L. petition at the carcass: opportuniti(\~ 50uthern Ontario. Canadian Journal
9
1980. Lead toxicosis in rap Medical Association 177:941-943. . at low exposure levels: trends in th(~ Toxicology 97: 11-17. rnia Condor (Gymnogyps california 1\. Poole and F. Gill, Eds.). The BirdH . ARENT.
Low Nest Success in a Reintroduced
Population of California Condors
{ and conservation of the Californiu ;alifornia Condor: A Saga of Natural " San Diego, CA.
ona's efforts to reduce lead exposure
:alifornia Condors in the 21st Century
ithology, no. 2.
Patagial transmitters for large vul
tor Conservation Today: ProceedingR
Prey and Owls (B.-D. Meyburg and
;roup for Birds of Prey. Pica Presa,
" P. H. BLOOM, AND C. J. STAFFORD.
lifornia Condors. Journal of Wildlife
:UUSH, S. A.
H. OSBORN, AND T. J. GUlE.
fornia Condors released in Arizona.
21st Century (A. Mee and L. S. Hall,
Allan Mee, 1,3 JanetA. Hamber,2 and Jennie Sinclairl
ABsTRAcT.-The primary goal in the recovery of any formerly extirpated taxa is the establishment of a viable, self-sustaining breeding population. Reintroduced populations of the endangered California Condor (Gymnogyps californianus) began breeding in southern California and northern Arizona in 2001. Here, we studied breeding condors in southern California from 2002-2005 to determine nest success and identify limiting factors for nesting condors. Although hatching success (66.7%) was comparable to the historic wild population of the 1980s, fledging success was extremely low (8.3%). Of 10 chicks hatched in the wild pince 2001, only one survived to fledge successfully. All post-hatching mortality since 2002 I)()curred in the mid to late nestling phase. In two cases, heavy metal toxicosis and complica tions due to the ingestion of foreign material, principally man-made trash, were the cause of death. All but one chick handled since 2002 held.such trash (::;;193.5 g). On average, feeding J'lltes were similar to those at historic nests but were more :variable. Most nests had lower rCleding rates and more prolonged periods of food deprivation than historical nests. Our data guggest that management, principally provisioning at single sites, has significantly altered foraging behavior with detrimental effects on chick survivorship. Whether trash ingestion is I'(\lated to calcium or other nutritional requirements needs urgent investigation. As a prior Ily, we recommend determining the timing of hone mineralization, and capacity for pellet rormation and regurgitation, of nestlings in captivity. In the wild, we recQmmend the removal of problem birds, closing or cleaning up trash sites and, -most importantly, altering current management to reduce dependence on single provisioning sites to promote the development of more natural foraging patterns. However, this is likely to come at a cost of increased exposure 10 lead contamination. Removal of the threat of lead poisoning would allow more flexible and ~eientifically driven management of condor populations.
I CRES,
Zoological Society ofSan Diego, 15600 San Pasqual Valley Road,
California 92027, USA.
~Santa Barbara Museum ofNatural History, 2559 Puesta del Sol, Santa Barbara,
California 93105, USA.
:IE-mail:
[email protected]
'~'scondido,
163
164
MEE, HAMBER, AND SINCLAffi
Apart from preventing extinction, the primary long-term goal III the recovery of any endangered taxa is the establishment of viable, sel r sustaining breeding populations in the wild, usually within the species' historical range (Scott and Carpenter 1987, Kleiman et al. 1994). Witholll the establishment of such populations a species cannot be considered furw tionally secure from extinction regardless of population size, because sudl a population can only be maintained either by immigration or augment:l tion with individuals from an artificially maintained source populati(H) Criteria for assessing the success of a reintroduction necessitate the 100lg term monitoring of demographic parameters such as population grow til. survival, and recruitment rates (see Sarrazin and Barbault 1996, Sarrazi II and Legendre 2000). However, in long-lived species with low reproducti \,' rates and delayed maturation, it may be several years after initial mlea;;,'" before reliable empirical data emerge. Therefore, a first step in assessillg the viability of breeding populations is an accurate measure of breedillg success and productivity. Further, many recovery programs involve inten sive, hands-on management to mitigate the effects of factors limiting Sl)(' cies recovery (e.g., lones et al. 1995, Biggins et al. 1998, Ellis et al. 2000). Therefore, it is also important to evaluate the effect of management stratI"~ gies themselves on the recovery of the reintroduced population. With the recent initiation of breeding by reintroduced Californiu Condors (Gymnogyps californianus), we had the opportunity to carry 0111 intensive studies of nesting condors to determine nest success and ideni iI'y potential limiting factors for the re-establishment of viable breeding pOpll lations in the wild. Previous studies of the recent historic population foulld no apparent deficiencies in either breeding effort or nest success (Snyd!'I' and Hamher 1985, Snyder and Snyder 1989). Instead, the major limitill/o( factor and apparent cause of the catastrophic decline to near extinctioll of the condor population was high adult mortality primarily due to lead poisoning (Snyder and Snyder 1989, 2000; Snyder this volume). Howewl', the intensive research conducted at nests in the 19808 provides an exccl· lent baseline against which current breeding effort and nest success can Itl' evaluated (see Snyder and Hamher 1985, Snyder and Snyder 2000, Snyd!'" and Schmitt 2002). The California Condor is one of the most critically endangered bird" in the world with a current population, as of 1 January 2006, of 275 birdM including 128 free-flying and 147 captive individuals (J. Grantham ill litt.). Reintroduction to the wild began in southern California (1992), and subsequently in northern Arizona (1996), central California (1997) ami most recently, Baja California, Mexico (2002). The first breeding attemplH occurred in 2001 in southern California and northern Arizona with the firlll successful fledging in the wild in 2003 in northern Arizona. Here, we evalu" ate the measure most critical to attaining the goal of viable self-sustainitlj,!
LOW NEST SUCCESS IN CONDORS
19-term goal in t of viable, self :hin the species' . 1994). Withou! considered func ze, because SUdl m or augmenta lrce population. ssitate the long mlation growth, t 1996, Sarrazin ow reproductive ,r initial releases :tep in assessing ;ure of breeding lS involve inten )rs limiting spe ,llis et al. 2000). Lagement strate .tion. liced California lity to carry out :ess and identify breeding popu opulation found success (Snyder ~ major limiting near extinction rily due to lead ume). However, )vides an excel t success can be er 2000, Snyder Ldangered birds
)6, of 275 birds
r. Grantham in aia (1992), and ilia (1997) and ~eding attempts na with the first Here, we evalu : self-sustaining
165
breeding populations in the wild-nest success-and ask what the data tell
us about the likelihood of reaching that goal after five years of reproduction
in the-wild. Further, we consider the effects of current management of the
southern California condor population on nest success .
METHODS
Study area and population.-We studied condors nesting in the Los Padres National Forest, southern California, between 2002 and 2005. All . condor nesting attempts occurred in the Transverse Ranges and were most often characterized by steep-sided canyons dominated by xeric chapar ral vegetation communities (Plate 15) similar to those described for the histori~ southern California condor population (see Koford 1953, Snyder and Snyder 2000). During the study period the resident condor population in southern California varied between 18 (2003) and 24 birds (2005). Although the number of condors in southern California may be augmented at anyone time by a temporary influx of birds from the central California population, the two "populations" have remained largely discrete. However, during the study period two females released in central California took up . permanent residence in southern California and commenced breeding in 2004. To date, no southern California released birds have dispersed to join other populations. Likewise, no central California released males have paired or attempted to breed in southern California. All adult condors were individually identifiable by having patagial tags with a unique number and color combination. Patagial numbers were derived from the last two digits of an individual's studbook number (SB), a number given to all condors for individual identification and popula tion management (.\1ace 2005). In addition, all adults were fitted with at least one conventional VHF radio-transmitter attached to the patagium (Wallace et al. 1994) or mounted on the tail attached to a central retrix. Some breeders were also fitted with solar-powered satellite transmitters (PTTs) attached to their patagia. One female released in central California and now breeding in southern California was fitted with a GPS satellite transmitter. General methods.-To assess nest success we monitored breeding pairs throughout the year from the pre-breeding courtship phase through egg laying, incubation, and brood care until the nesting attempt either failed or succeeded in fledging a,chick. Prior to egg-laying, pairs typically engage in two to three months of courtship involving. extended pair or. tandem flights, mate grooming and roosting, wing-out courtship displays, mount ingand eventu-ally copulation (Koford 1953, Snyder and Snyder 2000, Mee et .al. 2004). Pairs may also inspect a numbe,r of potential nest sites during this period but especially in the weeks priQr to egg-laying. We monitored
166
MEE, HAMBER, AND SINCLAIR
pairs closely to locate nests, and determine the timing of egg-Iaying~ and onset of incubation. Following egg-laying, we observed nests to determine attendance patterns, hatching, and subsequent brood care. Nests were occasionally Visited to check egg fertility (n = 3), to carry out health checks on nestlings (n 3), and to sift nest cave substrates to recover eggshell fragments and identify faunal and non-faunal material brought to nests by condors (n 8). Parental care in condors is one ofthe most extreme of any bird species including 53 to 60 days of incubation and up to six months or more of brood care prior to fledging (Snyder and Schmitt 2002). Parental care also extends for several months post-fledging so that pairs successfully rearing a chick in one year may skip breeding the next presumably because of the demands of care (Snyder and Hamber 1985). By studying pairs throughout the breeding season we could assess parental effort at nests and identify factors that may be limiting breeding effort and nest success in th-3 00 ~
C"J C"J t1j
00 00
2 C"J
o Z o
~
,... 0\ \.Q
170
MEE, HAMBER, AND SINCLAIR
from nests for health reasons (Plate 16). One was subsequently euthanized and two are recovering following surgery to remove ingested fQreign mate rial (hereafter called trash) at Los Angeles Zoo. Causes of nest failure dur ing the nestling phase have been various (Table 3). However, seven out of eight chicks examined between 2002 and 2005 held quantities of trash (Plate 17). In the most extreme case, one surviving chick removed from the wild in 2004 held 222.5 g of foreign material, 193.5 g of which were trash items. Necropsy of the six chicks that died revealed that in two cases death resulted directly from ingesting trash; one (SB #285) died from acute zinc toxicosis resulting from the ingestion of metallic objects; another (SB #308) was euthanized following surgery to remove trash and the development of chronic respiratory aspergillosis. Cause of death in a third chick (SB #333) was undetermined but the presence of .numeroustrash items was the most Significant post-mortem finding. One chick (SB #288) probably died of dehydration as a result of food deprivation over a period of at least 6-8 days (Table 3). A chick (SB #386) that died during recovery from a nest in 2005 was subsequently diagnosed as having succumbed to West Nile Virus, the first documented California Condor fatality to this disease (B. Rideout unpub!. data). Interestingly, most dead chicks examined to date have exhibited elevated levels of copper in liver samples, although the sig nificance of this finding is unknown. In two cases where the cause of death of nestlings was undetermined (SB #271, SB #333), elevated hepatic cop per was the only noteworthy finding: 531 ppm and 341 ppm, dry weight, respectively (B. Rideout unpubl. data). Food delivery at nests.-We investigated whether the frequency of food delivery to nests might influence nest success by comparing feeding rates at nests of reintroduced condors with those from the historical population during a period (1980-1984) when nest success and chick survivorship were thought to be normal. Mean feeding rates of reintroduced pairs aver aged across all nests were similar to that of ~ondors in the historic popu lation but showed greater variability (Plate 18). Feeding rates typically declined at reintroduced and historic condor nests after the first month of brood care. However, at all reintroduced condor nests feeding rates were lower than the average for historic nests in the first few weeks after hatch ing (Table 4 and Plate 18). Further, at some reintroduced condor nests, pairs delivered food at lower rates than at historical condor nests over prolonged periods (e.g., SC4 pair in 2005; see Table 4). Although feeding rates at two nests during the mid to late nestling phase were lower than that recorded for any nest in the historic population of the 1980s 5), there was no overall difference in feeding rates between the popula (t = 0.132, n = 5, P == 0.89). Effects of management.-Another useful measure of chick frequency is the proportion of days on which feeding occurs.
171
LOW NEST SUCCESS IN CONDORS
Table 4, Feeding rates at nests hatching chicks in southern California (2002-2005), Feeding rate (events h-1 ) by week after hatch Pair a 2002 So, Call 2003 So, Cal 4 2004 So. Cal 5 So. Cal 6 2005 So. Cal 4
1-4
5-8
9-12
13-16
17-20
21-24
Mean± SD
0,392
0,151
0,098
0,060
nd b
nd b
0,176 ± 0,149
0.127
0.079
0.115
0.111
0.098
0,207 0.340
0,226 0,266
0.109 0.098
0.156 0.133
0.157
0,319
0,131
0.073
0.106 ± 0,018 0.133
d
0.161 ± 0,041 0.209 ± 0,113 0.174 ± 0.129
1980-86 (n = 5): mean = 0.50 h-1 in week 1 after hatch f 1980-86 (n = 5): range =0.09-0.12 h-1 in week 10-25 after hatch f a Only
pairs hatching chicks with comprehensive data for each time period are presented here.
No data (nd) for this period; chick died day 171-174 (week 25).
C Chick removed from nest on day 223 (week 14) for health reasons, subsequently
eutl1anized at LAZ. dChick fell from nest on day 117-121 (week 19-20), removed to LAZ. e Chick died during removal from nest on day 98 (week 14). fSnyder and Snyder (2000). b
Table 5. Chick-feeding at reintroduced and historic condor nests during the mid-late nestling phase. Weeks 10-25 post-hatch Year
Pair
2002 2003 2004 2004 2005
So. Call So. Cal 4 So. Cal 5 So. Cal 6 So. Cal 6 Mean ± SD
1980-84 (n
Feeding rate (events h-1 )
Non-food days (%)
0,073 0.109 0.143 0.109 0.065
46.2 29.7 35,1 40,9 62.5
= 0,099 ± 0,031
42.9
= 5): Mean ± SD 0.102 ± 0,012a = 0.09-0.12b
14-30 b
a Mean feeding rate for historical nests derived from data presented in Snyder and Snyder (2000). b Snyder and Snyder (2000).
172
MEE, HAMBER, AND SINCLAIR
reintroduced condor parents obtain a large proportion of their food from provisioned sites designed to maintain birds on food fr~e of lead contami nation. Thus, because chicks may be fed disproportionately on days 011 which f
