program to be considered successful, two criteria should be met: predators (real or modeled) need to elicit appropriate responses in captive subjects and released birds must survive to breeding age. Birds have learned aversion to predators and demonstrated proper avoidance behaviors, but data indicating increased survival post-release are lacking (McLean, 2002). Obstruction Avoidance Some species tend to have problems avoiding or recognizing dangerous human- made obstructions or structures (e.g., power lines, windmills, etc). California Condors, cranes, and many other species have died by colliding with high-power electricity wires (Archibald, 1977; Johnson, 1992; Wallace, 1994; Bayle, 1999; Saint Jaime, 1999; •Meretsky et al., 2000; HaHagar, 2004; Kreger et al., 2006; Grantham, 2007; Reynolds et al., 2008). In addition, many birds have an affinity for perching atop power poles. In an effort to train species having an affinity to perch on power poles to avoid the potentially deadly structures, mock power poles have been set up in pre-release aviaries, as well as in their rearing environment (Saint Jaime, 1999; Utt et al., 2008). The mock power poles are designed to deliver a mild electric shock to a bird which tries to perch upon it. The mock power poles have proven useful in deterring the birds from approaching power lines too closely and can be considered a successful tool in pre-release training (Woods et al., 2007). Although trained birds learn a negative association with power poles, many still have difficulty seeing power lines and suffer power line collisions or electrocution (e.g. Eurasian Eagle Owl, Bubo bubo, SA-2; Bayle, 1999). Unfortunately, no feasible way to train birds to see power lines has been implemented and the responsibility has remained 170 with power companies to make the lines more visible to birds. Other species have also had collisions with power lines or other structures, including the Red-crowned crane (Grus japonensis; P-4), and Great Bustards (Otis tarda, P-4; Archibald, 1987; Johnson, 1992; Lane et al., 2001). Release Methodologies Choosing the appropriate release method is imperative for setting up any reintroduced species for success. There are two main reintroduction methods: hard and soft releases. Hard releases typically involve little more than releasing a captive-bred or translocated individual into a new habitat with no acclimation period, training, or supplemental food. Soft releases are more time-intensive and include components of acclimation to new habitats, predator control measures, supplemental feeding regimes (temporary or long-term), pre- and post-release monitoring, and for birds of prey, hacking. Hard Release Hard releases involve releasing captive-bred birds to the wild almost immediately upon arrival at the designated release site (Scott and Carpenter, 1987; Lovegrove, 1996). This release method is typically less successful, although more affordable, than soft releases (Bright, 2000; Lefty et al., 2000; Wanless et al., 2002). The survival rate for reintroduced birds is typically lower for those involved with hard releases (Waniess et al., 2002). Utilizing hard releases may be more common in reintroduction of carnivores, mammals, some translocated wild birds, and "headstarted" ectothemis (Kleiman, 1989; 171 Bright and Morris, 1994; Lovegrove, 1996; Bright, 2000; Richardson et al., 2006; Escobar et al., in press). At times, the hard release methodology is the preferred method for translocations of wild birds, where the risk of post-release failure is somewhat reduced (Lovegrove, 1996; Richardson et al., 2006). Translocations of wild birds have saved several species from extinction in New Zealand alone (Pierre, 1999). Even then, some provisions may be made for birds during this release method, such as spraying vegetation to provide drinking water for a period of time (Richardson et al., 2006). However, soft releases of captive-bred birds are strongly recommended for the best reintroduction success (Lovegrove, 1996; Wanless et al., 2002). Soft Release The primary goal of a soft release, in addition to allowing the monitoring of behaviors, stress levels, and body condition, is to gradually acclimatize animals to their new environment prior to release (Bright and Morris, 1994; Bright, 2000; Snyder et al., 1994; Lefty et al., 2000; Wanless et al., 2002; Gippoliti, 2004). Soft release involves placing pre-release individuals into large aviaries or enclosed areas in the location of eventual release (Lefty et al.., 2000). Soft release of groups (or pairs) favors development of cohesive social bonds which may persist post-release (Brown & Day, 2002; Munkwitz et al., 2005). Successful soft releases involve several components: acclimation period, predator training (see above), predator control, supplemental food program, and pre- and post-release monitoring. 172 Acclimation Birds are allowed to acclimatize to the habitat and often can view and interact with wild individuals of their own species, as well as potential predators from a safe distance (Table 18; Sanz and Grajal, 1998; White et al., 2005). Some studies have shown that individuals involved in a soft release had higher survival rates than those involved in hard releases (Wanless et al., 2002; Bright and Morris, 1994). Higher survival rates could in part be due to exposure to predators from a safer distance, thereby facilitating learning or predator recognition and avoidance (Sanz and Grajal, 1998). For example, the Yellow- shouldered Amazon Parrots were placed in large outdoor aviaries in their native habitat, which allowed them to see and hear wild parrot behavior and even experience predator pressures by a Boa constrictor snake and a Harris's Hawk (Parabuteo unicinctus, SA-1; Sanz and Grajal, 1998). While the parrots were not completely protected, such predator threats significantly assisted novice parrots in learning predator avoidance. Thus, development of species-specific behavior may require an individual's exposure to an environment normal for its species(Maxwell & Jamieson, 1997), Predator Control Predator control may be necessary in order for a reintroduction program to be successful (Priddel and Wheeler, 1994; Greene et al., 2004; Armstrong et al., 2006; Butchart et al., 2006; Smith et al., 2010). Predators may be removed from areas of threatened bird species by translocation, culling, or barriers (e.g., fences; Innes et al., 1999; Pierre, 1999; Pruitt, 2000; Greene et al., 2004; Groombridge et al., 2004; Ferreira et al., 2005; Reynolds et al., 2008; Cook et al., MO; Smith et al., 2010). Predator control 173 can be a controversial issue because of animal welfare/rights, including the welfare of threatened predator species (e.g., Hen Harrier, Circus cyaneus, SA-1; Golden Eagle, Aquila chrysaetos, SA-1; Smith et al., 2010). Predator control can benefit threatened populations by increasing hatching, fledgling success, and post-breeding population numbers (Smith et al., 2010). The effectiveness of predator control may vary for island and mainland populations; thus, each case should be evaluated on a species-by-species basis. For example, although an introduced predator (domestic at, Felis catus) was eradicated, the population of Seychelles Magpie Robins was not able to rebound (BirdLife International, 2008c). Many examples exist in the literature of extinctions or dramatic population declines of threatened species due to natural or introduced predators. As examples, the Guam Rails (Rallus owstoni, P-4) and the Micronesian Kingfisher (Halcyon cinnamomina, A) were predated by the invasive Brown Tree Snakes (Boiga irregularis; Carey, 1988); the Seychelles Magpie Robin was predated by domestic cats, Barn Owls (Tyto alba, SA-2), Common Mynas (Acridotheres tristis, A), and Brown Rats (Rattus norvegicus; BirdLife International, 2008c); and the Kakapo was subject to predation by introduced rats (Rattus exulans, R. norvegicus, R. rattus), domestic dogs (Canis familiaris), and multiple mustelids (Mustela ermine, M furo, M nivalis; Elliot et al., 2001). Several reintroduction programs have used predator control or eradication from the areas surrounding release sites to increase post-release success including those for the North Island Kokako (Callaeas cinerea wilsoni, A; Innes et al., 1999), Kaka (Greene et al., 2004), Hawaiian Honeycreeper, (Groombridge et al., 2004), New Zealand Fairy Tern 174 (Ferreira et al.., 2005), Seychelles Warbler (Acrocephalus sechellensis, A; Richardson et al., 2006), the San Clemente Loggerhead Shrike (Munkwitz et al., 2005; Farabaugh, personal communication), and the Seychelles Magpie Robin (BirdLife International, 2008c). Supplemental Feeding Providing supplemental food to released birds has become increasingly popular in soft releases. Typically, supplemental food can be provided until released individuals are able to forage on their own (Collins et al., 1998; Meretsky & Mannan, 1999; Tweed et al., 2003; Nicoll et al., 2004; White et al., 2005; Poulin et al., 2006; Reynolds et al., 2008). Supplemental feeding programs can increase site fidelity, breeding success, increase flock cohesion in some birds, and supplement wild populations at risk (Elliot et A, 2001; Greene et al., 2004; Kreger et at., 2005; Carrete et al., 2006; Oro et al., 2008; Walters et al., 2008; Deygout et al., 2009). Supplemental food can, at times, be used as a crutch in reintroductions. Several reintroduction programs utilize supplemental food when adequate resources are not present, or safe, in the wild (e.g. large birds of prey and vultures subject to lead poisoning or other contaminants: Meretsky & Mannan, 1999; Johnson et al., 2007; Oro et al., 2008; Walters et al., 2008; Saggase et al., 2009). When this happens, supplemental proffering becomes part of an expensive long-term management tool, which can preclude introduced populations from becoming self-sufficient in the wild. In addition, providing long-term supplementary feeding can alter population demographics and the normal dispersal and distribution of many species, and distract from remedying problems which 175 lead to supplemental feeding, which includes the use of poisons for pest eradication, lead bullets in territories of endangered scavengers, or medications (diclofenac) used in cattle known to harm scavengers (Green et al., 2004; Green et al., 2006; Oro et al., 2008; Walters etal., 2008; Hernandez & Margalida, 2009; Nam & Lee, 2009; Saggase et al., 2009). Finally, providing supplemental food will not help all released avian species. For example, released captive-bred Malleefowl (Leipoa ocellata, P-1) suffered poor survival, primarily from the introduced fox (Vulpes vulpes). Survival of the Malleefowl did not improve with the use of supplementary food (Priddel and Wheeler, 1994). For the reintroduction of any species to be considered successful, the ultimate reasons for their decline need to be addressed and eliminated (Temple, 1977; Kleiman, 1989; Kleiman etal., 1994; Mee & Snyder, 2007; Walters et al., 2008). Reintroductions have failed in species because the original threat was not removed (Klieman, 1989; Ebenhard, 1995). Even so, many examples exist in the literature where animals are released back into areas where the original cause for decline has not been ameliorated (Klieman, 1989; Meretsky & Mannan, 1999; Walters et al., 2008), which leads to the aforementioned long-term management and supplemental feeding programs. Monitoring Monitoring is imperative to gauge the success or failure of a reintroduction, although few programs are monitoring reintroduced populations adequately (Sarrazin and Barbault, 1996; Pierre, 1999; Greene et al., 2003; Seddon et al., 2007; Sutherland et al., 2010). In addition to locating dead birds to determine causes or mortality, close 176 monitoring can allow intervention if a bird is injured or ill. Early post-release monitoring can be used to assess the different phases of the establishment process of translocated or reintroduced individuals, as well as identify possible reasons for failure in a timely manner (Pierre, 1999; Reynolds et al., 2008). By doing this, management can become more proactive than reactive, and thus increase the chances of a successful reintroduction. Another important benefit of monitoring is to determine breeding success of released or translocated individuals (e.g., Laysan Teal, Anas laysanensis, P-2; Reynolds et al., 2008). Various monitoring techniques exist for birds, ranging from GPS tracking (e.g., Seychelles Warbler; Richardson et al., 2006) and radiotelemetry tracking (e.g., Scarlet Macaw; Myers and Vaughan, 2004), to simple mark-recapture or sighting estimates (e.g., South Island Saddleback [Philesturnus c. carunculatus] SA-2, Pierre, 1999). The method chosen for monitoring should be based on several aspects, including propensity of species to disperse far from release sites, desire to maintain distance from species (e.g., California Condor, use of GPS and radio transmitters; Hunt et al., 2007), and relative abundance of species. Monitoring is important not only for individual released birds, but also the efficacy of the reintroduction program as a whole. The ultimate objective is to collect data which will be useful as not only a gauge of success to a released population, but also for comparison with closely-related species (Sarrazin and Barbault, 1996). Hacking Some birds of prey can be released by the soft release technique of hacking (Cooper, 1983; Nicoll et al., 2003; Dzialack et al., 2006). Hacking is used when 177 individuals are released (typically at fledgling age) and provided supplemental food until the individuals achieve independence and are able to catch their own prey (Brown et al., 2006; Dzialak et al., 2006). Hacking is also a means of inducing breeding, and simulating of a home for the bird to recognize and settle in (Antkowiak and Hayes, 2004). Real predators, such as raptors, could face problems developing foraging and feeding habits after a long period in captivity (Sarrazin and Legendre, 2000). Temple (1978) compared the release of adult birds of prey to the release of juveniles by the hacking method and found that survivorship was reduced without the use of pre-release training (Sarrazan and Legendre, 2000). Peregrine Falcons, Mauritius Kestrels, Bald Eagles (Haliaeetus leucocephalus, SA-1), Ospreys (Pandion haliaetus, SA-1), Barn Owls, and Alpomado Falcons (Falco femoralis septentrionalis, SA-2) have been released in this way with success (Cade, 1980; Nicoll et al., 2003; Antkowiak and Hayes, 2004; Brown et al., 2006). In Situ versus Ex Situ Conservation Reintroduction programs benefit when cooperation exists between in situ and ex situ programs. In situ (on-site) conservation is when protection of an endangered species occurs in areas of original habitat and can include habitat protection, restoration, and predator control (Snyder et al., 1996). Ex situ (off-site) conservation is the process of protecting threatened or endangered species outside areas of natural habitat (Snyder et al., 1996). For critically endangered species, it may be necessary to maintain them ex situ while in situ conservation -efforts focus on preserving existing habitat fragments and opportunistically reconstructing artificially diverse ecosystems into which threatened 178 species can be reintroduced at a later date (Snyder et al., 1996; Kelly, 1997; Rabb and Saunders, 2005). Retaining viable populations in their native habitats is an essential conservation response for ensuring the long-term persistence of species, although such actions are frequently not sufficient on their own (Snyder et al., 1996; Willie et al., 2004). Site-based action frequently takes place by conserving existing habitat, with the aim of preventing future habitat loss and degradation, in addition to other management practices (e.g., predator control or translocation to predator-free locations, nest guarding or provision of nest boxes, and removal of competitors; Snyder et al., 1996; Curio, 1998; Baillie et al., 2004). The benefit of in situ conservation extends beyond the target species, and has the potential to improve populations of species living in the same locations (i.e., conserving entire ecosystems; Snyder et al., 1996). Although areas of protected habitat provide a valuable contribution to species conservation worldwide, the combination of varying legal statuses and management types for habitat, with many species of interest not living or staying within areas of protected habitat, makes this approach somewhat limited •(Willie et al, 2004). In many cases, habitat protection on its own is not sufficient, and direct intervention (ex situ conservation) is required to mitigate or eliminate specific threats to species (Wilson et al., 1994; Snyder et al., 1996; Willie et al., 2004; Rabb and Saunders, 2005; Snyder, 2007). Ex situ conservation (through captive breeding) can offer insurance against extinctions by providing a representative source population for future reintroductions or reinforcement of wild populations (Wilson et al., 1994; Snyder et al., 1996; Willie et al., 2004; Wisely et al., 2005; Oosterhout etal., 2007). The principal institutions which hold 179 ex situ populations of animal species for captive breeding purposes are zoos (Snyder et al., 1996; Saint Jaime, 1999). Zoos have contributed greatly in the past quarter of a century to many captive-breeding programs of endangered species through captive propagation of endangered species, research, gene banking, public awareness, and reintroduction programs (Rabb and Saunders, 2005). Other organizations involved in ex situ programs include government organizations such as the United States Fish and Wildlife Service, which created the Patuxent Wildlife Research Center in Maryland and is involved in the captive breeding of many endangered bird species. The ultimate goal of ex situ preservation programs is to maintain options for reestablishing natural populations (Snyder et al., 1996; Saint Jaime, 1999). Ideally, the ex situ period should be a transitional stage which enables the species to survive a temporary and critical situation. Another objective of ex situ programs is to provide support for education and public awareness programs (Saint Jaime, 1999). Public education and awareness can be an essential component of a reintroduction program and should not be overlooked when preparing a recovery plan (Trewhella et al., 2005). Reintroduction programs have succeeded through captive-bred animals born in zoos (e.g., the Bearded Vulture (Gypaetus barbatus, SA-1) released in the Alps; Gippoliti and Carpaneto, 1997; Gippoliti, 2004). Furthermore, zoos have a very important role in wildlife conservation through public education and awareness, research, and in situ conservation programs (Gippoliti and Catpaneto, 1997). Ideally, cooperation should exist between ex situ and in situ programs to have the best possible conservation outcome. Some restoration programs (e.g., California Condor program), involve recovery teams, including groups of individuals from the field, 180 captive-breeding specialists, and independent consultants (Walters et al., 2008). These teams make collaborative decisions on raising and releasing an endangered species for a successful reintroduction. More can be accomplished via collaborative planning and implementation with a comprehensive management plan, which often involves cooperation among many conservation organizations, zoos, and government agencies (Snyder et al., 1996; Saint Jaime, 1999; Butchart et al., 2006). The Future of Captive Breeding North American and European zoos often have the expertise and resources for successful captive breeding (Dixon, 1986; Rabb and Saunders, 2005). However, simply removing the animals from the wild without the sustained involvement of the species' native habitat can separate the process of conservation into two isolated programs: one for the wild population and the other for the population in captivity (Dixon, 19-86). Facilities which hold endangered species should not only consider what the optimal breeding conditions might be for animal, but should work in cooperation with other breeding centers and with the countries of origin to ensure that the wild populations will be able to survive through protective measures or carefully executed reintroduction projects (Luthin et al., 1986; Rabb and Saunders, 2005). Without this duality, a captive- breeding and reintroduction program may fail (Dixon, 1986). Ideally, reintroductions should be implemented when two conditions are satisfied: when adequate areas of unoccupied former habitat (or equivalent habitat) remain, and significant mitigation of the cause for decline (Klieman, 1989; Saint Jaime, 1999; Baillie 181 et al., 2004). Without these two conditions being met, reintroduction programs could be doomed to indefinite over-management or failure. For example, although sufficient habitat remains on Guam to allow the reintroduction of the Guam Rail into its native habitat, it will always require protection due to the continued presence of the introduced Brown Tree Snake (Klieman, 1989; Baillie et al., 2004). Sadly, since 1994, the Guam Rail has been extinct in the wild due the inability to reduce predation by invasive Brown Tree Snakes (BirdLife International, 2008(1). Likewise, California Condors, although released into areas of adequate habitat, still face the significant problem of lead poisoning by ingesting fragments of lead bullets (Church et al., 2006; Walters -et al., 2008). Recent research has concluded that lead ingested from deer shot and left by hunters is a significant cause of condor mortality in the wild (Church et al., 2006). Therefore, condors are provided supplemental clean food at all release sites as well as extensive blood tests on periodically recaptured birds to test for dangerous levels of lead (Parish et al., 2007; Walters et al., 2008). If birds are found to have high levels of lead, they must undergo arduous chelation therapy treatments before being released again, and sometimes return to the same areas where they ingested the lead and become re-poisoned (Meretsky & Mannan, 1999; Redig et al., 2003; Hall, 2007; Parish et al., 2007). Until a ban on lead shot within condor ranges is implemented, the over-management of this critically endangered bird will continue and the condor reintroduction program will not be considered successful or self-sustaining (Snyder, 2007; Walters et al., 2008). 182 Defining Success How can we define success in captive breeding and reintroduction of birds? In many programs, the standards of success have not been clearly defined (e.g., Campbell Island Teal {Anas nesiotis} P-2, Seddon and Maloney, 2003; California Condor, Utt et al., 2008) Sutherland et al. (2010) suggested several steps to standardize reintroductions for optimal success, including: 1) documenting reintroduction plans before release; 2) delineating objectives of release and monitoring plans; 3) documenting plans for publishing results of reintroduction monitoring; 4) standardizing release methodologies and documentation; 5) monitoring population at standardized intervals (i.e., 30-60 days post-release, 1 yr, 5 yr, 10 yrs, etc.); 6) estimating population size (e.g., mark/recapture and distance sampling); 7) determining age class and sex; 8) identifying causes of mortality in reintroduced individuals; and 9) publishing results (Innes et al., 1999). Following a standardized scientific approach can allow reintroduction specialists the ability to better gauge success of specific breeding and release methodologies and thus adapt management techniques in a timely manner and prevent "management lore" •(i.e., management techniques based on assumptions with little or no benefit to the reintroduced species; Innes et al., 1999; Wilhere, 2002; McCleery et al., 2007; Seddon et al., 2007). In addition to the guidelines suggested by Sutherland et al. (2010), it is also important to determine standards pertaining to reproductive success of released birds. A benchmark of a successful reintroduction program is one that has reintroduced species not only surviving to adulthood, but also breeding in the wild, producing fertile eggs, and rearing young to fledgling/adulthood. Survival of reintroduced birds is essentially 183 irrelevant if they are not able to successfully reproduce in the wild. Unfortunately, few reintroduction programs have the resources (e.g., adequate funding) necessary to follow reintroduced populations for an extended period of time. The lack of appropriate funding leads to the primary problems in avian reintroduction programs and can ultimately determine their success of failure (Wilhere, 2002). The ultimate measure of reintroduction success is that of the establishment of a self-sustaining wild population, and very few programs have met this standard (Scott and Carpenter, 1987; Walters et al., 2008; Sutherland et al., 2010). Conclusions With rapid human population growth and land development, reintroduction goals cannot be realistically met without the cooperation of land owners, governments, and breeding facilities (Sutherland, 1998; Saint Jaime, 1999). Unfortunately, captive breeding and reintroduction programs have only been able to benefit a small proportion of all species threatened with extinction at this time (Saint Jaime, 1999; Baillie et al., 2004). There are many reasons why a relatively small number of endangered species are being assisted, including adequate space for captive-breeding, time intensive reintroductions and monitoring, foreign government politics, suitable habitat availability, elimination of the original cause(s) of decline, and the cost of running a program which could last for decades (e.g., Guam Rail, California Condor, Hawaii forest bird restoration program, Peregrine Falcon; Kleiman, 1989; Bailie et al., 2004; Church et al., 2006). These issues further necessitate the urgent needs to be proactive about protecting vulnerable habitat and further behavioral research in conservation (Kleiman, 1989; Sutherland, 1998). 184 Without the proper knowledge of a species' behavior, natural history, and habitat requirements, protecting, breeding, and reintroducing threatened species will prove extremely difficult and expensive, time-intensive, and may ultimately lead to failure. Acknowledgments I would like to thank Dr. William Hayes, Dr. Nancy Harvey, Dr. Steven Dunbar, Dr. Floyd Hayes, and Dr. Ronald Carter for their critical reviews and comments on earlier versions of this manuscript. Loma Linda University's Department of Earth & Biological Sciences funded and provided funding and access and to a large body of published material, while Farzaneh Alemozaffar from the Loma Linda University library assisted this review by finding almost every obscure literature request imaginable. 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(1994) Captive-breeding and reintroduction project for the Milky Stork, Mycteria cinerea, at the Zoo Negara, Malaysia. International Zoo Yearbook. 33:39-48. 207 CHAPTER FIVE GENERAL CONCLUSIONS In the first study (Chapter 2), Behavioral analyses of captive-reared juvenile California Condors indicated the presence of measurable differences between varying rearing methodologies. This study was the first to be able to quantify such differences. Implications of puppet-reared California Condors exhibiting fewer social interactions compared with their parent-reared counterparts are profound. California Condors are a highly social species, and integrating into a social hierarchy is imperative for certain skills necessary for success living in the wild (i.e. mate selection, reproduction, competing at carcass for food). Results also indicate the establishment of a linear dominance hierarchy among juveniles and adult mentors (Utt et al., 2008). Although rearing method did not influence dominance in this study, it is still possible that a condor which exhibits long-term social deficiencies could also experience lower dominance status. The study in Chapter 2 is further significant to the scientific community because it represented the first published attempt to measure behavioral differences between rearing methods in captive-reared California Condor. This analysis was particularly relevant because of the bias towards puppet-reared birds. I was able to show that regardless of rearing type, these birds were able to integrate into a social group (i.e., dominance hierarchy analysis) and compete well with conspecifics. In order to improve any captive- 208 breeding and reintroduction program, research and intermittent progress evaluations must be undertaken. The second study (Chapter 3) comprised the most extensive analysis to date of efficacy of the California Condor Reintroduction Program. Such analyses are important to adaptive management techniques and are essential if a program is to evolve to better fit the needs of its particular species. Behavioral problems have decreased significantly since the beginning of the captive-breeding and reintroduction program; however, the effect of conspecific mentoring on the California Condor remains debatable (Chapter 3). We may conclude that mentoring may be more effective in behavior training for other avian species. In addition, mentoring may be more effective at mitigating undesirable behaviors in captive- reared California Condors if implemented around the sensitive imprinting periods for this species, if it occurred in appropriate social groupings, and if mentors were released with their juvenile mentees into the wild. Timing the mentoring appropriately would depend on the detailed knowledge of the species life history, developmental mode, and sociality (Tables 13, 14, 16, 17). Mentoring California Condor juveniles currently involves placing fledged juveniles in small groups (2-4 juveniles) with an adult mentor. This grouping is not typical of parent-rearing in the wild (2 adults, 1 juvenile). Understandably, space is at a premium at rearing facilities, so less-than-ideal group sizes are implemented. In addition, mentors are not released with their juvenile cohorts, which could prove beneficial to post-release behavior and survival. Finally, the efficacy of mentoring could be decreased by inclusion of captive-bred, puppet-reared condors as mentors, of which many were recaptured from the wild for behavior problems (NCH, unpublished data). 209 However, there are undoubtedly many behaviors not measured in our study that could be important in developing appropriate California Condor behaviors. Further studies on mentoring could prove useful, especially if the species life history was considered and implemented (Chapter 4). The difference between rearing facilities (with more birds exhibiting behavior problems being reared at the San Diego Zoo's Wild Animal Park) was unexpected. Further studies examining the differences between rearing facilities should be undertaken. In addition, any analysis of the California Condor Recovery Program would be incomplete without the cooperation of all breeding facilities. Thus, for example, the Peregrine Fund would need to participate in this type of research to further our understanding of the efficacy of the program as a whole. Implementing a successful avian captive-breeding and reintroduction program requires many important elements, including a detailed knowledge of the species life history, developmental mode, sociality, habitat use, behaviors, and breeding preferences. Unfortunately, many programs, like the California Condor program, were implemented as a "last ditch" effort to save a species; thus, with an emphasis on increasing population size as quickly as possible, little research and planning may have been executed. When this happens, a captive-breeding or reintroduction program will have to learn and adapt management techniques by trial and error, which impedes the efficacy of the program. Ideally, reintroduction programs should be treated as a well-designed experiment (McCleery et al., 2007; Sutherland et al., 2010). Cooperation should always exist between in situ (e.g., habitat conservation, etc.) and ex situ (e.g., captive-breeding) conservation efforts on behalf of a given species. 210 Essential to cooperation is the sharing of information, data, and analysis. Results should be published even if they are negative or lacking statistical significance. Defining the success of a reintroduction program is essential. Post-release monitoring, both in the short- and long-term, are essential in this process. Future Considerations and Implications The California Condor recovery program not only struggles with problems of maladaptive behavior in the wild, but also controlling the major contributing factor affecting survival in the wild: lead poisoning (Fisher et al., 2006; Mee & Snyder, 2007). Reintroductions have failed in other species because the original threat was not removed (Ebenhard, 1995; Meretsky et al., 2000). For the reintroduction of the California Condor (or any species) to be considered successful, the ultimate reasons for their decline need to be addressed and eliminated (Temple, 1977; Kleiman, 1989; Klieman et al., 1994; Meretsky & Mannan, 1999; Mee & Snyder, 2007; Walters et al., 2008). Lead poisoning was the leading cause of mortality in California Condors in the 1980s (Grantham, 2007). But unfortunately, lead (from spent lead ammunition) has neither been eliminated nor effectively controlled (Meretsky et al., 2000; Mee & Snyder, 2007). Spent lead ammunition is the main, if not exclusive source of lead that California Condors ingest in the wild (Fisher, 2006; McKeever, 2006; Pattee et al., 2006; Cade, 2007). Because condors are scavengers, they acquire lead at a higher rate than many other avian species (Houston, 1996; Snyder, 2007; Pain et al., 2009). Other vulture or raptor species have been known, or suspected, to acquire lead at toxic levels (Turkey Vulture [Cathartes aura] Wiemeyer et al., 1986; Kirk et al., 1998; Black 211 Vultures [Coragyps atratus] Buckley, 1999; Steller's Sea Eagle [Haliaeetus pelagicus] and White-tailed Sea Eagle [H. albicilla] Iwata et al., 2000; Bald Eagle [H. leucocephal] and Golden Eagle [Aquila chrysaetos] Johnson et al., 2007; Argentine Solitary Crowned Eagle [Harpyhaliaetus coronatus], and the Andean Condor [Vultur gryphus] Saggese et al., 2009). Susceptibility to lead poisoning is more dangerous to long-lived species (i.e., K-selected species; Wallace, 1994; Fisher et al., 2006). Thus, many condors die due to the chronic exposure to lead they obtained from the environment. From 1992-2005, three California Condors have died of lead poisoning, while 15 others have died or disappeared in the wild (Grantham, 2007). Several condor specialists suspect that many of the missing condors also died from lead poisoning but were not recovered (Grantham, 2007; Snyder, 2007). Countless others have had to be recaptured and administered chelation therapy, or sometimes even surgery to remove lead (Hunt et al., 2007; Parish et al., 2007). Chelation therapy requires injections of calcium versenate (CaEDTA) twice a day until blood levels reach near-normal levels (Redig et al., 2003; Parish et al., 2007; Sullivan et al., 2007). Trapping sick birds and treating with chelation therapy is not a permanent solution for lead poisoning. In fact, several birds have been treated as many as six times for increased lead levels (Parish et al., 2007), not to mention the added stress of multiple captures and increased exposure and possible desensitization to humans (Meretsky and Mannan, 1999). Repeat poisonings indicate the propensity for scavengers to return to the same foraging grounds where they have fed upon tainted meat in the past, even though proffered clean carcasses are available. Thomas Cade (and others) suggests that although some hunters are voluntarily using non-toxic lead, it may be necessary for the Environment Protection Agency (EPA) to step in to administer 212 controls on lead-based ammunition, just as they did with the pesticide DDT (dichloro- diphenyl-trichloroethane) over 35 years ago (McKeever, 2006; Cade, 2007; Hunt et al., 2007; Mee & Snyder, 2007). Methods to combat further lead poisonings include public education, focus groups, surveys, researching the danger of lead-shot in food killed for human consumption, and requests for volunteer use of non-lead ammunition (Cade, 2007; Mee & Snyder, 2007; Sullivan et al., 2007). Supplying lead-free food will not prevent scavengers from following their natural instincts to forage. Eventually they will feed on tainted carrion (Meretsky & Mannan, 1999; Mee & Snyder, 2007; Walters et al., 2008). It would be beyond comprehension that a recovery program would release animals to the wild without ensuring that the original cause for decline were mitigated or removed. In fact, without the insensitive hands-on management of the California Condor, failure to establish self-sustaining populations, and ultimately, extinction in the wild, would be the most likely outcome (Cade, 2007; Walters et al., 2008). The implication for captive-breeding and reintroduction programs is that they must include habitat conservation, political advocates, land managers, and land owners (Toone & Wallace, 1994). A new problem affecting the reproductive success of reintroduced California Condors is "microtrash" (Snyder and Snyder, 2000; Grantham, 2007). The pervasiveness of pollution (trash) has affected successful breeding in the wild, with parents bringing items such as rags, bolts, washers, nuts, plastic, glass, and copper wire to their nests (Snyder and Snyder, 2000). California Condors are naturally curious birds, and often they will pick up small objects, manipulate them, and ingest them. In fact, this propensity to 213 pick up small objects, including trash, is not unique to California Condors. Trash ingestion appears to be wide spread among other old and new vultures (Grantham, 2007). Historically, California Condors pick up, manipulate, and ingest bone fragments near carcasses, presumably to fulfill dietary calcium requirements and aid in digestion (Grantham, 2007). It is unknown if picking up trash instead of bone fragments is an unconscious mistake or a deliberate behavior. Condors are taking small pieces of trash back to their nests where chicks ingest them. Almost every wild-hatched chick has been exposed to microtrash, with several suffering direct mortality due to the ingestion of trash (Mee et al., 2007; Mee and Snyder, 2007). Through 2007, microtrash ingestion by chicks has been the primary cause of next failures in Southern California (Grantham, 2007; Mee et al., 2007). Bone fragments have been proffered with carcasses, but because of the propensity for the California Condor to forage over large areas, controlling trash ingestion has not been very successful. The California Condor Recovery Program has been successful on several fronts, including the propagation of Condors in captivity, preserving at least four genetic haplotypes, reintroduction of captive-bred birds at several release sites, and more recently, successful rearing of chicks in the wild (Adams and Villablanca, 2007). However, no program is perfect, and to better serve the California Condor, I have several proposed ideas which could assist the recovery team with their goals. 1. All rearing facilities must have open lines of communication and participate collectively in research (ideally involving external input, such as academic; Mee and Snyder, 2007). 214 2. Each rearing facility and release site should make efforts to standardize rearing techniques, housing protocols, pre- and post-release training, mentoring, clear definitions of behavior problems (with outline of how to deal with behavior issues in the wild), and a clear definition of "success" (which would require extensive post-release monitoring). 3. Suspend releasing captive-bred California Condors until the lead poisoning issue has been resolved (although potential benefits of reducing condor mortality in the wild should be weighed with potential for increased adaptation to captivity). 4. Mentor pre-fledgling juvenile California Condors in more realistic groups in rearing facilities (i.e., one or two adult mentors and one juvenile). Larger groupings can be beneficial for establishing group cohesion while being held at the release site. 5. Release suitable adult mentors with juvenile cohorts to continue the mentoring process in the wild and strengthen group cohesiveness. 6. Cease use of adult mentors which have never lived in the wild and/or were not parent-reared by wild-born condors, as the potential learning benefits from a captive bird as compared with an experienced bird can be expected to be diminished. 7. Undertake a more current and rigorous analysis of the California Condor • program to determine if any new trends have surfaced, or if past concerns are no longer relevant (McCieery et al., 2007). 215 8. 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First symposium on Steller's and White-tailed Sea Eagles in East Asia. Johnson CK, Vodovoz T, Boyce MW, Mazet MK. (2007) Lead exposure in California Condors and other Sentinel species in California. Wildlife Health Center. University of California Davis. 34p. 217 Kirk, David A. and Michael J. Mossman. (1998) Turkey Vulture (Cathartes aura), The Birds of North America Online. Poole A, Ed. Ithaca: Cornell Lab of Ornithology; Retrieved from the Birds of North America Online: http://bna.birds.come1l.edu/bna/species/339. doi:10.2173/bna.339 Kleiman DG. (1989) Reintroduction of captive mammals for conservation: guidelines for reintroducing endangered species into the wild. BioScience. 39(3):152-161. Klieman DG. (1994) Animal behavior studies and zoo propagation programs. Zoo Biology. 13:411-412. Kleiman DG, Reading RP, Miller, RI, Clark TW, Scott JIVI, Robinson J, Wallace RI, Cabin RJ, Felleman F. (2000) Improving the evaluation of conservation programs. Conservation Biology. 14(2):356-365. Mc°eery RA, Lopez RR, Siivy NJ. (2007) Transferring research to endangered species Management. Journal of Wildlife Management. 71(7):2134-2141. McKeever, Michael. (2006) Champion for birds of prey: Dr. Thomas Cade. Zoo Nooz. Zoological Society of San Diego. IXXIX(12):21. Mee A, Hamber JA, Sinclair J. (2007) Low nest success in a reintroduced population of California Condors. P 163-184. In Mee A & Hall LS, editors. California Condors in the 21st Century. Lancaster: Cadmus Communications. 296 p. Mee A, Snyder NFR. (2007) California Condors in the 21st century — conservation problems and solutions. P 243-279. In Mee A & Hall LS, editors. California Condors in the 21st Century. Lancaster: Cadmus Communications. 296 p. Meretsky VJ, Mannan RW. (1999) Supplemental feeding regimes for Egyptian vultures in the Negev Desert, Israel. Journal of Wildlife Management. 63(1):107-115. Meretsky VJ, Snyder NFR, Beissinger SR, Clendenen DA, Wiley JW. (2000) Demography of the California Condor: implications for reestablishment. Conservation Biology.14: 957-67. Pain D J, Fisher IJ, Thomas VG. (2009) A global update of lead poisoning in terrestrial birds from ammunition sources. P 99-118. In R. T. Watson, M. Fuller, M. Pokras, and W. G. Hunt, eds. Ingestion of Lead frorn Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho, USA. DOI 10.4080/ilsa.2009.0108 Parish CN, Heinrich WR, Hunt WG. (2007) Lead exposure, diagnosis, and treatment in California Condors released in Arizona. P 79-96 In Mee A & Hall LS, editors. California Condors in the 21st Century. Lancaster: Cadmus Communications. 296 p. 218 Pattee OH, Carpenter JW, Fritts SH, Rattner BA, Wiemeyer SN, Royal JA, Smith MR.. (2006) Lead poisoning in captive Andean Condors (Vultur gryphus). Journal of Wildlife Diseases. 42(4):772-229. Redig P, Artz N, Byrne R, Heinrich B, Gill F, Grantham .1, Jurek R, Lamson S, Palmer B, Patterson R, Sanborn W, Seymour S, Sieg R, Wallace M. (2003) A report from the California Condor lead exposure reduction steering committee a subcommittee of the California Condor recovery team. Saggase MG, Quaglia A, Lambertucci SA, Bo MS, Sarasota JH, Pereyra-Lobos R, Maceda JJ. (2009) Survey of lead toxicosis in free-ranging raptors from central Argentina. P 223-231. In Watson RT, Fuller M, Pokras M, and Hunt WG (eds.). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho. USA. 394 p. Seddon PJ, Armstrong DP, Maloney RF. (2007). Developing the science of reintroduction biology. Conservation Biology. 21(4303-312. Snyder N, Snyder H. (2000) The California Condor: A Saga of Natural History and Conservation. Academic Press. San Diego. 410 p. Snyder NFR. (2007) Limiting factors for wild California Condors. P 9-34. In Mee A & Hall LS, editors. California Condors in the 21st Century. Lancaster: Cadmus Communications. 296 ID. Sullivan K, Sieg R, Parish C. (2007) Arizona's efforts to reduce lead exposure in California Condors. P 109-121. In Mee A & Hall LS, editors. California Condors in the 21st Century. Lancaster: Cadmus Communications. 296 p. Sutherland WJ, Armstrong D, Butchart SHM, Earnhardt EVI, Ewen J, Jamieson I, Jones CG, Lee R, Newbery P, Nichols JD, Parker KA, Sarrazin F, Seddon P, Shah N, Tatayah V. (2010) Standards for documenting and monitoring bird reintroduction projects. Conservation Letters. Accepted Article; doi: 10.1111/.0755- 263X.2010.00113.x Temple, SA. (1977) Reintroducing birds of prey to the wild. P 355-363. In SA Temple, ed. Endangered birds, management techniques for preserving threatened species. University of Wisconsin Press. Madison. 466 p. Toone WD, Wallace MP. (1994) The Extinction in the Wild and Reintroduction of the California Condor (Gymnogyps californianus). P 411-419. In Olney PJS, Mace GM, Feistner ATC, eds. Creative Conservation: Interactive Management of Wild and Captive Animals. Chapman & Hall. London. 517 p. 219 Utt AC, Harvey NC, Hayes WK, Carter RL. (2008) The effects of rearing method on social behaviors of mentored, captive-reared juvenile California Condors. Zoo Biology. 27:1-18. Wallace MP. (1994) Control of behavioral development in the context of reintroduction programs for birds. Zoo Biology. 13:491-499. Walters JR, Derrickson SR, Fry DM, Haig SM, Marzluff .1.11/1, Wunderle JM, Jr. (2008) Status of the California Condor and efforts to achieve its recovery. The American Ornithologists Union and Audubon California. 59 p. Wiemeyer SN, Jurek RM, Moore JF. (1986) Environmental contaminants in surrogates, food, and feathers of California Condors (Gymnogyps californianus). Environmental Monitoring and Assessment. 6(1):91-111. 220 APPENDIX A DATA SUMMATION 221 Data Summarization Sample of data record sheet used in behavioral observation study (Chapter 2). Date: Bird ID: Start Time: End Time: Page Behaviors/Interval 1 2 3 4 5 6 7 8 9 10 Seeks/Becomes/Is Proximate to Other(s) Is Sought/Becomes/Is Proximate by Other(s) Leaves Other(s) Is Left by Other(s) Near to Other(s) Distant from Other(s) Preens Other(s) Is Preened by Other(s) , Displaces/Is Avoided by Other(s) •Is Displaced or Avoids Other(s) Pull Feather, Nibbles, Nudge Other(s) Revs Feather Pull, Nibble, Nudge from Other(s) Non Contact Aggress Other(s) Revs Non Contact Aggress from Other(s) Contact Aggress Other(s) Revs Contact Aggress from Other(s) Feeds First Feeds with Other(s) Feeds Alone (no one Proximate or Near) Focal Bird Not Visible Comments: 222 Sample of data recorded on a data record sheet (Chapter 2). Date: *-") 10 Bird ID la-Sr? Start Time: 10 44141, End Time: W,P-0." Page f Behaviors/ Interval Seeks/Becomes or is Proximate to Other(s) Is sought/becomes or is i-V9 proximate by other Leaves other (s) I ttl0 Is left by other (s) sommasanii mir.-Numium Near to others P t40 Distant from others 2e& 7.45b 9-560 7.10-0 2..V14 2,81,0 lit-to 1440 140 I, c, 1440 Preens Other Is Preened by Other Displaces/Or is Avoided b Others Is Displaced or LAO IMP Avoids Other Pull Feather, Nibbles, Itt) Nudge Other Revs Feather Pull, 1140 Nibble, Nudge from Other Non Contact Aggress Other Revs Non Contact Aggress from Other Contact Aggress Other Revs Contact Aggress From Other. Feeds First Feeds with Others Feeds Alone (No one in proximity or near) Focal Bird Not Visible Comments: 223 Sample of daily data summary taken from an Excel spreadsheet (2003). Each summary sheet is for one behavior and its designated focal bird. Thus, for each focal bird in my study, there are 20 summary sheets. Once the observational season is complete, data are converted from a 20- minute observational period to units of an hour (60 minutes). Then, averages are found for each focal bird and each behavior. Date Seek 63 Seek 265 Seek 266 Seek 270 Seek 278 Seek 286 4/18 0 0 6 0 13 0 4/20 0 0 0 10 0 0 5/13 0 9 0 0 0 0 5/14 0 20 0 0 0 0 5/16 0 0 20 0 20 20 5/18 0 6 0 0 0 0 6/2 4 ii 0 0 0 3 6/3 8 0 0 0 0 0 6/4 0 20 0 0 0 0 6/26 0 0 0 18 5 0 6/27 1 1 0 4 1 0 6/29 0 0 0 0 20 20 7/15 0 0 15 1 0 2 7/16 7 0 10 4 12 13 7/17 0 0 13 0 0 20 8/5 20 0 0 20 0 5 8/6 16 20 20 0 19 0 8/7 2 0 0 0 16 0 8/25 0 0 20 0 10 0 8/26 0 0 0 0 0 0 8/27 0 0 20 0 0 0 8/28 0 11 9 11 9 12 9/17 1 1 1 1 2 0 9/18 0 7 0 7 0 0 9/19 0 0 20 20 0 0 224 Sample of converted and averaged data (Chapter 2). Date Seek 63 Seek 265 Seek 266 Seek 270 Seek 278 Seek 286 4/18 0.00 0.00 18.02 0.00 39.04 0.00 4/20 0.00 0.00 0.00 30.03 0.00 0.00 5/13 0.00 27.03 0.00 0.00 0.00 0.00 5/14 0.00 60.06 0.00 0.00 0.00 0.00 5/16 0.00 0.00 60.06 0.00 60.06 60.06 5/18 0.00 18.02 0.00 0.00 0.00 0.00 6/2 12.01 33.03 0.00 0.00 0.00 9.01 6/3 24.02 0.00 0.00 0.00 0.00 0.00 6/4 0.00 60.06 0.00 0.00 0.00 0.00 6/26 0.00 0.00 0.00 54.05 15.02 0.00 6/27 3.00 3.00 0.00 12.01 3.00 0.00 6/29 0.00 0.00 0.00 0.00 60.06 60.06 7/15 0.00 0.00 45.05 3.00 0.00 6.01 7/16 21.02 0.00 30.03 12.01 36.04 39.04 7/17 0.00 0.00 39.04 0.00 0.00 60.06 8/5 60.06 0.00 0.00 60.06 0.00 15.02 8/6 48.05 60.06 60.06 0.00 57.06 0.00 8/7 6.01 0.00 0.00 0.00 48.05 0.00 8/25 0.00 0.00 60.06 0.00 30.03 0.00 8/26 0.00 0.00 0.00 0.00 0.00 0.00 8/27 0.00 0.00 60.06 0.00 0.00 0.00 8/28 0.00 33.03 27.03 33.03 27.03 36.04 9/17 3.00 3.00 3.00 3.00 6.01 0.00 9/18 0.00 21.02 0.00 21.02 0.00 0.00 9/19 0.00 0.00 60.06 60.06 0.00 0.00 E Scores 177.18 318.32 462.46 288.29 381.38 285.29 Mean 7.087 12.73 18.50 11.53 15.26 11.41 St. Dev 15.65 20.88 25.00 19.95 22.07 21.15 Var. 244.90 436.08 625.00 398.05 486.91 447.14 1 Means 76.52 225 APPENDIX B SUBJECT OBSERVATION ORDER Season 1 2003 San Diego Wild Animal Park Date Time Order of Observations 02/19/03 *13:44 286 140, 287, 264, 265, 141, 266, 270, 278, 138 02/21/03 9:37 266 264, 265 141, 270, 278, 138 287, 140, 286 02/26/03 14:31 270 138, 278 287, 140 286, 265 141, 266, 264. 02/28/03 9:10 287 286, 140 265, 266 264, 141 138, 278, 270, 266 264 03/02/03 13:39 270 138, 278 264, 265 266, 141 286, 140, 287 03/03/03 9:07 141 266, 264 265, 140 286, 287 138, 278,270 03/05/03 10:54 264 266, 141 265, 278 138, 270 286, 287, 140 03/07/03 9:00 278 270, 138 140, 286 287 266 265, 264, 141 03/12/03 13:21 140 287, 286 264, 141 265 266 270, 138, 278 03/14/03 11:58 140 286, 287 141, 264 265 266 138, 270, 278 03/16/03 13:09 278 270 138 286, 287 140 265 141, 266, 264 03/17/03 9:26 264 265 266 141, 278 270 138 286, 287, 140 03/19/03 9:29 138 278 270 286, 287 140,264, 266, 141, 265 03/23/03 12:23 278 270 138 286, 287 140 141 264, 265, 266 03/24/03 9:35 265 266 264 141, 138 270 278 286, 140, 287 03/25/03 10:36 287 140 286 270, 138 278 141 266, 265, 264 03/26/03 10:54 140 286 287 141, 264 265, 266, 138, 270, 278 03/27/03 8:07 287 286 140 278, 270 138 266 265, 264, 141 04/01/03 8:22 265 264 266 141, 286 287 140 270, 138, 278 04/03/03 10:00 286 140 287 138, 270 278 141 266, 264, 265 04/04/03 8:40 140 287 286 264, 266, 141 265 270, 278, 138 04/06/03 11:18 278 138 270 141, 264, 265 266 286, 287, 140 04/09/03 13:59 270 278, 138 141, 264, 265 266 286, 287, 140 04/11/03 9:06 270 138, 278 287, 286, 140, 266, 265, 264, 141 226 Ventana Wilderness Area Date Time Order of Observations (270, 278, 286*) 63, 265, 266, 04/20/03 09:20 270, 278, 286, 287 05/13/03 10:00 63, 265, 286, 278, 287, 270, 266 05/14/03 07:00 63, 265, 286, 278, 287, 270, 266 05/16/03 16:00 63, 265, 286, 278, 287, 270, 266 05/18/03 13:00 63, 265, 286, 278, 287, 270, 266 06/02/03 14:40 265, 286, 278, 287, 270, 266, 63 06/03/03 13:45 265, 286, 278, 287, 270, 266, 63 06/04/03 12:20 265, 286, 278, 287, 270, 266, 63 06/27/03 16:00 286, 278, 287, 270, 266, 63, 265 06/28/03 07:00 286, 278 287, 270, 266, 63, 265 06/30/03 10:00 286 278 287, 270, 266, 63, 265 07/16/03 07:00 278 287 270, 266, 63, 265, 286 07/17/03 10:00 278 287 270, 266, 63, 265, 286 07/18/03 07:00** 278 287 270, 266, 63, 265, 286 08/05/03 16:00 287 270 266, 63, 265, 286, 278 08/06/03 13:00 287 270 266, 63, 265, 286, 278 08/07/03 06:00 287 270 266, 63, 265, 286, 278 08/25/03 16:00 270 266 63, 265, 286, 278, 287 08/26/03 10:00 270 266 63, 265, 286, 278, 287 08/27/03 13:00 270 266 63, 265, 286, 278, 287 08/28/03 07:00 270 266, 63, 265, 286, 278, 287 Pinnacles National Monument Date Time Order of Observations 09/17/03 10:30* 266, 63, 265, 286, 278, 287, 270 09/18/03 09:15 266, 63, 265, 286, 278, 287, 270 09/19/03 10:27 266, 63, 265, 286, 278, 287, 270 227 Season 2 - 2004 San Diego Wild Animal Park Date Time Order of Observations 11/11/03 12:00 141, 294, 298, 303, 311 11/13/03 11:50 Apollo, 301, Athena 11/18/03 10:50 301, Athena, Apollo; 294, 298, 303, 311 141 11/20/03 10:53 Athena, Apollo, 301; 298, 303, 311, 141 294 11/25/03 10:56 Apollo, 301, Athena; 303, 311, 141, 294 298 12/2/03 10:40 301, Athena, Apollo; 311, 141, 294, 298 303 12/3/03 9:40 Athena, Apollo, 301; 141, 294, 298, 303 311, 301 12/4/03 10:40 Apollo, 301, Athena, 141, 294, 298, 303, 311, 301 12/8/03 8:50 294, 298, 303, 311, 141; 301, Athena, Apollo Hopper Mountain Wildlife Refuge Complex Date Time Order of Observations 01/06/04 13:00 36, 294, 298, 301, 303, 311 01/07/04 11:00 294 298, 301, 303, 311, 36 01/08/04 09:00 298 301, 303, 311, 36, 294 01/09/04 07:45 301 303, 311, 36, 294, 298 01/20/04 13:45 303 311, 36, 294, 298, 301 01/21/04 11:15 311 36, 294, 298, 301, 303 01/22/04 09:15 36, 294, 298, 301, 303, 311 02/04/04 11:15 294 298, 301, 303, 311, 36 02/05/04 09:00* 298 301, 303, 311, 36, 294 02/20/04 09:55** 301 303, 311, 36, 294, 298 03/03/04 10:20** 303 311, 36, 294, 298, 301 03/04/04 14:00 311 36, 294, 298, 301, 303 03/05/04 07:40 36, 294, 298, 301, 303, 311 03/17/04 15:50 294 298, 301, 303, 311, 36 03/18/04 09:00*** 303 311, 36, 294, 298, 301 04/01/04 09:20 298 301, 303, 311, 36, 294 04/05/04 13:10 301 303, 311, 36, 294, 298 04/14/04 14:30 303 311, 36, 294, 298, 301 04/15/04 11:40 311 36, 294, 298, 301, 303 04/16/04 09:30 36, 294, 298, 301, 303, 311 04/28/04 17:00 36, 294, 298, 301, 303, 311 04/29/04 08:08 294, 298, 301, 303, 311, 36 228 APPENDIX C RESEARCH PERMITS 229 Permit to collect observational data at Pinnacles National Monument. September, 2004. (Chapter 2) Studyti: PINN-00304 Permit#: PINN-2003-SCI-0004 Start Date: Sep-41-2003 Expiation Date: Sep-30-2004 • Coop Agreement#: nia Optional Park Code: nia Name of principal investigator: . , Name: Ms Amy Utt Phone: (909) 289-7774 Email: naniregirl78gjuno.com Name of institution represented: Loma Linda University .. Co-Irivestigatinii Name: Dr. Ronald Carter Phone: (909) 588-4300 ext. Email: [email protected] , 48905 Name: Dr. Nancy C. Harvey Phone: (619) 557-3956 Email: [email protected] Project title: ADULT MENTORING OF CAPTIVE-REARED CALIFORNIA CONDOR FLEDGLINGS, Gymnogyps californianus, SCHEDULED FOR RELEASE INTO THE WILD Purpose of study: Proposed Investigation: , • . The purpose of this study is evaluate -whether adult mentoring of captive-reared California condor fledglings will affect their success or failure after release in the wild. The' California 'Condor: a comehattstory. The fate of North America s rarest native bird grew much dimmer in *1987 when the last remaining condors were captured and removed from the wild. From 27 surviving birds in 1987, the population has grown to 196 individuals currently, of which 78 are now living in the wild. Unfortunate.ly, none of the wild birds have successfully raised young. The majority of released birds were puppet reared in captivity (to increase offspring survival), but many exhibited maladaptive behaviors (e.g., visiting human structures, antisocial behavior). ' Consequently, more emphasis was ,placed.on.parent-yeared birds and their release in the wild. Present data suggest that i parent-reared birds behave more normally than puppet-reared birds. Can puppet-reared condors be equally successful? A 'mentor rig program was recently instated to better prepare young captive-bred condors for introduction to the wild. Mentoring ad&essed the possibility.that puppet-reared condors • - exposed to adult condors would more likely develop the social skills necessary to survive and reproduce in the wild. For a period of time prior to release, several juvenile condors are housed together with an adult. .. I wish to achieve three objectives: To document and compare behaviors of parent-mised and puppet-raised mentored fledglings observed at the San Diego Wild Animal Park and in holding pens prior to release in the Ventana Wilderness Area. To correlate behavioral data during the mentoring period with field data on the success or failure of released condors. \ PemtPINN-2003-SCI-0004 - Page I of 2 230 To compare behavior outcomes of mentored fledglings that experienced varying durations of mentoring using pooled data from condor breeding facilities. I hypothesize that mentoring will help mediate differences between parent-reared and puppet-reared condors, such that both will have similar success upon release. Success will be measured as the percent of released fledglings that are not recaptured for behavioral problems during the 9-12 months after initial release. This study will be significant for several reasons. It will be the first attempt to develop an ethogram and scoring system to quantify the behaviors of nientored birds. Quantitative analyses may permit problem birds to be recognized and worked with prior to release. The ability for these young condors to survive and adapt in the wild is pivotal to the success of the conservation of California condors. Locations authorized: All described data collection activities will take place in the blind of the California condor flight pen at Pinnacles National Monument Transportation method to research site(s): Method of access to the California condor flight pen will be by foot once inside Pinacles National Monument. Collection of the following specimens or materials, quantities, and any limitations on collecting: No specimens will be collected. Name of repository for specimens or sample materials if applicable: nia Specific conditions or restrictions (also see attached conditions): There are a series of Standard Operating Procuedures established for the condor project that must be adhered to while working on this project. These include: waste management, access, and overnight stays. These are attached. In addition, you must be familiar with the emergency evacuation plan and the protocol for visiting the site to ensure your safety and the safety of the condors. These are also attached. Recommended by park staff(name and title): Reviewed by Collections Manager: F /049/44- Oje44 Yes K No Approved by p official: Date Approved: g&Pr 0-5 Superintendent I Agee To All Conditions And Restrictions Of this Permit As Specified (Not valid unless signed and dated by the principal investigator) rniaia f6iiiiiatoes signature) (Date) THIS PERMIT AND ATTACHED CONDITIONS AND RESTRICTIONS MUST BE CARRIED AT ALL TIMES WHILE CONDUCTING RESEARCH ACTIVITIES IN THE DESIGNATED PARK(S) PernxitPENN-2003-SCI-41004 - Page 2 of 2 231 Permit to collect observational data at Hopper National Wildlife Refuge Complex. January 6 through April 30, 2004. (Chapter 2) Station No. to be Credited Permit No. UNITED STATES DEPARTMENT OF THE INTERIOR 11674 U.S. FMK AND WILDLIFE SERVICE Permittee Name: SPECIAL USE PERMIT Amy C Utt Permiftee Address: • 10650 Mountain View Ave. #607 Application Date: 12/30/03 Period of Use (Inclusive) From: 01/06/04 To: 04/30/04 , Purpose: 0 Agriculture 0 Special Event 0 Commercial Activities 5: Other (explain) El Commercial Filming Research on California...... _...... ,....."...... _ condor , El Commercial Visitor Services - _.,...... Describe the Above Activity: Permittee will supply own transportation to Hopper Mountain NWR and have use of the ranch house as a research station and living quarters. Permittee will have access to condor flight pen to do behavioral observations of captive California condors. , Applicant Signature: Date: (ofc y For Official Use Only • Special Conditions: Record of Payments: Amount of Fee: Record of Partial Payments: Payment Exempt. Full Payment: Partial Payment: This permit is issued by the US. Fish and Wildlife Service and accepted by the signed, subject to the terms, covenants, obligations, and reservations, expresssed or implied herein, and to the notice, conditions and requirements appearing on the reverse side. Issuing Officer Signature and litlef Date: 0 oy. mpum reirtirs t'A - ilit% Motu 110/14 filitl 1=1112 14 1 nun Arkrarstml 41 11,112/14110 232 APPENDIX D IACUC CERTIFICATION FOR ZOOLOGICAL SOCIETY OF SAN DIEGO (CHAPTER 2). 233 - CERTIFICATE OF COMPLETION - This is to certify that PkvIANA L 34 has (Please print participant's name) completed the Zoological Society's IACUC Research Training Self Study Program. Participant's Signature: Date of Completion: ^ For IACUC use only: • The individual named abo ed he r quired reviews with satisfactory results. (Approved by (Forward original to .personnel file in Human Resources, one copy to be retained by IACUC and return, one copy to participant.) - 234 APPENDIX E RELEASE SITE QUESTIONNAIRE & RESULTS - 235 Release Site Questionnaire (Chapter 3).. 1. What would be a serious enough behavior problem to bring a bird in? Can you give me several examples of what a serious problem is? 2. What are examples of mild behavior problems that do not warrant bringing the bird in? 3. Would you re-release a condor that had behavior problems in the past, and if so, how many times are you willing to recapture and re-release a bird? 4. What is your philosophy on managing birds that have behavioral problems? 4. Can you think of reasons why some birds have maladaptive behaviors while others do not? Have there been things you've observed at your release site to give any indicators? 236 Results of Release Site Questionnaire, 2004. 1. Serious behavior 2. What are examples of 3. Would you re-release a 4. What is your 5. Reasons why some problem to bring a bird in? MILD behavior problems condor that had problems philosophy on managing birds have maladaptive Examples. that do not warrant in the past, how many birds that have behaviors while others do bringing bird in? times? behavioral problems? not? What have you observed? HOPPER - Mike Stockton Hanging around towns, Bird lands in neighborhood, Three times. There is room Give them slack, teach Age group - Younger ones. yards, freeway, homes, too oil pump, roosting on in zoos to hold birds, and them not to do it, bringing Nothing to do with Rearing. close to humans. They are ground. It is not an can't hold birds as long in them in won't teach them Parent-reared are more usually young birds that established pattern, try to the field. anything - keep an eye on confident, but they outgrow this. Cut them a flush the bird first. Bringing a them. The idea is to eventually even out and act little slack. Tameness is a bird it doesn't teach it TRAIN them, Young birds the same. They do watch problem as well as attraction anything. have to learn. puppet-reared juveniles to power poles. more at the beginning of a 1\.) release. PINNACLES - Rebecca Leonard Behaviors that jeopardize the Recaptures should be based As many times as needed Virtually any behavioral Origins of maladaptive heath/safety of a condor. on behavior pattern. If a bird until the individual was problem can be behaviors could lie in Inappropriate behavior that lands on a building, is doing well in the field or I corrected/allayed through genetics, events and could corrupt others flushed and doesn't return, was certain it would never aversive training, hazing, experiences occurring (approaching people, landing that's great. It's the pattern be able to model time-out, isolation or other during rearing. Observed on structures - buildings & that is the problem. "acceptable" behavior. Feels creative techniques. experiences, interactions power poles). that virtually any Employ specific strategy and observations at release "behavioral" problem can for behavior you want to site, and mimicking the be corrected or allayed. modify. (based on specific behavior or older condors. bird, environment it lives Nothing more significant in) than another. VENTANA - Jessica Koning Repeatedly approaching Infrequent landing on For severe behavior Mild problems: food Notices older birds tend to people (or letting buildings/allowing people & problem, captivity for at placement away from be more likely to approach people/potential predators to potential predators too close. least 1 month where hazed problem areas and hazing people (less fear) than get too close or landing on Perching on ground once due to fear people/predators. to train condors. Often younger birds. Young birds buildings - ingesting harmful to special circumstances, Must bond with other times it's the people who make the mistake of substances (gasoline, landing beside highway but condors to fit into are intruding on areas roosting on the ground. insulation, lead). Landing on not on it, landing on human dominance hierarchy. where condors have valid Distinction of young birds highway, some pairing structures, but staying on Monitor bird for progress, reasons for using. Seems not being experienced, and problems during breeding roof and not being no progress, long-term easier to train condors than older birds learning the (homosexuality). Can't feed destructive or attempt to eat captivity (1 year) is the tourists. limits of people/situations with other condors (will anything. necessary. Willing to do and learning to exploit starve). Landing on power multiple times for MILD them. poles and wing-begging in problems, only ONE time response to human stimuli. for BAD problems. Roosting on the ground. Sometimes release at difference release site. VENTANA - Joe Burnett Bird actively approaching When it's the issue of people Assesses bird's reaction to Time outs. He Young condors that are people, placing themselves in approaching the bird, not the management technique (if it implemented this practice unprepared for life in the a dangerous location bird approaching the flushes or allows itself to be with Mike Clark at the LA wild. He still seems to have (highway, inside building, person...? captured)? Zoo to help correct an issue with hand-reared cornered in any way, misguided, human- birds, but feels that ground). Each incident is orientated behaviors. immersion with adult unique. Immerse bird with adult condors and other juveniles mentors to focus on social that have been parent-reared hierarchy. may have a good influence on these birds. UN'VERSTY LiBRARLS LOMA LINDA, CALIFORNIA APPENDIX F Release Age of Juvenile California Condors (in months) from 1996-2005. Age at Initial Release in Months 32 Seriesl , 30 -Linear (Series1) 28 26 24 22 20 4e1 18 *16 G4)14 r 12 10 11, 8 6 4 2 0 r r t r 11 f 5 9 13 17 21 25 29 33 37 41 45 49 53 57 61 65 69 73 77 81 85, 89 93 97 101 105 109 Individual birds 1996-2005 239