Egg Size, Fertility, Hatchability, and Chick Survivability in Captive California Condors (Gymnogyps Californianus)

Zoo Biology 23:489–500 (2004)

Egg Size, Fertility, Hatchability, and Chick Survivability in Captive California Condors (Gymnogyps californianus)

Nancy C. Harvey,1n Jenine D. Dankovchik,1 Cynthia M. Kuehler,2 Tom Levites,3 Susie Kasielke,4 Lloyd Kiff,5 Michael P. Wallace,1 and Michael E. Mace3 1Center for Reproduction of Endangered Species, Zoological Society of San Diego, San Diego, California 2Keauhou Bird Conservation Center, Volcano, Hawaii 3San Diego Wild Animal Park, Escondido, California 4Los Angeles Zoo, Los Angeles, California 5The Peregrine Fund, Boise, Idaho

California condors are one of the most endangered species native to the mainland United States and are subject of intense effort regarding captive breeding and reintroduction. We analyzed 20 years of California condor egg records from the wild and from three captive propagation facilities for fertility, hatchability, and chick survivability, along with changes in egg size due to multiple clutching. Overall annual mean percent of fertile eggs was 80.2%, hatchability was 87.3%, and chick survivability to Z60 days was 95.5%. One egg-laying site had a significantly lower fertility rate (P r 0.0001) than the other sites, which was probably due to pair incompatibility rather than any physiological factors. Egg volume of the first egg was significantly greater than both the second (t ¼ 6.73, P ¼ 0.0001) and third egg (t ¼ 6.62, P r 0.0001) of the season, while the second egg had a significantly greater volume (t ¼ 3.20, P ¼ 0.0084) than the third egg. Chicks from the second egg (t ¼ 3.24, P ¼ 0.029) and third egg (t ¼ 7.94, P ¼ 0.0014) of the season were significantly smaller than chicks from the first egg of the season. The decrease in egg measures and chick hatch weight due to multiple clutching did not affect hatchability or chick survivability. There were significant positive relationships (Po0.0001) between fresh egg weight and chick hatch weight and between egg volume and chick hatch weight, as well as between fresh egg weight and egg volume. In spite of the decrease in fresh egg weight, egg volume and chick hatch weights, due to egg removal to stimulate double and sometimes triple clutching, the captive propagation program has been nCorrespondence to: Nancy C. Harvey, Center for Reproduction of Endangered Species, Zoological Society of San Diego, P.O. Box 120551, San Diego, CA 92112. E-mail: [email protected] Received for publication July 1, 2003; Accepted October 26, 2003. DOI 10.1002/zoo.20015 Published online in Wiley InterScience (www.interscience.wiley.com).

c 2004 Wiley-Liss, Inc. 490 Harvey et al. successful in producing birds for the restoration of this species. Zoo Biol 23: 489–500, 2004. c 2004 Wiley-Liss, Inc.

Key words: endangered; Gymnogyps californianus; multiple clutching; egg volume

INTRODUCTION Successful captive breeding programs for the restoration of critically endangered avian species, such as the Peregrine falcon (Falco peregrinus) [Cade et al., 1988], California condor (Gymnogyps californianus) [Kuehler and Witman, 1988], San Clemente loggerhead shrike (Lanius ludovicianus mearnsi) [Farabaugh et al., 2002], and a variety of Hawaiian forest birds [Kuehler et al., 2000, 2001] require high rates of viable fertile eggs, hatchability, and chick survivability for such programs to be successful. Although detailed records on egg weight, length, breadth, fertility, and/or viability, along with hatchability and chick survivability, are routinely maintained in captive propagation programs, few of the data from such records have been published. For seven endangered Hawaiian forest bird species, hatchability for viable eggs was 82.0%, and survivability to 30 days of age was 86.0% and (Kuehler, personal communication). Egg records from another captive passerine species, the San Clemente loggerhead shrike, revealed 82.7% fertility, 96.9% viability, 72.2% hatchability, and 54.4% chick survivability for eggs that were removed for artificial incubation and hand-rearing (Farabaugh, personal communication). When shrike eggs were left with the parents for incubation and chick rearing, 31.3% of the eggs disappeared or were broken, so their fertility and viability could not be determined. Of the total eggs from captive parent-reared nests, known fertility was only 66.9%, hatchability was 81.4%, and chick survivability was 92.9% (Farabaugh, personal communication). Captive propagation programs for the restoration of endangered species often resort to double and sometimes triple clutching to rapidly increase the population. For captive Peregrine falcons [Burnham et al., 1984], this strategy resulted in a significant decline in mean egg weight and mean egg breadth from the first to the second, and again from second to the third clutches laid in the same year for captive Peregrine falcons [Burnham et al., 1984]. Similar data are unavailable for the San Clemente loggerhead shrike and the Hawaiian forest birds captive propagation programs. Field biologists recognized California condors as critically endangered by the early 1980s [Snyder and Snyder, 1989, 2000]. Starting in 1982, the Condor Recovery Team (CRT) agreed to transfer wild eggs and immature birds to the Zoological Society of San Diego’s (ZSSD) facility at the San Diego Zoo (SDZ) and Los Angeles Zoo (LAZ) to minimize extinction risks. Following additional condor losses in the wild, the U.S. Fish and Wildlife Service agreed with CRT recommendations and began removing the remaining nine birds from the wild and placing them in captive facilities [Snyder and Snyder, 1989]. The entire population of condors numbered 27 at the start of the captive propagation program in 1987, with 15 birds at the ZSSD’s facility at the Wild Animal Park (WAP) and 12 birds at the (LAZ). In 1995, The Peregrine Fund (TPF) became the third organization to participate in the captive- breeding program. California condors become sexually mature at around 6 years of age [Koford, 1953; Snyder and Snyder, 1989] and typically lay a single egg every 2 years. California Condor Egg Size and Fertility 491

California condors have the capacity to lay a replacement egg if the previous egg/ chick is lost or removed early in the season [Snyder and Hamber, 1985]. From 1987 to 1994, the condor staff routinely removed eggs from the captive pairs on the day of oviposition for artiﬁcial incubation and hand rearing, allowing the birds the possibility of laying a second clutch, and in some cases a third clutch, within a single season. Protocols for artiﬁcial incubation, egg weight loss, adult and chick diets, feeding schedules, and record keeping were established early in the program [Kuehler and Witman, 1988; Toone and Risser, 1988]. In 1995, the CRT recommended that birds hatch and rear their second egg of the season, therefore eliminating the possibility of them laying a third egg within one breeding season. Almost two decades of egg records from three captive propagation facilities dedicated to the recovery of the California condor provide a unique opportunity for analyzing information on fertility, hatchability, and chick survivability.

MATERIALS AND METHODS Housing and Diet Each captive pair is housed in a large outdoor ﬂight pen, with an adjacent roost area leading to a secluded nest box. At all three facilities, the birds are fed rabbits, rats, and ﬁsh. At the WAP and TPF, the diet also includes chicken. In addition, the WAP provides canine diet and beef spleen, while the LAZ provides feline diet and horsemeat. Water is provided ad libitum. In an effort to control weight gain and to mimic food availability in the wild, the birds at the WAP are fasted 2 to 3 nonconsecutive days per week, and at the LAZ they are fasted during the 2 weekend days plus 1 nonconsecutive day during the week.

Source of Eggs and Sample Size A total of 46 females and 42 males in 53 different pairing combinations contributed 406 eggs to the database from 1983 to the end of the 2003 breeding season. Of the 406 eggs, 16 eggs came from the wild, 141 from the WAP facility, 131 from the LAZ facility, and 118 from TPF facility.

Incubation From 1983 to 1985, modiﬁed Lyon incubators were used for incubation [Kuehler and Witman, 1988]. After 1985, Peterson Model 1 incubators were used at both the WAP and the LAZ. The Lyon incubators were used as hatchers at the WAP, while at the LAZ the Peterson Model 1 incubator tray was maintained at a level position for hatching. Finally, TPF used a Humidaire Model 21 for both incubation and hatching. The incubation parameters used for the ﬁrst 15 eggs brought in from the wild [Kuehler and Witman, 1988] included a theoretical mean egg weight loss of 12.0% (fresh egg to pip). Out of 298 fertile eggs, 253 eggs hatched, and 238 chicks survived to Z60 days of age. Chicks were hand-reared (n ¼ 192), parent-reared (n ¼ 45), or cross-fostered (n ¼ 16) to either a different pair of California Condors or to a pair of Andean Condors (Vultur gryphus). 492 Harvey et al.

Egg Measurements Upon removal from the nest, the aviculturalists weighed the eggs to the nearest 0.10 gram on Satorius (WAP), A&D Co. Ltd. (LAZ), and Denver (TPF) digital scales. Fresh egg weights were acquired on 239 eggs. There were records for 338 eggs for which both length and breadth measures were available to calculate egg volume. Aviculturalists measured the length and breadth of each egg to the nearest 0.10 mm. Length and breadth measures for the wild and captive eggs at the WAP were acquired with a Mitutoya digital caliper, while the LAZ and TPF facilities used SPI and Craftsman dial calipers, respectively. Since we had more length and breadth measures than fresh egg weights, we also calculated egg volume (V) using Hoyt’s 2 [1979] equation (V ¼ Kv LB ) where the estimated volume coefﬁcient (Kv ¼ 0.507) is applicable to all eggs which are not very pointed.

Fertility Evaluation Out of 406 eggs, avicultural records showed that 298 were fertile, 92 were infertile, and 16 eggs (12 broken and four with fertility undetermined) were unknown. At the WAP, pathologists cultured egg contents for eggs that failed to show development of vascularization after 10 days of incubation, in order to substantiate the aviculturalists’ classiﬁcation of fertility status. At the LAZ, all but three such eggs were broken open and evaluated for fertility status, while at TPF, candling was the sole method of determining fertility status of eggs that failed to show signs of vascularization. Well trained, aviculturalists usually can detect early signs of fertility during candling prior to the onset of vascularization. Nevertheless it is possible that some of the eggs from TPF that were classiﬁed as infertile may in fact have been early embryonic deaths (EEDs).

Data Analysis We calculated the percent of eggs classified as fertile, infertile, and fertility unknown, along with hatchability and chick survivability for each year. In order to control for the use of different scales and calipers across the captive-breeding sites, a mean fresh egg weight and volume was calculated for each female and an ANOVA was undertaken to determine if the length and breadth measures were significantly different between sites. Since neither mean fresh egg weight (F ¼ 1.27, P ¼ > 0.30) nor mean egg volume (F ¼ 1.21, P ¼ 0.32) differed between sites, pooling of data from the different sites for seasonal egg number weight and volume was possible. Mean egg weight and volume for the first, second, and third egg of the season, as well as initial chick hatch weight from the first, second, and third egg of the season, were also calculated. We used ANOVAs for comparisons between facilities, with regard to fertility, hatchability, and survivability, as well as examining season egg number and fertility status. Fisher’s protected least significant difference (PLSD) post hoc tests were used for determining which pairwise combinations were significantly different from each other. For eggs that were fertile and hatched, mean overall percent weight loss for fresh eggs at each site was calculated, along with the number of hours from pip to hatch and Kruskal-Wallis tests were undertaken to determine if there was a facility difference during incubation for these two variables. We used Chi-squared tests to examine facility differences in stages of embryonic death. Paired t-tests were undertaken to compare egg weight, volume, and chick-hatch weights across the first, California Condor Egg Size and Fertility 493 second, and third egg of the season. Simple linear regressions were calculated to evaluate the relationship between fresh egg weight and chick hatch weight, egg volume and chick hatch weight, as well as fresh egg weight and Hoyt volume. Significance for all tests was Po0.05.

RESULTS Egg Weight, Length, Breadth, Volume and Season Egg Number When fresh egg weight, breadth, length, egg volume, and chick hatch weights were compared across the first, second, and third eggs of the season (Table 1), we found significant differences over the breeding season. The first egg of the season was significantly heavier than the second egg (t ¼ 7.14, Po0.0001) and third egg of the season (t ¼ 6.69, P ¼ 0.0003). The second egg of the season was also significantly heavier than the third egg of the season (t ¼ 3.88, Po0.004). There was a significant difference in egg breadth, with the first egg of the season being significantly larger in breadth than the second egg (t ¼ 6.90, Po0.0001) and the third egg of the season (t ¼ 4.52, P ¼ 0.0011). The breadth of the second egg was also significantly different (t ¼ 2.55, Po0.030) from the third egg of the season. In contrast, egg length decreased significantly (t ¼ 2.23, P ¼ 0.0445) only from the first to the third egg of the season. Volume of the first egg was significantly greater than the second (t ¼ 6.73, Po0.0001) and third egg (t ¼ 6.62, Po0.0001), and the volume of the second egg was significantly greater (t ¼ 3.20, P ¼ 0.0084) than the third egg. Finally, chick hatch weight declined with season egg number, with chicks from the second and third egg of the season weighing significantly less (t ¼ 3.24, P ¼ 0.029 and t ¼ 7.94, P ¼ 0.0014, respectively) than chicks from the first egg of the season (Table 1). There were significant positive relationships (Fig. 1) between fresh egg weight and chick hatch weight (R2 ¼ 0.854, Po0.0001), between egg volume and the initial hatch weight of chicks (R2 ¼ 0.769, Po0.0001), as well as between fresh egg weight and Hoyt volume (R2 ¼ 0.901, Po0.0001).

Fertility, Percent Egg Weight Loss, Hatchability, and Chick Survivability Mean annual fertility was 80.2% (7 3.6 SE), infertility 16.6% (7 3.0 SE), and unknown fertility 3.2% (7 1.0 SE). There were 111 eggs for which fresh weights and percent weight loss during artiﬁcial incubation were available. For these data, overall mean fresh egg weight loss for artiﬁcially incubated eggs was 13.3% (7 0.10 SE)

TABLE 1. Comparisons of mean weight, length, breadth, and volume of eggs, and initial hatch weights of chicks from the ﬁrst, second, and third egg of the breeding season Egg length Egg breadth Egg volume Egg weight (mm) (mm) (mm3)a Chick weight (g) Egg number n Mean7SE n Mean7SE n Mean7SE n Mean7SE n Mean7SE First 69 268.5772.55 101 106.3870.43 106 66.9570.21 105 242.3471.99 33 180.5272.41 Second 71 260.1272.80 100 105.7070.48 106 65.9870.22 104 233.7372.23 32 173.4673.16 Third 10 246.8779.18 13 105.7571.94 11 65.0270.69 13 224.8077.45 5 165.4679.13 aHoyt [1979]. 494 Harvey et al.

Fig. 1. Scatterplots of hatching mass in relation to egg volume of 173 California condor chicks hatched in captivity. percent with a range from 10.0 to 14.8 %. Comparison between facilities revealed a signiﬁcant difference (H ¼ 19.35, Po0.0001) with LAZ having a smaller mean egg weight loss over the course of incubation than either the WAP and TPF facilities (Table 2). California Condor Egg Size and Fertility 495

Among fertile eggs, mean annual hatchability was 87.3% (7 2.4 SE) and chick survivability to >60 days of age was 95.5% (7 1.5 SE). All of the 16 eggs removed from the wild for the initiation of the captive program were fertile. Subsequently, each of the captive facilities had both infertile eggs and eggs of unknown fertility. Comparisons between sites revealed significant differences in fertility and infertility (Table 3), with the newest facility (TPF) having a significantly lower percentage of fertile eggs than the wild (Po0.0001), the LAZ (Po0.0001), and the WAP (Po0.0001). No significant differences were found between sites in the percent of eggs identified as fertility unknown, hatchability, or in chick survivability (Table 3). While the LAZ had the lowest annual percentage of infertile eggs, it also had a greater number of early embryonic deaths (Table 4), but the difference was not

TABLE 2. Comparisons of mean egg weight loss across facilities Facility No. of eggsa Egg weight lossb WAP 50 13.5970.15 LAZ 53 12.9370.13 TPF 8 13.7170.09 aNumber of fertile eggs where both fresh egg weights and percent weight loss were available. bMean7SE.

TABLE 3. ANOVA results of site comparisons for egg fertility, hatchability, and chick survivability toZ60 days of age for all eggs hatched in captivity % Fertility % Survive No. of No. of % Fertile % Infertile unknown % Hatch Z60 days Facility eggs years per yearb per yearb per yearb per yearb per yearb Wilda 16 4 100.070.0 0.070.0 0.070.0 91.778.3 93.876.2 WAP 141 15 81.773.7 15.273.5 3.171.2 88.473.0 94.872.2 LAZ 131 14 88.175.4 5.772.8 6.273.2 81.574.7 93.972.9 TPF 118 8 38.277.8 56.476.7 5.471.9 82.476.6 100.070.0 Df 3 3 3 3 3 F 16.37 28.59 0.79 0.79 0.78 P o0.0001 o0.0001 0.51 0.51 0.52 aEggs that were brought in from the wild and hatched in captivity. bMean7SE averaged across years.

TABLE 4. Number of early, middle, and late embryonic deaths for each condor breeding facility Early embryonic Middle embryonic Late embryonic Total embryonic Facility death (EED) death (MED) death (LED) death WILDa 10 01 WAP 2 0 10 13 LAZ 10 2 10 22 TPF 2 0 6 8 Totals 15 2 26 43 aAll eggs brought in from the wild were incubated and hatched at the Avian Propagation Center at the San Diego Zoo. This program was transferred to the WAP after the incubation and captive breeding facility was completed. 496 Harvey et al. TABLE 5. ANOVA comparison of fertility classiﬁcation of all California condor eggs hatched in captivity by season egg number First Second Third Egg fertility classiﬁcation n Mean %7SE n Mean %7SE n Mean %7SE df FP Fertile 186 78.974.0 101 82.774.4 11 93.876.2 2 1.27 0.29 Infertile 63 16.673.7 27 15.874.4 2 6.276.2 2 0.67 0.52 Fertility unknown 11 3.471.1 5 1.571.1 0 n/a 2 1.28 0.29

TABLE 6. ANOVA comparisons of hatchability of fertile eggs and survivability of California condor chicks toZ60 days of age by season egg number Season egg number No. hatch % hatch per year No. survive % survive per year First 159 87.572.8 152 95.6%71.6 Second 84 88.773.2 78 91.7%73.7 Third 10 100.070.0 9 87.5%712.5 df 2 2 F 1.81 0.78 P 0.17 0.46

significant (df ¼ 6, X2 ¼ 7.94, Po0.25) indicating that candling alone was a reliable method for determining fertility classification at TPF. With regard to season egg number, no significant fertility classification differences were found (Table 5). Likewise, if eggs were fertile, there were no significant differences between season egg number with regard to hatchability or survivability of chicks to Z60 days of age (Table 6). Infertile Eggs In an attempt to identify possible factors involved in infertility, we separated 90 of the 92 infertile eggs by facility into three male breeding categories (Table 7). Males from all three categories were paired with sexually mature females. Category I included infertile eggs from sexually immature males (age r 5). Category II included infertile eggs from sexually mature males, which had never produced fertile eggs. Category III included infertile eggs from sexually mature males (Z6 years), which previously produced fertile eggs with their mates. Eggs from category I males accounted for 5.6% (5/90), category II for 80.0% (72/90), and category III for 14.4% (13/90) of the infertile eggs. A greater proportion 79.2% (57/72) of the infertile eggs from category II males came from TPF facility (Table 7). Males in category II accounted for 47.8% (43/90) of the infertile eggs, in spite of being paired for 2 to 6 years after both partners were sexually mature (Table 8). With the exception of one male (SB# 28), five of the remaining six males at TPF were provided with new mates only in the last 1 or 2 years. As a result, one male (SB# 50) produced a fertile egg in the first year of his new pairing, and two other males (SB#s 48 and 61) did so in the second year of their new pairings. In total, seven of the nine males were provided new mates, with 57.1% (4/7) of them producing fertile eggs (Table 8). California Condor Egg Size and Fertility 497 TABLE 7. Facility, male breeding experience category, number of pairs, and number of infertile eggs WAP 11 pairs LAZ 10 pairs TPF 26 pairs No. of No. of No. of Category Description infertile eggs infertile eggs infertile eggs Total I Sexually immature males 1 0 4 5 II Sexually mature unproven 10 5a 57b 72a,b breeding males III Sexually mature proven 10 0 3 13 breeding males Total 21 5a 64b 90a,b aOne infertile egg was excluded from LAZ, as the egg was laid just after the male was introduced into the flight pen with the female. bOne infertile egg was excluded from TPF, as it was classified as having a very small yolk.

TABLE 8. Pairing combinations where both mates were sexually mature and only produced infertile eggs along with the outcome of the new pairing combinations First pairing combination Subsequent pairings with new femalesa Eggs Male Female Years Infertile Year male Female Fertile Infertile fertility SB#b SB#b pairedc Facility eggs repaired SB# eggs eggs unknown Comments 28 30d 6 WAP 4 1997 47 4 1 1 48 68 5 TPF 8 2002 97 1 1 0 67 49 4 TPF 7 2001 80 0 3 0 60 70 4 TPF 5 2002 68 0 1 0 50 57e 4 TPF 8 2002 88 2 0 0 73 59 5 TPF 5 N/A Planned separation in 2004 61 97 2 TPF 2 2002 70 1 1 74 82 3 TPF 3 NA Released and died 90 80 2 TPF 1 2001 48 0 2 1

Total 43 8 9 2 aIncludes 2003 egg production. bSB#, SSP studbook number. cNumber of years paired since sexual maturity. dFemale SB# 30 paired with a new male, SB# 54 in 1995 at TPF and produced three infertile and 11 fertile eggs in 7 years. eFemale SB# 57 paired with new male, SB# 99 in 2001 at TPF and produced two fertile eggs in 2 years.

The high rate of infertility at TPF was not necessarily due to a delay in pair- bond formation for the production of fertile eggs. Of the 20 original pairings at TPF facility, one or both of the mates were still sexually immature at the time of pairing. Nevertheless, 12 pairs produced fertile eggs, with 16.7% (2/12) doing so in the first year, 41.7% (5/12) in the second year, 33.3% (4/12) in the third year, and 8.3% (1/12) in the fourth year of sexual maturity. In contrast, for six males (SB#s 61, 50, 60, 67, 48, and 73) of the remaining eight pairs, 16.7% (1/6) failed to produce fertile eggs by the second year, 50.0% (3/6) by the fourth year, and 33.3% (2/6) by the fifth 498 Harvey et al. year of sexual maturity. These six pairs alone accounted for 54.7% (35/64) of the infertile eggs from TPF facility (Table 8). For the two remaining sexually mature pairs that failed to produce fertile eggs, one pair (SB# 90 and 80) were separated after their first egg-laying year and the second pair (SB# 74 and 82) were released and subsequently died (Table 8).

DISCUSSION While egg removal was successful in maximizing egg production, it also revealed that female physiological investment was greatest for the first egg of the season. This was seen in the significant decline in egg volume between the first, second, and third egg of the season, as well as in initial chick hatch weights between the first and third chick of the season. In spite of the female’s reduced investment in the replacement eggs and therefore replacement chicks of the season, it did not affect hatchability or chick survivability. At present, it is unknown whether the high hatch and chick survival rates from replacement eggs are characteristic of the species or simply an artifact of intense captive management. It should be noted however, that egg size did not affect hatchability in other studies [Schifferlie, 1973; Moss et al., 1981; Reid and Boersma, 1990; Bolton, 1991; Meathrel et al., 1993; Smith et al., 1995]. Finally, the positive relationship between egg volume and chick hatch weight found in California condors is similar to results found in other avian studies [Schifferlie, 1973; Nolan and Thompson, 1978; Moss and Watson, 1982; Reid and Boersma, 1990; Bolton, 1991; Croxall et al., 1992; Smith et al., 1995; Erikstad et al., 1998]. For a single-clutch layer, it is not surprising that the first egg of the season would be more robust than subsequent replacement eggs. It may be the case that, in California condors, the first egg of the season has a different ratio of yolk to albumen than in replacement eggs, which in turn may affect chick hatch weights, as suggested by Williams [1994] and Christians [2002]. A physiological mechanism of this sort may also account for the high rates of hatchability and chick survivability from seasonal replacement eggs in captive California condors. The significant differences that were found between facilities in egg weight loss did not result in any differences between facilities in either hatchability or chick survivability. These results indicate that acceptable weight loss for fresh condor eggs has at least a 2.0% plus or minus range from the theoretical mean of 12.0% reported by Kuehler and Witman [1988]. Due to the significantly lower fertility rate at TPF compared to the WAP and LAZ, three factors are considered in the production of infertile eggs: 1) absence of copulation, 2) timing of copulation in relation to female oviposition, and 3) mate incompatibility. Absence of copulation due to sexual immaturity of males paired with mature females accounted for a very small percentage of infertile eggs. At the WAP, focal behavioral observations showed that absence of copulation from sexually mature males accounted for five of the 20 (25.0%) infertile eggs. During a pair-bond formation study at the LAZ, one sexually mature male was not observed to copulate for three of his four (75.0%) infertile eggs laid in the early years of the program [Cox et al., 1993]. At TPF, during the course of his daily activities, the aviculturalist did not observe any copulations for the original eight pairs that never produced fertile eggs (Townsend, personal communication). California Condor Egg Size and Fertility 499

California condors engage in multiple copulations over many days before oviposition [Harvey et al., 1996]. In spite of observed copulations, four sexually mature males produced 45.0% (9/20) and 40.0% (2/5) of the infertile eggs at the WAP and LAZ, respectively. This suggests that the timing of copulation in relation to female ovulation and oviposition is not necessarily well coordinated. Unfortu- nately, there are no data on vultures regarding seasonal variation in male sperm production and viability of stored sperm in the female oviduct that would elucidate the temporal relationship between copulation and egg fertility. The high percentage of infertile eggs from some of the pairs at TPF may be a result of pair incompatibility. Separation of forced pairings due to incompatibility problems has already proven successful for three of the six California condor males at TPF as well as one condor male at the WAP. We anticipate that the re-pairing of the three remaining males at TPF with new mates will eventually reduce the high number of infertile eggs in the next 2 to 3 years.

CONCLUSIONS 1. Egg removal to stimulate double- and triple-clutching resulted in a signiﬁcant decrease in fresh egg weight and egg volume. 2. There was a signiﬁcant positive relationship between fresh egg weight and chick hatch weight and between egg volume and chick hatch weight, as well as between fresh egg weight and egg volume. 3. The decrease in egg size due to multiple clutching did not affect hatchability and chick survivability to Z60 days of age under intense captive management procedures. 4. Fertility was high for two of the three captive facilities. The lower rate of fertility at the third facility appears to be more of a function of mate incompatibility. At this facility, separation and re-pairing for production of fertile eggs was successful in three out of six pairs. 5. There was no difference between captive sites in hatchability and chick survivability. 6. The captive propagation of California condors has been successful in producing birds for the recovery of the species.

ACKNOWLEDGMENTS We thank all the condor aviculturalists at the three propagation facilities, including Don Sterner, Debbie Jones, Mike Clark, and Randy Townsend for their record keeping on egg measures, fertility, hatchability, and chick survivability. We also thank Dr. Fred Bercovitch and Alan Lieberman for their constructive comments on the initial draft of this paper.

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