Noninvasive evaluations of hormones can contribute to the assessment of health and welfare of animals. Variations in insulin levels and sensitivity, for example, have been linked to health concerns in non-human and human primates including insulin resistance, diabetes, and heart disease, the leading cause of death in zoo-housed gorillas. Few published studies have assessed insulin concentrations in western lowland gorillas (Gorilla gorilla gorilla), and all did so using serum. Anesthesia is typically required to collect blood samples from zoo-housed gorillas, limiting sampling frequency and restricting samples to the fasted state. The ability to measure insulin levels in saliva would eliminate these constraints and provide a minimally invasive means for monitoring this hormone. The purpose of this study was to analytically and biologically validate the measurement of insulin in saliva of western lowland gorillas using a commercially available enzyme immunoassay. For validation, an oral sugar test was conducted on five adult gorillas residing at Cleveland Metroparks Zoo. Such assessments are common practice in both human and equine medicine to evaluate the body's insulin response to ingestion of sugars. The test involved measuring salivary insulin at timed intervals before and after gorillas consumed doses of sugar. Salivary insulin levels increased from 15 min post-sugar ingestion and peaked after 90 to 120 min. One female had a high response and peaked at 990.21 mU/L. The other four gorillas had peaks between 49.82 and 167.04 mU/L. The assessment provided a biological validation for the measurement of salivary insulin in western lowland gorillas.
Cognitive biases reveal underlying affective state by indicating optimism and pessimism. This methodology may permit assessment of positive welfare in animals that have few validated positive welfare indicators, such as bears. Our goal was to validate a judgment bias test for assessing optimism in brown bears, using a touchscreen. After training the bears on a conditional discrimination, we compared responses to an ambiguous stimulus in a 2 × 2 nested design involving four experimental conditions representing presence or absence of a behind-the-scenes tour and presence or absence of a keeper training session with food reinforcement. We recorded bears' behavior during the conditions as a measure of convergent validity. Testing revealed the possibility of pessimism in the absence of reinforcement in one bear. More frustration behaviors were also observed during the no food reinforcement conditions. This is the first experimental demonstration of brown bears using a touchscreen and one of only three reports in which bears have been reported to perform a conditional discrimination. This method of assessing underlying affective state shows promise for the future.
A biohybrid sensor is reported to integrate live insect antennae with micro electrode arrays. High resolution recording of voltage responses generated by olfactory sensory neurons (OSNs) were obtained in response to a panel of four volatile organic compounds (VOCs) at two concentrations, 20 parts per billion (ppb) and 20 parts per million (ppm). Biohybrid sensor lifetime was sustained by a novel micro fluidic platform with sensor responses acquired at 24 hours, 48 hours, 7 days, and 14 days post resection of antenna from the host. VOC identity was classified by providing OSN firing rate histograms as input into a multilayer perceptron artificial neural network (MLP ANN). Biohybrid sensor response was found to be affected by anatomical location and VOC identity and thus influenced classification accuracies. Significant classification accuracies were achieved at the 24-hour and 14-day timepoints. Toluene at the 14-day timepoint elicited a unique response resulting in 100% classification at the distal anatomical location. We believe this works provides a framework for utilizing biohybrid sensing systems for VOC detection and identification.
Odor-guided navigation is fundamental to the survival and reproductive success of many flying insects. Despite its biological importance, the mechanics of how insects sense and interpret odor plumes in the presence of complex flow fields remain poorly understood. This study employs numerical simulations to investigate the influence of turbulence, wingbeat-induced flow, and Schmidt number on the structure and perception of odor plumes by flying insects. Using an in-house computational fluid dynamics solver based on the immersed-boundary method, we solve the three-dimensional Navier–Stokes equations to model the flow field. The solver is coupled with the equations of motion for passive flapping wings to emulate wingbeat-induced flow. The odor landscape is then determined by solving the odor advection–diffusion equation. By employing a synthetic isotropic turbulence generator, we introduce turbulence into the flow field to examine its impact on odor plume structures. Our findings reveal that both turbulence and wingbeat-induced flow substantially affect odor plume characteristics. Turbulence introduces fluctuations and perturbations in the plume, while wingbeat-induced flow draws the odorant closer to the insect’s antennae. Moreover, we demonstrate that the Schmidt number, which affects odorant diffusivity, plays a significant role in odor detectability. Specifically, at high Schmidt numbers, larger fluctuations in odor sensitivity are observed, which may be exploited by insects to differentiate between various odorant volatiles emanating from the same source. This study provides new insights into the complex interplay between fluid dynamics and sensory biology and behavior, enhancing our understanding of how flying insects successfully navigate using olfactory cues in turbulent environments.
Many animals locate food, mates and territories by following plumes of attractive odors. There are clear differences in the structure of this plume-tracking behavior depending on whether an animal is flying, swimming, walking or crawling. These differences could arise from different control rules used by the central nervous system during these different modes of locomotion or one set of rules interacting with the different environments while walking on the surface versus flying or swimming. Flow speeds and turbulence that characterize the environments where walking and flying insects track plumes may alter the structure of odor plumes in an environment-specific way that results in the same control rules generating behaviors that appear quite different. We tested these ideas by challenging walking male cockroaches, Periplaneta americana, and flying male moths, Manduca sexta, to track plumes of their species' sex pheromones in low wind speeds characteristic of cockroach experimental environments, higher wind speeds characteristic of moth experimental environments, and conditions ranging from low to high turbulence. Introducing a turbulence-generating structure into the flow significantly improved the flying plume tracker's ability to locate the odor source, and changed the structure of the behavior of both flying and walking plume trackers. Our results support the idea that plume trackers moving slowly along the substrate may use the spatial distribution of odor, while faster moving flying plume trackers may use the timing of odor encounters to steer to locate the source.
Evaluating how primates in human care function within their social environment is important for understanding and optimizing their management and welfare. The neuroendocrine hormone oxytocin is associated with affiliation and bonding, suggesting it can be used to evaluate the affiliative nature of social groupings. When paired with cortisol concentrations, social stressors can simultaneously be assessed, providing a more complete picture of primate social environments than if measuring either hormone independently. Here, we measured both oxytocin and cortisol in urine within a large subset of male western lowland gorillas (Gorilla gorilla gorilla; n = 71) living in North American zoos. Both endocrine measures were compared between social group types, with an emphasis on comparing bachelor and mixed-sex groupings to understand how these broad management practices affect male gorillas in zoos. Oxytocin concentrations were greater in bachelor group males than mixed-sex group males and singly housed males, providing physiological evidence that males in bachelor groups form comparatively stronger affiliative relationships than males in other group types. Cortisol concentrations did not differ between bachelor and mixed-sex group males and males in both group types had lower cortisol concentrations than singly housed males. These results indicate that males are similarly capable of coping with group-specific social stressors, and single management may expose males to additional stressors for which further study is needed. These data contribute to a larger body of research highlighting the value of bachelor groups from both a population management and individual welfare perspective.
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Flying insects track turbulent odor plumes to find mates, food and egg-laying sites. To maintain contact with the plume, insects are thought to adapt their flight control according to the distribution of odor in the plume using the timing of odor onsets and intervals between odor encounters. Although timing cues are important, few studies have addressed whether insects are capable of deriving spatial information about odor distribution from bilateral comparisons between their antennae in flight. The proboscis extension reflex (PER) associative learning protocol, originally developed to study odor learning in honeybees, was used as a tool to ask if hawkmoths, Manduca sexta, can discriminate between odor stimuli arriving on either antenna. We show moths discriminated the odor arrival side with an accuracy of >70%. Information about spatial distribution of odor stimuli may be available to moths searching for odor sources, opening the possibility that they use both spatial and temporal odor information.This article has an associated First Person interview with the first author of the paper.
In natural environments, bear behavior follows seasonal patterns but the zoo environment differs from the natural environment in several ways, including the presence of zoo visitors. Although typically difficult to disentangle, we were able to tease apart the effects of seasonal changes and visitor density on the visibility and behavior of 10 bears representing five species housed at Cleveland Metroparks Zoo due to the disruption caused by COVID-19. We conducted a longitudinal bear behavior monitoring project from June, 2017-November, 2020. Bears were more visible in the spring and in the presence of visitors, locomoted more and were less inactive when large crowds were present, foraged and locomoted more when it was earlier in the day, and locomoted more at higher temperatures. There were limited differences in bear visibility to observers between 2020 (when the zoo was temporarily closed to visitors) and the previous three years. There were no differences in rates of stereotypy or social behavior across seasons, crowds, or daily attendance categories. Based on these limited differences, neither season nor visitor density seemed to have an apparent effect on bear behavior or welfare.
Flapping-wing micro air vehicles (FWMAVs) that mimic the flight capabilities of insects have been sought for decades. Core to the vehicle’s flight capabilities is the mechanism that drives the wings to produce thrust and lift. This article describes a newly designed flapping-wing mechanism (FWM) inspired by the North American hawk moth, Manduca sexta. Moreover, the hardware, software, and experimental testing methods developed to measure the efficiency of insect-scale flapping-wing systems (i.e., the lift produced per unit of input power) are detailed. The new FWM weighs 1.2 grams without an actuator and wings attached, and its maximum dimensions are 21 × 24 × 11 mm. This FWM requires 402 mW of power to operate, amounting to a 48% power reduction when compared to a previous version. In addition, it generates 1.3 gram-force of lift at a flapping frequency of 21.6 Hz. Results show progress, but they have not yet met the power efficiency of the naturally occurring Manduca sexta. Plans to improve the technique for measuring efficiency are discussed as well as strategies to more closely mimic the efficiency of the Manduca sexta-inspired FWM.
Positive reinforcement training (PRT) is associated with increases in species-typical behavior and decreases in stereotypic and abnormal behavior in participating animals. Physiological changes following PRT, for example, increases in oxytocin (OXT) and/or decreases in cortisol (CORT), may facilitate these behavioral changes. This study evaluated salivary OXT and salivary CORT concentrations in two adult male western lowland gorillas (Gorilla gorilla gorilla) following PRT with their primary animal care staff. Following PRT, no change in OXT was observed. CORT decreased in one subject following PRT. Changes in endogenous OXT are related to affiliative interactions and interact with strongly bonded conspecifics. PRT may not activate the oxytocinergic system because PRT is not a species-specific affiliative interaction and/or animal care staff are not viewed as conspecifics. Regardless, PRT may still be viewed as a positive interaction resulting in stress reduction via a decrease in CORT. Relationships are unique, thus these results only apply to these two gorillas and one animal caregiver. Larger population-level studies are needed to understand overall trends in human-animal interactions, and ultimately human-animal relationships. Further evaluation of physiological changes following human-animal interactions should be informative for understanding the human-animal relationship in zoos.
This work includes the analysis and evaluation of surgically removed wings from Manduca sexta hawkmoth and the fabrication and testing of moth-like wings for the eventual goal of developing a flapping wing micro air vehicle. The natural and manufactured wings are compared in three main characteristics, their distribution of mass, their flexural stiffness, and their camber. Previous results indicate that if these three properties can be mimicked, manufactured wings could produce similar flight properties to the natural wings. Wings are manufactured based on templates created from three different moths. Additionally, three different materials are used for fabricating the membrane, Icarex Ripstop Fabric, Mylar Film, and Kapton Film. Strips of unidirectional carbon fiber are used to mimic the venation structure. Wings manufactured from Icarex and Kapton replicated the mass of the natural wings. However, all manufactured wings are far stiffer than the natural ones. Icarex retains its camber the best.
The hawkmoth Manduca sexta is nocturnally active, beginning its flight activity at sunset, and executing rapid controlled maneuvers to search for food and mates in dim light conditions. The visual system of this moth has been shown to trade off spatial and temporal resolution for increased sensitivity in these conditions. The study presented here uses tethered flying moths to characterize the flight performance envelope of the wide-field-motion-triggered steering response of M. sexta in low light conditions by measuring attempted turning in response to wide-field visual motion. Moths were challenged with a horizontally oscillating sinusoidal grating at a range of luminance, from daylight to starlight conditions. The impact of luminance on response to a range of temporal frequencies and spatial wavelengths was assessed across a range of pattern contrasts. The optomotor response decreased as a function of decreasing luminance, and the lower limit of the moth's contrast sensitivity was found to be between 1 and 5%. The preferred spatial frequency for M. sexta increased from 0.06 to 0.3 cycles deg(-1) as the luminance decreased, but the preferred temporal frequency remained stable at 4.5 Hz across all conditions. The relationship between the optomotor response time to the temporal frequency of the pattern movement did not vary significantly with luminance levels. Taken together, these results suggest that the behavioral response to wide-field visual input in M. sexta is adapted to operate during crepuscular to nocturnal luminance levels, and the decreasing light levels experienced during that period changes visual acuity and does not affect their response time significantly.
Zoo-housed bears are prone to exhibiting stereotypic behaviors, generally considered indicators of negative welfare. We explored the effects of a variable-time feeding enrichment schedule on behavioral indicators of welfare in four bear species at Cleveland Metroparks Zoo. We distributed the diets of eight bears in one of five enrichment items, for two consecutive days each, and monitored behavior throughout the day. In Experiment 1, we compared variable-time to fixed-time presentation of enrichment over two, 10-day periods. Overall, bears performed more exploratory behavior when enriched (p < 0.0001). Furthermore, variable-time enrichment was associated with a greater increase in exploratory behavior than fixed-time enrichment when compared to baseline (p < 0.001). Both fixed-time (punadjusted <0.05, padjusted = 0.07) and variable-schedule (punadjusted <0.05, padjusted = 0.09) enrichment were also associated with similar decreases in abnormal behavior compared to baseline. For Experiment 2, we tested habituation to enrichment over 30 days using multiple items and a semi-variable presentation schedule. Again during the enrichment period, bears exhibited increased exploratory behavior (p < 0.0001) and decreased abnormal behaviors compared to baseline (punadjusted = 0.05, padjusted = 0.09). We observed no habituation during the 30-day sustained enrichment period for these behaviors. Collectively, these results suggest that daily, variable-schedule feeding enrichment, with intermittent presentation of unique enrichment items, increases behavioral indicators of positive welfare and decreases behavioral indicators of negative welfare.