Large Outdoor Enclosure Research Articles

Parentage assignment reveals multiple paternity in the critically-endangered Guatemalan beaded lizard (Heloderma charlesbogerti)

Within captive management programs for species of conservation concern, understanding the genetic mating system is of fundamental importance, given its role in generating and maintaining genetic diversity and promoting opportunities for sperm competition. If a goal of a conservation program is reintroduction, knowledge of the mating system may also inform prediction models aimed at understanding how genetic diversity may be spatially organized, thus informing decisions regarding where and which individuals should be released to maximize genetic diversity in the wild population. Within captive populations, such information may also influence how animals are maintained in order to promote natural behaviors. Here we investigate the genetic mating system of the Guatemalan beaded lizard, Heloderma charlesbogerti, a member of an entire clade lacking such information. A group of adult male and female H. charlesbogerti co-habited a large outdoor enclosure for five years during the species’ perceived breeding season. Through genomic parentage analysis, 50% of clutches comprising multiple offspring were found to result from multiple paternity, with up to three males siring offspring within single clutches. Both males and females were observed to produce offspring with multiple partners within a given year. As such, within this captive environment, where opportunities existed for mating with multiple partners, the genetic mating system was found to be highly polygamous, with multiple paternity common within clutches. These findings are novel for the family Helodermatidae, and the results have broader implications about how reproductive opportunities should be managed within captive conservation programs.

Improved nutritional status may promote an “asset protection” reproductive strategy in male rock lizards

AbstractInvesting in the current reproduction requires diverting energy resources from other metabolic functions, which may compromise future reproduction and lifespan. To solve this trade-off, an individual may consider its labile state to decide how much to invest in current reproduction. We tested experimentally whether the “state quality” of male rock lizards influences their reproductive strategies. To improve the nutritional status of males before the mating season, we captured and supplemented experimental males (N = 20) with dietary vitamin D3 (an essential nutrient for lizards) and had a control group of males (N = 20). Then, we released all these males and females (N = 31) in a large semi-natural outdoor enclosure where lizards could interact and mate freely during the mating period. Activity levels of males did not vary between treatments, but supplemented males started fewer intrasexual agonistic interactions and made fewer mating advances to females. When the mating season ended, we incubated eggs laid by females to obtain the offspring and estimated the paternity of males using DNA microsatellites. Supplemented males sired fewer offspring than control males. These results suggest that vitamin D3 supplemented males used a low risk/less costly mating strategy to protect their assets (i.e., vitamin D reserves), but that still resulted in “some” current reproductive success, while likely increasing longevity and the expected future total reproductive success.

Sleep Time in the European Starling Is Strongly Affected by Night Length and Moon Phase.

Sleep is considered to be of crucial importance for performance and health, yet much of what we know about sleep is based on studies in a few mammalian model species under strictly controlled laboratory conditions. Data on sleep in different species under more natural conditions may yield new insights in the regulation and functions of sleep. We therefore performed a study with miniature electroencephalogram (EEG) data loggers in starlings under semi-natural conditions, group housed in a large outdoor enclosure with natural temperature and light. The birds showed a striking 5-h difference in the daily amount of non-rapid-eye-movement (NREM) sleep between winter and summer. This variation in the amount of NREM sleep was best explained by night length. Most sleep occurred during the night, but when summer nights became short, the animals displayed mid-day naps. The decay of NREM sleep spectral power in the slow-wave range (1.1-4.3Hz) was steeper in the short nights than in the longer nights, which suggests that birds in summer have higher sleep pressure. Additionally, sleep was affected by moon phase, with 2h of NREM sleep less during full moon. The starlings displayed very little rapid-eye-movement (REM) sleep, adding up to 1.3% of total sleep time. In conclusion, this study demonstrates a pronounced phenotypical flexibility in sleep in starlings under semi-natural conditions and shows that environmental factors have a major impact on the organization of sleep and wakefulness.

Does intraspecific competition among Allenby’s gerbils lead to an Ideal Free Distribution across foraging patches?

Employing the Ideal Free Distribution (IFD) principle as a tool, we investigated how Allenby’s gerbils (Gerbillus andersoni allenbyi) utilized food patches within and moved between connected quadrants (i.e., ‘habitats’) in a large outdoor semi-natural enclosure. These habitats differed in initial forager densities, but provided equal numbers of standardized food patches that provided equal rewards (i.e. food) and costs (i.e. predation risk, metabolic, and missed opportunity). We quantified the gerbils’ giving-up-densities (GUDs) within foraging patches and recorded their daily distribution between habitats. Individual gerbils were tagged with unique bar-coded numbers to compare their locations within and across habitats. The mean number of gerbil foragers (9.1 and 8.9 individuals, respectively) and GUDs evened out across habitats over time. Despite this, the distribution of gerbils did not remain static within foraging patches; instead, gerbils altered their use of patches across and within habitats on a nightly basis. This may be due to a combination of factors including, high levels of interference competition between foragers at patches, a lag effect before the gerbils perceived changes in competition intensity with the arrival and departure of individuals, and gerbils having imperfect knowledge of their environment. Furthermore, the pattern of microhabitat (open vs bush patches) use by gerbils differed over time, indicating that despite the distribution of gerbils and their GUDs evening out between habitats, they still preferred foraging from safer bush patches over riskier open patches. This study provides insights into how under low predation risk, strong levels of intraspecific competition can shape the distribution of foragers across and within habitats.

Light pollution affects space use and interaction of two small mammal species irrespective of personality

BackgroundArtificial light at night (ALAN) is one form of human-induced rapid environmental changes (HIREC) and is strongly interfering with natural dark–light cycles. Some personality types within a species might be better suited to cope with environmental change and therefore might be selected upon under ongoing urbanization.ResultsWe used LED street lamps in a large outdoor enclosure to experimentally investigate the effects of ALAN on activity patterns, movement and interaction of individuals of two species, the bank vole (Myodes glareolus) and the striped field mouse (Apodemus agrarius). We analyzed effects combined with individual boldness score. Both species reduced their activity budget during daylight hours. While under natural light conditions home ranges were larger during daylight than during nighttime, this difference vanished under ALAN. Conspecifics showed reduced home range overlap, proximity and activity synchrony when subjected to nighttime illumination. Changes in movement patterns in reaction to ALAN were not associated with differences in boldness score of individuals.ConclusionsOur results suggest that light pollution can lead to changes in movement patterns and individual interactions in small mammals. This could lead to fitness consequences on the population level.

How moths escape bats: predicting outcomes of predator-prey interactions.

What determines whether fleeing prey escape from attacking predators? To answer this question, biologists have developed mathematical models that incorporate attack geometries, pursuit and escape trajectories, and kinematics of predator and prey. These models have rarely been tested using data from actual predator-prey encounters. To address this problem, we recorded multi-camera infrared videography of bat-insect interactions in a large outdoor enclosure. We documented 235 attacks by four Myotis volans bats on a variety of moths. Bat and moth flight trajectories from 50 high-quality attacks were reconstructed in 3-D. Despite having higher maximum velocity, deceleration and overall turning ability, bats only captured evasive prey in 69 of 184 attacks (37.5%); bats captured nearly all moths not evading attack (50 of 51; 98%). Logistic regression indicated that prey radial acceleration and escape angle were the most important predictors of escape success (44 of 50 attacks correctly classified; 88%). We found partial support for the turning gambit mathematical model; however, it underestimated the escape threshold by 25% of prey velocity and did not account for prey escape angle. Whereas most prey escaping strikes flee away from predators, moths typically escaped chasing bats by turning with high radial acceleration toward 'safety zones' that flank the predator. This strategy may be widespread in prey engaged in chases. Based on these findings, we developed a novel geometrical model of predation. We discuss implications of this model for the co-evolution of predator and prey kinematics and pursuit and escape strategies.

Effect of weather conditions and presence of visitors on adrenocortical activity in captive African penguins (Spheniscus demersus)

A number of potential stressors are present in captive environments and it is critically important to identify them in order to improve health and welfare in ex situ animal populations. In this study, we investigated the adrenocortical activity of a colony of African penguins hosted in an immersive zoo in Italy, with respect to the presence of visitors and local microclimatic conditions, using the non-invasive method of assessing faecal glucocorticoid metabolites (FGMs). The penguins’ exhibit is a large naturalistic outdoor enclosure, which closely reproduces the natural habitat of this species. Data collection took place from the beginning of June to the end of August 2014, during the period of maximum flow of visitors. We carried out 12 sampling periods, each involving 2 consecutive days; during the first day we counted the visitors and we registered the meteorological data, and on the second day, we collected the faecal samples, which amounted to a total of 285 faecal samples. Our results showed that the number of visitors did not influence the adrenocortical activity of the African penguins. Conversely, the local microclimatic conditions did influence the physiological stress on these birds. We found that an increase of the daily mean temperature induced a significant increase in FGM concentrations, although humidity and wind speed had a moderating effect on temperature and reduced the heat-induced stress. Moreover, we calculated two climatic indices, commonly used to assess the thermal discomfort in animals, namely the THI (Temperature-Humidity Index) and WCI (Wind Chill Index), and we detected a positive relationship between their values and the FGM levels, demonstrating that these indices could be useful indicators of weather discomfort in African penguins. Our study shows that the simulating naturalistic conditions could have significant benefits for zoo animals, such as reducing the negative effect of visitors. Nevertheless, it should be taken into account where the zoological facility is located and if the local microclimatic conditions are compatible with the hosted species, to ensure that they do not differ greatly from their natural habitat.

Evidence of individual odors and individual discrimination in the raccoon,Procyon lotor

Abstract Although raccoons (Procyon lotor) were originally categorized as solitary carnivores, recent evidence shows that some raccoons have overlapping home ranges, travel in groups, and share dens. Moreover, raccoons use communal latrines and scent mark, suggesting that chemical signals may be important for communication. Using a familiarization–discrimination technique we investigated whether raccoons can discriminate individual differences in the odors of conspecific urine or feces. The subjects were wild caught (n = 10 raccoons for urine experiments; n = 8 raccoons for feces experiments) and tested in a large outdoor enclosure. We demonstrated that raccoons can distinguish individual differences in the odor of unfamiliar and unrelated conspecific urine, but not in the odor of feces. Gas chromatography was also done on the urine samples to look for chemical differences. The gas chromatograms showed visible differences and qualitative as well as quantitative differences in chemical composition. This is...

Social Dominance Is Associated with Individual Differences in Heart Rate and Energetic Response to Food Restriction in Female Red Deer

Energy expenditure is a key mechanism underlying animal ecology, yet why individuals often differ in metabolic rate even under identical conditions remains largely unexplained. Individual variation in metabolism might be explained by correlations with other behavioral and physiological traits, with individual syndromes having environment- or state-dependent costs and benefits to fitness. We tested whether social rank within herds of female red deer is associated with individual differences in resting heart rate, an index of metabolic rate, and energetic response to monthly periods of food restriction during winter in a large outdoor enclosure near Vienna, Austria. Social rank had a strong positive effect on average daily heart rate, independent of the effects of food intake, air temperature, body temperature, and body mass. Subordinate individuals had lower heart rates than dominants, and consequently they suffered lower rates of body mass loss during periods of restricted pellet food supply. A greater capacity to minimize energy requirements might benefit the survival of subdominant female red deer during periods of negative energy balance in winter. Our study provides empirical support in a large mammal for linkages in behavior and metabolism within individuals that have environment-dependent consequences to the energy budget.

Chimpanzees and bonobos exhibit divergent spatial memory development

Spatial cognition and memory are critical cognitive skills underlying foraging behaviors for all primates. While the emergence of these skills has been the focus of much research on human children, little is known about ontogenetic patterns shaping spatial cognition in other species. Comparative developmental studies of nonhuman apes can illuminate which aspects of human spatial development are shared with other primates, versus which aspects are unique to our lineage. Here we present three studies examining spatial memory development in our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (P. paniscus). We first compared memory in a naturalistic foraging task where apes had to recall the location of resources hidden in a large outdoor enclosure with a variety of landmarks (Studies 1 and 2). We then compared older apes using a matched memory choice paradigm (Study 3). We found that chimpanzees exhibited more accurate spatial memory than bonobos across contexts, supporting predictions from these species' different feeding ecologies. Furthermore, chimpanzees - but not bonobos - showed developmental improvements in spatial memory, indicating that bonobos exhibit cognitive paedomorphism (delays in developmental timing) in their spatial abilities relative to chimpanzees. Together, these results indicate that the development of spatial memory may differ even between closely related species. Moreover, changes in the spatial domain can emerge during nonhuman ape ontogeny, much like some changes seen in human children.

The p66Shc knockout mice are short lived under natural condition

Deletion of the p66(Shc) gene results in lean and healthy mice, retards aging, and protects from aging-associated diseases, raising the question of why p66(Shc) has been selected, and what is its physiological role. We have investigated survival and reproduction of p66(Shc)-/- mice in a population living in a large outdoor enclosure for a year, subjected to food competition and exposed to winter temperatures. Under these conditions, deletion of p66(Shc) was strongly counterselected. Laboratory studies revealed that p66(Shc)-/- mice have defects in fat accumulation, thermoregulation, and reproduction, suggesting that p66(Shc) has been evolutionarily selected because of its role in energy metabolism. These findings imply that the health impact of targeting aging genes might depend on the specific energetic niche and caution should be exercised against premature conclusions regarding gene functions that have only been observed in protected laboratory conditions.

Olfactory Attraction of the Larval Parasitoid,Hyposoter horticola, to Plants Infested with Eggs of the Host Butterfly,Melitaea cinxia

Parasitoids locate inconspicuous hosts in a heterogeneous habitat using plant volatiles, some of which are induced by the hosts. Hyposoter horticola Gravenhost (Hymenoptera: Ichneumonidae) is a parasitoid of the Glanville fritillary butterfly Melitaea cinxia L. (Lepidoptera: Nymphalidae). Melitaea cinxia lays eggs in clusters on leaves of Plantago lanceolata L. (Lamiales: Plantaginaceae) and Veronica spicata L. (Lamiales: Plantaginaceae). The parasitoid oviposits into host larvae that have not yet hatched from the egg. Thus, though H. horticola is a parasitoid of Melitaea cinxia larvae, it must find host eggs on plants that have not been fed on by the larvae. Using a Y-tube olfactometer, the response of H. horticola to odors of Melitaea cinxia and extracts of the attacked plant species were tested. Three week-old eggs (near hatching) were attractive to young H. horticola, but one week-old eggs were attractive only to old or experienced H. horticola. Melitaea cinxia larvae were not attractive. A water extract of P. lanceolata was attractive, but ethanol or hexane extracts were not. None of the extracts of V. spicata were attractive. Leaves of V. spicata were attractive only if harboring eggs, but P. lanceolata leaves with eggs were not. Free flying H. horticola in a large outdoor enclosure were presented with host and plant cues. As in the olfactometer, V. spicata was attractive only when eggs were on it, and P. lanceolata was somewhat attractive with or without eggs. This study shows for the first time that a parasitoid of larvae uses egg volatiles or oviposition-induced plant volatiles, to find host larvae, and that Melitaea cinxia eggs or traces of oviposition induce the production of these volatiles by the plant. Based on the results, and given the natural distribution of the plants and M. cinxia eggs, parasitism of Melitaea cinxia eggs on P. lanceolata would be expected to be low. Instead, under natural conditions, a fraction of the eggs in virtually all egg clusters are parasitized on both plant species. The mismatch between the experimental results and the natural pattern of host-parasitoid interactions is discussed in terms of the expected coupling foraging cues with foraging success.

Role of male‐biased dispersal in inbreeding avoidance in the grey‐sided vole (Myodes rufocanus)

Effects of male-biased dispersal on inbreeding avoidance were investigated in a semi-natural population of Myodes (formerly Clethrionomys) rufocanus using a large outdoor enclosure (3 ha). Parentage of 918 voles weaned from 215 litters and relatedness of mates were analysed using microsatellite loci, and dispersal distances were obtained from mark-recapture live-trapping data. Natal and breeding male-biased dispersal was observed. There remained, however, chances that incestuous mating could occur, because not all males dispersed from their natal site, and 51 matings occurred between relatives (relatedness r > 0). The number of weaned juveniles from inbred litters was significantly smaller than that from non-inbred litters. Fourteen incestuous matings occurred between close relatives (r >or= 0.25), most of which were those between non-littermate maternal half siblings (four cases) and those between paternal half siblings (seven cases). When comparing the observed frequencies to the expected ones generated by combining every oestrous female with a male randomly chosen from her surroundings, the observed values for inbreeding of r >or= 0.25 were significantly smaller than the expectations, while no difference was observed for inbreeding of 0 < r < 0.25. These results suggest that male-biased dispersal is partly effective to avoid incestuous mating, but it does not provide complete separation of male and female close relatives. Additional mechanisms such as kin discrimination based on familiarity may work in inbreeding avoidance of the vole.

With a Little Help from a Friend

An old female, named Peony, spends her days with other chimpanzees in a large outdoor enclosure near Atlanta, Georgia (United States). On bad days, when her arthritis is acting up, she has great trouble walking and climbing. But other females help her out. For example, Peony is huffing and puffing to get up into the climbing frame in which several chimpanzees have gathered for a grooming session. An unrelated younger female moves behind her, places both hands on her ample behind, and pushes her up with quite a bit of effort, until Peony joins the rest.

The structure of social relationships among captive female giraffe (Giraffa camelopardalis).

Giraffe herds have been characterized as random associations of individuals, but recent evidence suggests giraffe have a more complex social structure. The authors formulated 3 hypotheses designed to evaluate whether a herd of captive giraffe (Giraffa camelopardalis) associated randomly or patterned their behavior and proximity in a manner indicative of social relationships. Affiliative interaction, proximity, and nearest neighbors for 6 captive female giraffe living in a large outdoor enclosure were analyzed, and all three measures were nonrandomly distributed, indicating female giraffe had social preferences. Furthermore, preferences were consistent across measures and time, suggesting that adult female giraffe maintain relationships. Mother-daughter pairs and pairs with large age differences between members interacted and associated most often. The social structure of this captive herd is influenced by social relationships between individual adult females, and the social behavior of individual females should be examined more closely in the wild.

Sociosexual behavior, male mating tactics, and the reproductive cycle of giraffe Giraffa camelopardalis

Female distribution exerts a major impact on male mating tactics. Giraffe cows have a reproductive cycle, and a social system, that should favor a male roaming reproductive tactic. We conducted a 2-year study of female Rothschild's giraffe (G. c. rothschildi) reproductive endocrinology in order to characterize attributes of the reproductive cycle and investigate how female endocrine and behavioral cues influence mating activity. We used non-invasive fecal steroid methods to determine reproductive state among females residing in a herd in a large outdoor enclosure. We found that females had an estrous cycle of 14.7 days and that they regularly had multiple ovarian cycles prior to conception. Adult males were more likely to associate with, and sexually investigate, females when they were cycling than when they were either pregnant or acyclic. During the estrous cycle, male–female proximity and sociosexual behavior were more pronounced during the probable fertile phase than the rest of the cycle. Sexual activity between giraffe coincided with the periovulatory period, with male interest in females peaking during the fertile window in the absence of proceptive behavior by females. We conclude that males detect reliable cues revealing female reproductive status and partition their reproductive effort in response to such cues. We propose that male giraffe adopt a roaming reproductive strategy with their large size, enabling them to search for and mate guard fertile females while minimizing metabolic costs.

Fecal steroid analysis of female giraffe ( Giraffa camelopardalis) reproductive condition and the impact of endocrine status on daily time budgets

Gestation and lactation can impose substantial energetic costs on female mammals. We developed a non-invasive means to determine reproductive condition in female giraffe using fecal steroid analysis. Giraffe may be especially challenged during their reproductive cycle because of two characteristics: they are impregnated while lactating and they do not breed seasonally. We studied the social behavior and endocrinology of seven female giraffe in a large naturalistic outdoor enclosure in order to chart connections between maternal physiology and behavior across the reproductive cycle. We found that giraffe gestation averages 448 days among females producing a calf that survived, with fecal pregnane concentrations reaching a zenith during the last trimester of pregnancy. Resumption of ovarian cyclicity following parturition was accelerated after neonatal calf mortality, but ovarian cycles resumed as early as 39 days postparturition while nursing. Although time spent feeding was unaffected by reproductive state, pregnant females significantly reduced time allocated to social behavior and had a tendency to locomote less than when cycling or acyclic. We suggest that modifications in foraging strategies as a function of reproductive state among wild giraffe derive from antipredator activity rather than from metabolic demands. Female giraffe probably cope with simultaneous lactation and gestation by producing high quality milk for neonatal calves commensurate with slow fetal growth and accelerating fetal growth simultaneous with weaning of nursing calves.

Reproduction of the Critically Endangered Anegada Island iguanaCyclura pinguisat San Diego Zoo

Details are given of the first reproduction of the Critically Endangered Anegada Island iguana Cyclura pinguis at a zoological facility. Two pairs of iguanas were housed indoors in enclosures measuring 3.6 m × 3 m × 2.4 m high and an additional pair was kept in a large outdoor semi-circle display enclosure measuring 12.1 m × 10.6m. Annual average temperature in the indoor enclosures ranged between 16.1 and 31.5°C, with temperature at each of the basking spots (two per enclosure) reaching as high as 65.5°C on the substrate surface. For fertile, unbroken eggs that hatched, failed to hatch or are still incubating (n= 25), average egg mass was 73.1 +4.5 g and average egg length and width were 6.9 × 0.4 cm and 4.4 × 0.7 cm, respectively. Eggs were incubated on perlite and water (at a ratio of 1:1 by mass) or vermiculite and water (at a ratio of 0.75:1 by mass), at a temperature of 30–30×2°C. Ten eggs hatched after an average incubation period of 88.1×4.1 days. Hatchlings averaged 49.4×12.8g mass and 9.7×0.4 cm SVL (snout-vent length). Average growth rates for the first 6 months were recorded as 0.67 g/day (mass) and 0.02 mm SVL/day (n= 7).

Vigilance as a measure of fear in dairy cattle

Wild animals increase vigilance at the expense of feeding time in response to predation risk or threats from conspecifics. Increased vigilance may therefore indicate increased fear. We tested dairy cattle to determine whether time spent vigilant changed in response to the novelty of their location, the presence of a dog or the presence of an aversive, gentle or unfamiliar handler. We conducted 12 3 min trials per cow on 40 cows tested individually in a large outdoor enclosure containing an attractive food source. The feeders restricted the animal’s view so that it could not feed and scan simultaneously, so vigilance time was defined as any time the animal’s head was raised. During the initial trials, the degree of vigilance was high, but the amount of vigilance decreased significantly with number of trials. Time vigilant was significantly higher in the presence of a dog than in the presence of a human or when neither was present. In a second experiment, 20 cows, that had been trained to recognise an aversive and a gentle person for 3 weeks prior to testing, were tested in an indoor pen containing an attractive food source with the aversive, gentle, or an unfamiliar person nearby. The presence of the aversive person significantly increased vigilance time compared to the unfamiliar and gentle people. However, vigilance time did not decrease with repeated exposure to the enclosure, perhaps because the testing barn was already familiar. These results suggest that cows alter their vigilance according to their degree of fearfulness toward people and toward different environments, and that measures of vigilance may provide information on the degree of fearfulness of the animals.

289 In vitro effects of preserved or unpreserved antiglaucoma drugs on apoptotic marker expression by human trabecular cells

This study compares the effects of orbitofrontal and temporal neocortical lesions on the integration and expression of grooming, huddling, and spatial relationships in vervet monkeys (Cercopithecus aethiops sabaeus). Two groups of socially living vervet monkeys were observed in a large outdoor enclosure. Nine members (four male and five female) of one group received orbitofrontal lesions and seven members of the other group (four male and three female) were subjected to temporal neocortical lesions. Unoperated control subjects, matched for age, gender, and rank, received sham operations. Animals with orbitofrontal lesions groomed less, huddled less, and were less likely to be within 1 m of their nearest neighbor. Animals with temporal neocortical lesions also groomed less, but their huddling behavior and spatial relationships were not altered. These data suggest that when a single species of Old World monkey is observed in a similar setting using comparable behavioral units, the effects of orbitofrontal and temporal neocortical lesions on affiliative behaviors can be dissociated.