Reproductive behavior in captive California condors (Gymnogyps californianus)

From the fall of 1987 to the spring of 1994, data on reproductive behavior were collected on seven different pairs of California condors (Gymnogyps californianus) housed at the San Diego Wild Animal Park. Behavioral data were collected from videotaped activities in their flight pens. Behaviors for this report include male and female displays and incomplete and complete copulations. Data on the time it took for females to recycle and lay another egg after egg removal were acquired from the California Condor Studbook. Male display rates were significantly higher than female rates throughout the breeding season. Males began displaying 52–132 days before the start of copulations. Copulations slowly increased from Day -51 and peaked ∼ Day -8, prior to egg laying. Female display rates were significantly more frequent at the end of the season after the last egg was laid. An average of 26.8 (±3.1 SEM) copulations occurred prior to egg laying. Copulations occurred throughout the day, with the higher mean percentages occurring between 0700 and 0900 hours. After egg removal, the interval between laying of the first and second eggs and between the second and third eggs had a mean of 34.1 (±10.1 SD) days. © 1996 Wiley-Liss, Inc.     

Changes in incubation sharing in one pair of captive California condors (Gymnogyps californianus)

Three years of behavioral data were collected on incubation behavior in one pair of captive condors (Gymnogyps californianus) at the San Diego Wild Animal Park. Data were collected from daily video tape reviews of the nest box. The amount of time each bird was in the nest box, and whether it was on or off the egg were recorded, along with any aggressive interactions observed in the nest. For the first 2 years, the female incubated the egg(s) significantly more than the male. During the third year, the male increased his incubation time on the egg, resulting in no difference between the two sexes in incubation time. Changes in male incubation behavior may be a result of several factors: increased compatibility between the pair, social maturation, and/or increased dominance on the part of the male. © 1994 Wiley-Liss, Inc.     

Report on captive hatches of California condors (Gymnogyps californianus): 1983–1990

The California condor (Gymnogyps californianus) recovery plan entails increasing the reproductive rate via replacement-clutch manipulation and artificial incubation of eggs. During the period from 1983 to 1990, 37 eggs have been artificially incubated; 32 of these were known to be fertile and 28 hatched (fertility: 86.5%; hatchability: 87.5%).     

Egg size,fertility, hatchability,and chick survivability in captive California condors (Gymnogyps californianus)

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 ≥60 days was 95.5%. One egg-laying site had a significantly lower fertility rate (P ≤ 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=6.73, P=0.0001) and third egg (t=6.62, P ≤ 0.0001) of the season, while the second egg had a significantly greater volume (t=3.20, P=0.0084) than the third egg. Chicks from the second egg (t=3.24, P=0.029) and third egg (t=7.94, P=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 (P<0.0001) 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 successful in producing birds for the restoration of this species. Zoo Biol 23:489–500, 2004. © 2004 Wiley-Liss, Inc.     

Artificial incubation of California condor Gymnogyps californianus eggs removed from the wild

The currrent California condor (Gymnogyps californianus) recovery plan entails increasing the reproductive rate via replacement-clutch manipulation of eggs. During the period from 1983 to 1985, 15 eggs were removed from wild nesting pairs for artificial incubation. The eggs were incubated at a dry bulb temperature of 36.4°C in modified forced-air Lyon Electric incubators. The incubation humidity was adjusted for individual eggs based on weight loss data (water = weight), 25.6–30.0°C wet bulb (41.0–63.0% Relative Humidity (RH)). The chicks were hatched initially under forced-air conditions of 36.1°C dry bulb, 31.1–01.7°C wet bulb (70.0–73.0% RH). In 1984, hatching parameters were changed to still-air conditions, 36.1°C dry bulb (top of the egg), 35.0°C dry bulb (bottom of the egg), 31.1–31.7°C wet bulb (70.0-73.0% RH). Tactile and auditory stimulation was utilized during the pip-to-hatch interval. From among 15 eggs collected, 13 hatched, and 12 condor chicks were raised successfully (hatchability: 86.7%; survivability: 92.3%).     

Patterns of mortality in free-ranging California Condors (Gymnogyps californianus)

We document causes of death in free-ranging California Condors (Gymnogyps californianus) from the inception of the reintroduction program in 1992 through December 2009 to identify current and historic mortality factors that might interfere with establishment of self-sustaining populations in the wild. A total of 135 deaths occurred from October 1992 (the first post-release death) through December 2009, from a maximum population-at-risk of 352 birds, for a cumulative crude mortality rate of 38%. A definitive cause of death was determined for 76 of the 98 submitted cases, 70% (53/76) of which were attributed to anthropogenic causes. Trash ingestion was the most important mortality factor in nestlings (proportional mortality rate [PMR] 73%; 8/11), while lead toxicosis was the most important factor in juveniles (PMR 26%; 13/50) and adults (PMR 67%; 10/15). These results demonstrate that the leading causes of death at all California Condor release sites are anthropogenic. The mortality factors thought to be important in the decline of the historic California Condor population, particularly lead poisoning, remain the most important documented mortality factors today. Without effective mitigation, these factors can be expected to have the same effects on the sustainability of the wild populations as they have in the past.     

Effects of Lead Exposure,Flock Behavior,and Management Actions on the Survival of California Condors (Gymnogyps californianus)

Translocation is an increasingly important tool for managing endangered species, but factors influencing the survival of translocated individuals are not well understood. Here we examine intrinsic and extrinsic drivers of survival for critically endangered California condors (Gymnogyps californianus) whose wild population recovery is reliant upon releases of captively bred stock. We used known fate models and information-theoretic methods to compare the ability of hypothesized covariates, most of which serve as proxies for lead exposure risk, to predict survival rates of condors in California. Our best supported model included the following predictors of survival: age of the recovery program, precipitation, proportion of days observed feeding on proffered carcasses, maximum blood lead concentration over the preceding 18 months, and time since release. We found that as flocks have increased in size and age, condors are increasingly likely to range more widely and less likely to be observed feeding on proffered food, and these “wilder” behaviors were associated with lower survival. After accounting for these behaviors, we found a positive survival trend, which we attribute to ongoing improvements in management. Our findings illustrate that the survival of translocated animals, such as highly social California condors, is influenced by behaviors that change through time.

     

Cytogenetic analysis of California condor (Gymnogyps californianus) chromosomes: comparison with chicken (Gallus gallus) macrochromosomes

The California condor is the largest flying bird in North America and belongs to a group of New World vultures. Recovering from a near fatal population decline, and currently with only 197 extant individuals, the species remains listed as endangered. Very little genetic information exists for this species, although sexing methods employing chromosome analysis or W-chromosome specific amplification is routinely applied for the management of this monomorphic species. Keeping in mind that genetic conditions like chondrodystrophy have been identified, preliminary steps were undertaken in this study to understand the genome organization of the condor. This included an extensive cytogenetic analysis that provided (i) a chromosome number of 80 (with a likelihood of an extra pair of microchromosomes), and (ii) information on the centromeres, telomeres and nucleolus organizer regions. Further, a comparison between condor and chicken macrochromosomes was obtained by using individual chicken chromosome specific paints 1-9 and Z and W on condor metaphase spreads. Except for chromosomes 4 and Z, each of the chicken (GGA) macrochromosomes painted a single condor (GCA) macrochromosome. GGA4 paint detected complete homology with two condor chromosomes, viz., GCA4 and GCA9 providing additional proof that the latter are ancestral chromosomes in the birds. The chicken Z chromosome showed correspondence with both Z and W in the condor. The homology suggests that the condor sex chromosomes have not completely differentiated during evolution, which is unlike the majority of the non-ratites studied up till now. Overall, the study provides detailed cytogenetic and basic comparative information on condor chromosomes. These findings significantly advance the effort to study the chondrodystrophy that is responsible for over ten percent mortality in the condor.     

Inbreeding in three captive groups of rhesus monkeys

Using electrophoretic and serological genetic markers each of 17 potentially inbred matings in three groups of rhesus monkeys could be classified as either inbred or noninbred matings. Although nine of these 17 matings involved either father-daughter or paternal half-sib matings, only 7.4 were expected by chance alone. At least two, and possibly as many as three, of the nine cases of inbreeding involved father-daughter matings. Thus, no evidence of avoidance of inbreeding was observed in the closed captive groups of rhesus monkeys studied. Colony management policies must be developed to minimize the opportunity for or the deleterious effects of both father-daughter and half-sib matings. Furthermore, kin selection theory should consider why kin recognition, if it occurs, does not lead to avoidance of inbreeding.     

The captive husbandry and reproduction of the pink-eared turtle (Emydura victoriae) at Perth Zoo

In 1997, Perth Zoo acquired six pink-eared turtles (Emydura victoriae) from the wild for display in the reptile facility. There is very little documented information on pink-eared turtles in captivity. This article looks at the reproductive biology, ecology, behavior, diet, and captive husbandry of the species. Eight clutches of eggs were documented over a 2-year period with an average clutch size of 10 eggs. Egg size was recorded with three clutches incubated to hatching. Ten hatchlings were maintained for a growth and development study. Measurements of weight, carapace length, width, height, and plastron length were recorded weekly for about 12 months, and then monthly for approximately 2 years. The data were analyzed and showed positive growth curves in all animals. Sexual dimorphism was observed after 20 weeks and sexual maturity in males observed after 2 years.     

Food consumption and growth of California sea lions (Zalophus californianus californianus)

The daily food consumption of 26 California sea lions at the Harderwijk Marine Mammal Park was recorded. Average annual food consumption of males increased with age to stabilize at approximately 4,000 kg/year by the age of 10 years. Females showed a rapid increase in average annual food consumption until they were 3 years old. Thereafter, females housed outdoors averaged 1,800 kg/year, whereas those housed indoors ate approximately 1,400 kg/year. Between the ages of 4 and 7 years, the food intake of males began to fluctuate seasonally, decreasing between May and August. The low food intake in summer was associated with an increase in aggressive behavior. Seasonal fluctuation in the food intake of non‐reproductive females was negligible. Between the ages of 6 and 8 years, many females began to reproduce successfully. Pups were born in May and June. The females' food intake decreased approximately 3 days before birth and ceased the next day. Feeding resumed the day after birth, and by 2 days after birth, it had usually returned to normal. On average, female intake increased in the year of conception, the year of birth, during which the pup was suckled for 6 months, and the following calendar year, during which the pup was weaned. Pups began to eat fish at approximately 11 months of age. When forcefed, they were fully weaned within 2 to 23 days. Male weight and body length increased until approximately 20 years of age. Females increased in body length until 6 years and in weight until approximately 13 years of age. The relationship between standard body length and body weight is given. The heavier an animal is, the lower is its food intake as a percentage of body weight. Zoo Biol 19:143–159, 2000. © 2000 Wiley‐Liss, Inc.     

Effects of diet on captive black-footed ferret (Mustela nigripes) food preference

Black-footed ferrets (Mustela nigripes) are both habitat and prey specialists that depend on prairie dogs (Cynomys spp.) for food and utilize prairie dog burrows for refuge. In this study we investigated the effects of captive diet during early development on adult black-footed ferret food preferences. To test the hypothesis that early diet affects the food preferences of adult black-footed ferrets, we exposed 22 kits (divided into three experimental groups) to different quantities of prairie dog in the diet: no prairie dog, prairie dog three times per week, and prairie dog daily during the assumed sensitive period for olfactory imprinting, i.e., between 60–90 postnatal days. At age 5 months, kits were individually tested in a food choice cafeteria trial. Results indicated that higher amounts of prairie dog in the ferrets' early diet led to a higher preference for this food item when ferrets reached adulthood. These results have important implications for black-footed ferret recovery and have been considered in the reintroduction protocol. © 1996 Wiley-Liss, Inc.     

Interannual variation in the at‐sea behavior of California sea lions (Zalophus californianus)

To be successful, marine predators must alter their foraging behavior in response to changes in their environment. To understand the impact and severity of environmental change on a population it is necessary to first describe typical foraging patterns and identify the underlying variability that exists in foraging behavior. Therefore, we characterized the at‐sea behavior of adult female California sea lions (n = 32) over three years (2003, 2004, and 2005) using satellite transmitters and time‐depth recorders and examined how foraging behavior varied among years. In all years, sea lions traveled on average 84.7 ± 11.1 km from the rookery during foraging trips that were 3.2 ± 0.3 d. Sea lions spent 42.7% ± 1.9% of their time at sea diving and displayed short (2.2 ± 0.2 min), shallow dives (58.5 ± 8.5 m). Among individuals, there was significant variation in both dive behavior and movement patterns, which was found in all years. Among years, differences were found in trip durations, distances traveled, and some dive variables (e.g., dive duration and bottom time) as sea lions faced moderate variability in their foraging habitat (increased sea‐surface temperatures, decreased upwelling, and potential decreased prey abundance). The flexibility we found in the foraging behavior of California sea lions may be a mechanism to cope with environmental variability among years and could be linked to the continuing growth of sea lion populations.     

On the sunny side of (new) life: Effect of sunshine duration on age at first reproduction in Japanese macaques (Macaca fuscata)

To produce offspring early in life is energetically demanding and depends greatly on environmental conditions. In female primates, age at first reproduction (AFR) has been associated with social parameters (e.g., population density and social rank), food availability and meteorological conditions (e.g., photoperiod, rainfall patterns, and temperature). Regarding the latter, less attention has been given to the influence of sunshine. In nonhuman primates, including the northern‐most distributed Japanese macaque (Macaca fuscata), sunbathing is an effective thermoregulatory strategy to maintain sufficient energy intake during harsh winter months. Furthermore, the energetic value of sunshine and its role in the synthesis of essential vitamins important for sexual development and overall fertility is well investigated using human and animal models. In the present study, we hypothesized that female's AFR is influenced by the amount of sunshine in a semi‐free‐ranging, provisioned a group of Japanese macaques. To test this, we gathered data on sunshine duration in the year females theoretically experienced the onset of puberty. This phase of the female life cycle is particularly prone to the effects of environmental conditions. In addition to the investigation of sunshine duration and other meteorological conditions (i.e., rainfall and temperature) we controlled for social parameters (i.e., group size and sex ratio) as potential covariates. We found a clear effect of sunshine duration on female AFR: Females who entered puberty in years with more sunshine reproduced for the first time at significantly younger ages than females who experienced less sunshine during this specific period of their development. Possible mechanisms for how the sunshine influences sexual maturation in Japanese macaques are discussed.     

Successful captive breeding of Mitchell's water monitor,Varanus mitchelli (Mertens 1958), at Perth Zoo

Mitchell's water monitors (Varanus mitchelli) have been maintained on display at Perth Zoo since 1997. They are generally a timid species but have been maintained and bred in a mixed species water feature exhibit. In this article we describe their captive management and behavior with an insight into their reproductive biology. Between 2002 and 2005, 11 clutches were laid ranging from 13 to 27 (X? = 20) eggs from one female. Egg size ranged between 3.00 and 6.08 g (X? = 4.77 g) in weight, 22.8 and 31.9 mm (X? = 28.3 mm) in length, and 11.1 and 19.3 mm (X? = 17.1 mm) in width. Oviposition included double and triple clutches ranging between 41 and 60 days apart (X? = 48 days), events n = 6. Four clutches were incubated at three different temperatures and hatchlings emerged after 157–289 days. The weight of the hatchlings ranged between 2.60 and 4.52 g (X? = 4.34 g). Total length ranged between 140.1 and 178.0 mm (X? = 165.9 mm) and snout–vent length ranged from 53.8 to 70.0 (X? = 64.4 mm). Juvenile growth and development information is presented from hatching through to approximately 3 years of age. Zoo Biol 29:615–625, 2010. © 2009 Wiley‐Liss, Inc.     

Association between hybrid status and reproductive success of captive male and female rhesus macaques (Macaca mulatta) at the California National Primate Research Center (CNPRC)

The California National Primate Research Center (CNPRC) houses more than 1,000 rhesus macaques (Macaca mulatta) of mixed Chinese-Indian ancestry. Most of these animals are kept in outdoor field cages, the colony's long term breeding resource. Since 2001, hybrids comprised between 4 and 49% of the field cage populations, but in most cases have represented a maximum of 10% of those populations. The increasing prevalence of hybrids is partly due to management efforts to distribute genetic diversity effectively and minimize genetic subdivisions. However, other factors may also contribute to the spread of hybrids within the colony, most notably variance in socio-sexual behaviors and physical attributes. It is known that hybrids of some species exhibit heterosis, such as early maturation, that can enhance reproductive success, and anecdotal observations of mixed groups of hybrid, Indian and Chinese animals at the CNPRC suggest that hybrids are more sexually active. To determine whether hybrids experienced a reproductive advantage, a study was conducted using birth records of 5,611 offspring born in the CNPRC colony between 2003 and 2009. We found that while the degree of Chinese ancestry (DCA) appeared to influence the maturational schedule of both males and females (maturation was inversely related to proportion of Chinese ancestry), DCA had no independent effect on either male or female RS or rank. Therefore, we have found no evidence that a hybrid phenotype confers an absolute reproductive advantage in our colony.     

Molecular Epidemiology of Cryptosporidium spp. and Giardia spp. in Mussels (Mytilus californianus) and California Sea Lions (Zalophus californianus) from Central California

Cryptosporidium and Giardia are of public health importance, with recognized transmission through recreational waters. Therefore, both can contaminate marine waters and shellfish, with potential to infect marine mammals in nearshore ecosystems. A 2-year study was conducted to evaluate the presence of Cryptosporidium and Giardia in mussels located at two distinct coastal areas in California, namely, (i) land runoff plume sites and (ii) locations near sea lion haul-out sites, as well as in feces of California sea lions (CSL) (Zalophus californianus) by the use of direct fluorescent antibody (DFA) detection methods and PCR with sequence analysis. In this study, 961 individual mussel hemolymph samples, 54 aliquots of pooled mussel tissue, and 303 CSL fecal samples were screened. Giardia duodenalis assemblages B and D were detected in hemolymph from mussels collected near two land runoff plume sites (Santa Rosa Creek and Carmel River), and assemblages C and D were detected in hemolymph from mussels collected near a sea lion haul-out site (White Rock). These results suggest that mussels are being contaminated by protozoa carried in terrestrial runoff and/or shed in the feces of CSL. Furthermore, low numbers of oocysts and cysts morphologically similar to Cryptosporidium and Giardia, respectively, were detected in CSL fecal samples, suggesting that CSL could be a source and a host of protozoan parasites in coastal environments. The results of this study showed that Cryptosporidium and Giardia spp. from the feces of terrestrial animals and CSL can contaminate mussels and coastal environments.