UV irradiance effects on komodo dragon (Varanus komodoensis) vitamin D3, egg production, and behavior: A case study.

Modifications to UV irradiance for indoor housed herpetofauna can affect behavior and physiology. Low ultraviolet B (UVB) irradiance can result in vitamin D3 deficiency resulting in calcium metabolism disorders including metabolic bone disease and immune suppression. High UVB can result in skin and eye issues, which can be severe enough to cause shock and death. Using tools available for the assessment of UV light, including Ferguson zones and the UV working tool designed by the British and Irish Association of Zoos and Aquaria, we redesigned lighting in our indoor komodo dragon (Varanus komodoensis) habitat to better suit the UV requirements of this species, while studying changes in behavior and physiology. We measured serum vitamin 25-hydroxy D3 values in one male and one female komodo dragon before and after they were housed in indoor and outdoor habitats. We also measured behavior changes in our male komodo as he moved from an outdoor habitat, to an indoor habitat with changing UV irradiance. Our female komodo showed a 98% increase in vitamin D3 values after being moved outdoors, and laid her first clutch of eggs. Our male dragon's vitamin D3 remained consistent 200 days after moving inside. He did show increased activity when higher UV irradiance was available. Importantly, we found the UV lamps we used stopped producing desired UV irradiance within 3.5 months of regular use. We suggest all animal care facilities develop UV monitoring programs to research output and longevity of UVB lamps used in indoor herpetofauna habitats.

Out of Sight, Out of Mind or Just Something in the Way? Visual Barriers Do Not Reduce Intraspecific Agonism in an All-Male Group of Nile Crocodiles (Crocodylus niloticus).

Here, we evaluated if visual barriers could reduce intraspecific agonism in an all-male group of Nile crocodiles (Crocodylus niloticus) living in a zoo. Crocodiles were monitored for nearly 100 h, and four "hotspots" of aggression within their exhibit were identified. Within these four locations, visual barriers were placed at the surface of the water with the goal of reducing agonism by targeting sight lines associated with their species-typical minimum exposure posture, where crocodiles submerge their body but maintain facial sensory organs above the water line. Crocodile behavior was then monitored for 226 h, evaluating both short- and long-term effects of the visual barriers. In both observation periods, intraspecific agonism was unaffected by visual barriers. However, crocodiles were more likely to be on land and closer together, after the barriers were installed, showing the barriers affected nonagonistic behaviors. Monitoring of such unintended effects is significant to ensure no welfare concerns are created in any exhibit or husbandry modification attempt. Additionally, time of day and temperature were significant predictors of behavior, highlighting the importance of such factors in the analysis of reptilian behavior. While ineffective at reducing agonism, this is the first published study evaluating exhibit design and behavior of crocodilians in zoos and aquariums. The methodologies and findings here should provide useful information for future behavioral and welfare studies of this understudied taxa.

Wild Sri Lankan elephants retreat from the sound of disturbed Asian honey bees.

Asian elephants (Elephas maximus) are threatened primarily by habitat loss and human-elephant conflict. In addition to establishing protected areas and corridors for wildlife, empowering farmers to protect their crops is crucial for Asian elephant conservation [1,2]. Elephants can habituate to artificial deterrents, hence natural biological alternatives are of great interest [2,3]. African elephants (Loxodonta africana) avoid African honey bees (Apis mellifera scutellata), inspiring 'beehive fences' as a successful means of small-scale crop protection [4,5]. Here, we used a recording of a disturbed hive of cavity-dwelling Asian honey bees (Apis cerana indica) and conducted sound playbacks to 120 wild elephants in 28 different groups resting under trees in Uda Walawe National Park in Sri Lanka. Elephants responded by moving significantly further away from their resting site in bee playback trials compared to controls. Elephants also increased vocalization rates, as well as investigative and reassurance behaviours in response to bee sounds, but did not display dusting or headshaking behaviour.

Sound at the zoo: Using animal monitoring, sound measurement, and noise reduction in zoo animal management.

A clear need for evidence-based animal management in zoos and aquariums has been expressed by industry leaders. Here, we show how individual animal welfare monitoring can be combined with measurement of environmental conditions to inform science-based animal management decisions. Over the last several years, Disney's Animal Kingdom® has been undergoing significant construction and exhibit renovation, warranting institution-wide animal welfare monitoring. Animal care and science staff developed a model that tracked animal keepers' daily assessments of an animal's physical health, behavior, and responses to husbandry activity; these data were matched to different external stimuli and environmental conditions, including sound levels. A case study of a female giant anteater and her environment is presented to illustrate how this process worked. Associated with this case, several sound-reducing barriers were tested for efficacy in mitigating sound. Integrating daily animal welfare assessment with environmental monitoring can lead to a better understanding of animals and their sensory environment and positively impact animal welfare.

Walking Behavior of Zoo Elephants: Associations between GPS-Measured Daily Walking Distances and Environmental Factors, Social Factors, and Welfare Indicators.

Research with humans and other animals suggests that walking benefits physical health. Perhaps because these links have been demonstrated in other species, it has been suggested that walking is important to elephant welfare, and that zoo elephant exhibits should be designed to allow for more walking. Our study is the first to address this suggestion empirically by measuring the mean daily walking distance of elephants in North American zoos, determining the factors that are associated with variations in walking distance, and testing for associations between walking and welfare indicators. We used anklets equipped with GPS data loggers to measure outdoor daily walking distance in 56 adult female African (n = 33) and Asian (n = 23) elephants housed in 30 North American zoos. We collected 259 days of data and determined associations between distance walked and social, housing, management, and demographic factors. Elephants walked an average of 5.3 km/day with no significant difference between species. In our multivariable model, more diverse feeding regimens were correlated with increased walking, and elephants who were fed on a temporally unpredictable feeding schedule walked 1.29 km/day more than elephants fed on a predictable schedule. Distance walked was also positively correlated with an increase in the number of social groupings and negatively correlated with age. We found a small but significant negative correlation between distance walked and nighttime Space Experience, but no other associations between walking distances and exhibit size were found. Finally, distance walked was not related to health or behavioral outcomes including foot health, joint health, body condition, and the performance of stereotypic behavior, suggesting that more research is necessary to determine explicitly how differences in walking may impact elephant welfare.

Recumbence Behavior in Zoo Elephants: Determination of Patterns and Frequency of Recumbent Rest and Associated Environmental and Social Factors.

Resting behaviors are an essential component of animal welfare but have received little attention in zoological research. African savanna elephant (Loxodonta africana) and Asian elephant (Elephas maximus) rest includes recumbent postures, but no large-scale investigation of African and Asian zoo elephant recumbence has been previously conducted. We used anklets equipped with accelerometers to measure recumbence in 72 adult female African (n = 44) and Asian (n = 28) elephants housed in 40 North American zoos. We collected 344 days of data and determined associations between recumbence and social, housing, management, and demographic factors. African elephants were recumbent less (2.1 hours/day, S.D. = 1.1) than Asian elephants (3.2 hours/day, S.D. = 1.5; P < 0.001). Nearly one-third of elephants were non-recumbent on at least one night, suggesting this is a common behavior. Multi-variable regression models for each species showed that substrate, space, and social variables had the strongest associations with recumbence. In the African model, elephants who spent any amount of time housed on all-hard substrate were recumbent 0.6 hours less per day than those who were never on all-hard substrate, and elephants who experienced an additional acre of outdoor space at night increased their recumbence by 0.48 hours per day. In the Asian model, elephants who spent any amount of time housed on all-soft substrate were recumbent 1.1 hours more per day more than those who were never on all-soft substrate, and elephants who spent any amount of time housed alone were recumbent 0.77 hours more per day than elephants who were never housed alone. Our results draw attention to the significant interspecific difference in the amount of recumbent rest and in the factors affecting recumbence; however, in both species, the influence of flooring substrate is notably important to recumbent rest, and by extension, zoo elephant welfare.

Acoustic and behavioral repertoires of the hippopotamus (Hippopotamus amphibius).

This study describes the acoustic and behavioral repertoires of the common hippopotamus (Hippopotamus amphibius). Simultaneous audio and video recordings were collected of male and female hippos at Disney's Animal Kingdom(®). Visual inspection of spectrograms resulted in classifying signals into three main categories (burst of air, tonal, and pulsed) produced in-air, underwater, or simultaneously in both mediums. Of the total acoustic signals, most were produced underwater (80%), and the majority of the total signals were tonal (54%). Using multivariate analysis of the acoustic parameters, 11 signal types were described and differentiated. In the burst of air category, chuffs and snorts were distinguished by minimum and peak frequency, and bubble displays were described. In the tonal category, grunts, groans, screams, and whines were distinguished by several frequency measures (e.g., minimum, maximum, fundamental, peak frequency). Wheeze honks were tonal signals that often involved a chorus of overlapping calls. In the pulsed category, click trains, croaks, and growls were distinguished by frequency and duration. Video analysis demonstrated that chuffs, groans, and whines were associated with submissive contexts, while snorts, grunts, and growls were associated with dominance contexts. These results provide further information about the acoustic signals and concurrent behavior of hippos.

African elephant alarm calls distinguish between threats from humans and bees.

The Samburu pastoralists of Northern Kenya co-exist with African elephants, Loxodonta africana, and compete over resources such as watering holes. Audio playback experiments demonstrate that African elephants produce alarm calls in response to the voices of Samburu tribesmen. When exposed to adult male Samburu voices, listening elephants exhibited vigilance behavior, flight behavior, and produced vocalizations (rumbles, roars and trumpets). Rumble vocalizations were most common and were characterized by increased and more variable fundamental frequencies, and an upward shift in the first [F1] and second [F2] formant locations, compared to control rumbles. When exposed to a sequence of these recorded rumbles, roars and trumpets, listening elephants also exhibited vigilance and flight behavior. The same behavior was observed, in lesser degrees, both when the roars and trumpets were removed, and when the second formants were artificially lowered to levels typical of control rumbles. The "Samburu alarm rumble" is acoustically distinct from the previously described "bee alarm rumble." The bee alarm rumbles exhibited increased F2, while Samburu alarm rumbles exhibited increased F1 and F2, compared to controls. Moreover, the behavioral reactions to the two threats were different. Elephants exhibited vigilance and flight behavior in response to Samburu and bee stimuli and to both alarm calls, but headshaking behavior only occurred in response to bee sounds and bee alarm calls. In general, increasingly threatening stimuli elicited alarm calls with increases in F0 and in formant locations, and increasing numbers of these acoustic cues in vocal stimuli elicited increased vigilance and flight behavior in listening elephants. These results show that African elephant alarm calls differentiate between two types of threat and reflect the level of urgency of threats.

The vocal repertoire of the Key Largo woodrat (Neotoma floridana smalli).

The Key Largo woodrat (Neotoma floridana smalli) is an endangered rodent endemic to the island of Key Largo, FL. There is little information on vocal communication in this species and descriptions of the acoustic structure of calls are lacking. A captive breeding program was established as part of the recovery plan for the species, providing the opportunity to investigate the vocal repertoire and acoustic structure of calls in both wild and captive contexts. Audio and video recordings were conducted at the Crocodile Lake National Wildlife Refuge in Key Largo and at Disney's Animal Kingdom(®). Analysis of the acoustic structure of calls resulted in four provisional call types: "Tonal calls" consisted of "ultrasonic vocalizations" (40 kHz fundamental frequency, F(0)), "high squeaks" (10 kHz F(0)), and "squeaks" (1.8 kHz F(0)). "Noisy," broadband calls known as "raspy" vocalizations did not exhibit fundamental frequencies, but contained several prominent spectral peaks (from 9 to 40 kHz). The social contexts of vocal production showed that all four call types were associated with pup need or interactions between pups and dams, and that raspy vocalizations were associated with courtship and copulation. Adults without pups exhibited little or no vocal activity, which may result from solitary lifestyles and predator avoidance.

Measuring positive and negative affect in the voiced sounds of African elephants (Loxodonta africana).

As in other mammals, there is evidence that the African elephant voice reflects affect intensity, but it is less clear if positive and negative affective states are differentially reflected in the voice. An acoustic comparison was made between African elephant "rumble" vocalizations produced in negative social contexts (dominance interactions), neutral social contexts (minimal social activity), and positive social contexts (affiliative interactions) by four adult females housed at Disney's Animal Kingdom®. Rumbles produced in the negative social context exhibited higher and more variable fundamental frequencies (F(0)) and amplitudes, longer durations, increased voice roughness, and higher first formant locations (F1), compared to the neutral social context. Rumbles produced in the positive social context exhibited similar shifts in most variables (F(0 )variation, amplitude, amplitude variation, duration, and F1), but the magnitude of response was generally less than that observed in the negative context. Voice roughness and F(0) observed in the positive social context remained similar to that observed in the neutral context. These results are most consistent with the vocal expression of affect intensity, in which the negative social context elicited higher intensity levels than the positive context, but differential vocal expression of positive and negative affect cannot be ruled out.

Bee threat elicits alarm call in African elephants.

Unlike the smaller and more vulnerable mammals, African elephants have relatively few predators that threaten their survival. The sound of disturbed African honeybees Apis meliffera scutellata causes African elephants Loxodonta africana to retreat and produce warning vocalizations that lead other elephants to join the flight. In our first experiment, audio playbacks of bee sounds induced elephants to retreat and elicited more head-shaking and dusting, reactive behaviors that may prevent bee stings, compared to white noise control playbacks. Most importantly, elephants produced distinctive "rumble" vocalizations in response to bee sounds. These rumbles exhibited an upward shift in the second formant location, which implies active vocal tract modulation, compared to rumbles made in response to white noise playbacks. In a second experiment, audio playbacks of these rumbles produced in response to bees elicited increased headshaking, and further and faster retreat behavior in other elephants, compared to control rumble playbacks with lower second formant frequencies. These responses to the bee rumble stimuli occurred in the absence of any bees or bee sounds. This suggests that these elephant rumbles may function as referential signals, in which a formant frequency shift alerts nearby elephants about an external threat, in this case, the threat of bees.

Vocal communication in African elephants (Loxodonta africana).

Research on vocal communication in African elephants has increased in recent years, both in the wild and in captivity, providing an opportunity to present a comprehensive review of research related to their vocal behavior. Current data indicate that the vocal repertoire consists of perhaps nine acoustically distinct call types, "rumbles" being the most common and acoustically variable. Large vocal production anatomy is responsible for the low-frequency nature of rumbles, with fundamental frequencies in the infrasonic range. Additionally, resonant frequencies of rumbles implicate the trunk in addition to the oral cavity in shaping the acoustic structure of rumbles. Long-distance communication is thought possible because low-frequency sounds propagate more faithfully than high-frequency sounds, and elephants respond to rumbles at distances of up to 2.5 km. Elephant ear anatomy appears designed for detecting low frequencies, and experiments demonstrate that elephants can detect infrasonic tones and discriminate small frequency differences. Two vocal communication functions in the African elephant now have reasonable empirical support. First, closely bonded but spatially separated females engage in rumble exchanges, or "contact calls," that function to coordinate movement or reunite animals. Second, both males and females produce "mate attraction" rumbles that may advertise reproductive states to the opposite sex. Additionally, there is evidence that the structural variation in rumbles reflects the individual identity, reproductive state, and emotional state of callers. Growth in knowledge about the communication system of the African elephant has occurred from a rich combination of research on wild elephants in national parks and captive elephants in zoological parks.

GPS assessment of the use of exhibit space and resources by African elephants (Loxodonta africana).

In public discussions of animal rights and welfare, we as members and proponents of zoological institutions often face significant challenges addressing the concerns of our detractors due to an unfortunate deficiency in systematically collected and published data on the animals in our collections. In the case of elephants, there has been a paucity of information describing their use of space within captive environments. Here, using collar-mounted GPS recording devices, we documented the use of exhibit space and resources by a herd of five adult female African elephants (Loxodonta africana) housed at Disney's Animal Kingdom((R)). We found that dominant animals within the herd used a greater percentage of the available space and subordinate females avoided narrow or enclosed regions of the enclosure that we termed "restricted flow areas." In their use of other resources, dominant females demonstrated increased occupation of the watering hole over subordinate females, but all females demonstrated relatively equivalent use of the mud wallow. Overall, our results provide preliminary evidence that position within the dominancy hierarchy impacts the percentage of space occupied in a captive setting and may contribute to resource accessibility. These findings can be applied to future decisions on exhibit design and resource distribution for this species.

The expression of affect in African elephant (Loxodonta africana) rumble vocalizations.

Affective states are thought to be expressed in the mammalian voice, but such investigations are most common in primates. Source and filter features of rumbles were analyzed from 6 adult female African elephants (Loxodonta africana) at Disney's Animal Kingdom. Rumbles produced during periods of minimal social interaction ("low affect") were compared to those produced during dominance interactions ("high affect"). Low-ranking females produced rumbles with increased and more variable fundamental frequencies, and increased durations and amplitudes during dominance interactions with superiors, compared to the low affect context. This acoustic response is consistent with the expression of affect in mammals and may signal submission to superiors. The 2 highest ranking females were codominant and competed for alpha status. They produced rumbles with decreased and less variable fundamental frequencies, increased durations and amplitudes, and a decrease in formant dispersion during dominance interactions with each other, compared to the low affect context. This response is not generally consistent with the expression of affect, but may signal large body size to competitors. These results suggest that affect can be expressed in the voiced sounds of elephants.

GPS determination of walking rates in captive African elephants (Loxodonta africana).

The movements of elephants in captivity have been an issue of concern for animal welfare activists and zoological professionals alike in recent years. In order to fully understand how movement rates reflect animal welfare, we must first determine the exact distances these animals move in the captive environment. We outfitted seven adult female African elephants (Loxodonta africana) at Disney's Animal Kingdom with collar-mounted global positioning recording systems to document their movement rates while housed in outdoor guest viewing habitats. Further, we conducted preliminary analyses to address potential factors impacting movement rates including body size, temperature, enclosure size, and social grouping complexity. We found that our elephants moved at an average rate of 0.409+/-0.007 km/hr during the 9-hr data collection periods. This rate translates to an average of 3.68 km traveled during the observation periods, at a rate comparable to that observed in the wild. Although movement rate did not have a significant relationship with an individual's body size in this herd, the movements of four females demonstrated a significant positive correlation with temperature. Further, females in our largest social group demonstrated a significant increase in movement rates when residing in larger enclosures. We also present preliminary evidence suggesting that increased social group complexity, including the presence of infants in the herd, may be associated with increased walking rates, whereas factors such as reproductive and social status may constrain movements.

How costly are ejaculates for Japanese macaques?

Much sexual selection theory is based on the idea that ejaculate is cheap. Since further details are unknown our aim was to determine the energy that primate males require for ejaculate production. We addressed this problem by measuring the energy content (in kJ) of ejaculates from Japanese macaques (Macaca fuscata) using standard bomb calorimetry. Then, we estimated the relative amount of energy that individuals require for ejaculate production by relating the net energy content of ejaculates to males' daily basal metabolic rate (BMR). Fresh macaque ejaculate contains 3.0 kJ ml(-1). Assuming a mean volume of 2.7 ml an average macaque ejaculate contains 8.1 kJ. Depending on the individuals' body mass (6-13 kg) and the number and volume of the ejaculates, macaque males are assumed to use between at least 0.8% and at most 6.0% of their BMR for ejaculate production per day during the breeding season. Even when regarding only the minimal energy investment of 0.8% of daily BMR for ejaculate production, clearly ejaculates come with some cost for primate males.

Urinary prolactin is correlated with mothering and allo-mothering in squirrel monkeys.

The hormone prolactin is implicated in infant care-giving by parents and allo-parents in a variety of species. Adult female squirrel monkeys (Saimiri spp.) engage in allo-mothering behavior, which includes carrying and nursing infants, but communal care of offspring has not been investigated from an endocrine standpoint in this taxon. We attempted to fill this gap by examining prolactin levels in squirrel monkeys (Saimiri sciureus) as a function of parental responsiveness. Subjects were housed at the National Institutes of Health Animal Center and assays were performed at the Wisconsin National Primate Research Center. To test for the presence of prolactin in squirrel monkey, saliva, blood and saliva were simultaneously collected from anesthetized subjects during routine health examinations. Prolactin was detectable in serum but not in saliva samples. In the core investigation, behavioral data were collected by focal animal sampling on three 1-male multi-female groups, and individually identified urine was collected non-invasively from foil containers underneath group cages on a daily basis throughout the behavioral study. Changes in urinary prolactin over time reflected changes in the reproductive state of a female who was pregnant, gave birth and lactated during the study. Mean urinary prolactin levels in non-lactating females and a male housed with infants in one group were higher than in adults from 2 groups without infants. In the group with infants, mean urinary prolactin levels in adults increased with the amount of infant contact and care-giving. The squirrel monkey may represent a new primate model for investigating the endocrinology of infant care-giving.

The signal functions of early infant crying.

In this article I evaluate recent attempts to illuminate the human infant cry from an evolutionary perspective. Infants are born into an uncertain parenting environment, which can range from indulgent care of offspring to infanticide. Infant cries are in large part adaptations that maintain proximity to and elicit care from caregivers. Although there is not strong evidence for acoustically distinct cry types, infant cries may function as a graded signal. During pain-induced autonomic nervous system arousal, for example, neural input to the vocal cords increases cry pitch. Caregivers may use this acoustic information, together with other cues, to guide caregiving behavior. Serious pathology, on the other hand, results in chronically and severely abnormal cry acoustics. Such abnormal crying may be a proximate cause of adaptive infant maltreatment, in circumstances in which parents cut their losses and reduce or withdraw investment from infants with low survival chances. An increase in the amount of crying during the first few months of life is a human universal, and excessive crying, or colic, represents the upper end of this normal increase. Potential signal functions of excessive crying include manipulation of parents to acquire additional resources, honest signaling of need, and honest signaling of vigor. Current evidence does not strongly support any one of these hypotheses, but the evidence is most consistent with the hypothesis that excessive early infant crying is a signal of vigor that evolved to reduce the risk of a reduction or withdrawal of parental care.

Adult cortisol response to immature offspring play in captive squirrel monkeys.

Variable environmental and social conditions influence hypothalamic-pituitary-adrenal activity in captive animals. Socially separated and individually housed animals generally experience increased cortisol secretion compared to animals housed with conspecifics, and social companionship can buffer the stress response when exposed to challenges such as introduction to novel environments. Nevertheless, the presence of conspecifics may also be the cause of stress because social dynamics impact individuals. Squirrel monkeys (Saimiri spp.) readily form same-sex affiliative social relationships, but in captivity, the presence of immature offspring severely disrupts affiliative associations among adults. We examined behavioral and physiological effects of the presence of immature offspring on adults by comparing two groups of adults with immature offspring to an all-adult group. We conducted behavioral observations and collected urine from adult members, and urine was assayed for cortisol at the Wisconsin National Primate Research Center. Adults in groups with immature offspring received an average of 18 play attempts per hour from the offspring, experienced a fivefold decrease in adult affiliation, and showed higher urinary cortisol levels compared to the all-adult group. A principal components analysis showed that adults characterized by receiving play attempts, rejecting play attempts, and lacking affiliative contact with other adults showed the highest mean urinary cortisol levels. Further analyses demonstrated that the persistent play attempts by immature offspring, not the resulting lack of adult huddling, were primarily responsible for the observed increase in urinary cortisol levels. Taken together, these data suggest that the disruptive effect of immature offspring produces a chronic cortisol increase in captive adult squirrel monkeys.