Improving the Welfare of Captive Macaques (Macaca sp.) Through the Use of Water as Enrichment

This review evaluates the use of water as a tool for enriching the environments of macaques (Macaca sp.) in captivity. Many macaque species are known to swim and forage in water in the wild, and in-situ reports suggest that access to water promotes activity and cultural behavior. Yet, there is a relative dearth of information on water enrichment, covering only a small number of macaque species in both laboratory and zoo settings. Previous studies in captivity report high levels of usage of water enrichment as well as further behavioral benefits, including increases in play, exploratory behavior, and tool use. Subsequently, there is a clear need for more research on the potential benefits of water enrichment for both macaques and other primate species, especially given that small water troughs and pools provide an inexpensive method for enriching nonhuman primate lives in captivity.     

Tailored Enrichment Strategies and Stereotypic Behavior in Captive Individually Housed Macaques (Macaca spp.)

The welfare of nonhuman animals in captivity is widely dependent on the natural psychological, physical, and behavioral needs of the animals and how adequately these needs are met. Inability to engage in natural behaviors can lead to chronic stress and expression of stereotypic behavior. The majority of research on decreasing stereotypic behavior in captivity addresses problems at the group level and does not account for individual variability in each animal's needs, history, and preferences. This study combined physiological and behavioral measures of well being to comprehensively assess the unique needs of individually housed captive macaques (Macaca spp.) with the aim of developing tailored welfare strategies. Behavioral and hormonal data were collected under 2 conditions: baseline and individualized enrichment. The results showed a significant decrease in stereotypic behavior under the enrichment condition. Additionally, 7 out of 9 individuals showed a decrease in fecal glucocorticoid (stress hormone) levels, indicating a reduction in hypothalamic-pituitary-adrenal activity. Addressing welfare on an individual, rather than group, level allows for a better overall characterization of well being and maximizes the probability of improving the welfare of each animal.     

Assessing the Welfare of Dairy Cattle

This article attempts to determine the effects of environment (captive or wild) and a simple form of environmental enrichment on the behavior and physiology of a nonhuman animal. Specifically, analyses first compared behavioral budgets and stereotypic behavior of captive coyotes (Canis latrans) in kennels and pens to their counterparts in the wild. Second, experiments examined the effect of a simple form of environmental enrichment for captive coyotes (food-filled bones) on behavioral budgets, stereotypies, and corticosteroid levels. Overall, behavioral budgets of captive coyotes in both kennels and pens were similar to those observed in the wild, but coyotes in captivity exhibited significantly more stereotypic behavior. Intermittently providing a bone generally lowered resting and increased foraging behaviors but did not significantly reduce stereotypic behavior or alter corticosteroid levels. Thus, coyote behavior in captivity can be similar to that exhibited in the wild; in addition, although enrichment can affect proportions of elicited behaviors, abnormal behaviors and corticosteroid levels may require more than a simple form of environmental enrichment for their reduction.     

Is Postconflict Affiliation in Captive Nonhuman Primates an Artifact of Captivity?

Researchers have conducted most studies on primate conflict management and resolution in captive settings. The few studies on groups of the same species in captivity and in the wild and the overall comparison across species of findings from studies in both settings have reported patterns of variation in the rates of various postconflict affinitive behaviors that may be setting related. In fact, some authors have claimed that the high rates of postconflict affiliation reported in captive studies could represent an artifact of captivity. I explored the claim and conclude that it is unjustified. I argue that the dichotomy captivity vs. wild is conceptually meaningless and scientists should abandon it as an explanatory variable, that differences across studies both in setting-related variables and in the methods used for assessing postconflict affiliation reduce the strength of comparisons within and across settings, that the empirical evidence thus far available neither allows adequate assessment nor supports any claim that links the rate of postconflict affiliation to captivity or wild conditions, and that studies conducted in both settings may be equally useful—and should be used—to test theoretically relevant hypotheses regarding the causes and predictors of variation in postconflict affiliation. Instead of asking the title question, I would ask which variables influence postconflict affiliation and then whether the variables are really associated only with one of the two settings.     

Improving the welfare of captive macaques (Macaca sp.) through the use of water as enrichment

This review evaluates the use of water as a tool for enriching the environments of macaques (Macaca sp.) in captivity. Many macaque species are known to swim and forage in water in the wild, and in-situ reports suggest that access to water promotes activity and cultural behavior. Yet, there is a relative dearth of information on water enrichment, covering only a small number of macaque species in both laboratory and zoo settings. Previous studies in captivity report high levels of usage of water enrichment as well as further behavioral benefits, including increases in play, exploratory behavior, and tool use. Subsequently, there is a clear need for more research on the potential benefits of water enrichment for both macaques and other primate species, especially given that small water troughs and pools provide an inexpensive method for enriching nonhuman primate lives in captivity.     

A work‐for‐food enrichment program increases exploration and decreases stereotypies in four species of bears

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 (p_unadjusted <0.05, p_adjusted = 0.07) and variable‐schedule (p_unadjusted <0.05, p_adjusted = 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 (p_unadjusted = 0.05, p_adjusted = 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.     

Preference assessments as a tool to evaluate environmental enrichment

Environmental enrichment is an important tool utilized to improve animal welfare in zoological institutions through opportunity for mental and physical stimulation. Many past studies have focused on the impact enrichment has on animal behavior; however, none have conducted preference assessments on enrichment items to examine the relationship between animals' preferences and interaction with enrichment over a 24-hr period. Ten-minute free operant, paired-choice preference assessments were implemented in Study 1 to determine the enrichment preferences of African lions (N = 3). Following Study 1, Study 2 was conducted, which examined the behavior of African lions with enrichment items over the course of 30, 24-hr trials to evaluate the relationship between preferences established in Study 1 and long-term interaction with the enrichment. Generalized estimating equations revealed a statistically significant relationship between the percentage of time the enrichment was approached first and the average duration of interaction in Study 1 to the total duration of interaction and the percent of hours interacted with the item in Study 2. Additionally, the first 2 min of the preference data resulted in comparable statistically significant findings, demonstrating shorter preference assessments can produce similar results. The results support our prediction that preference assessments can be used to estimate the amount of interaction with enrichment over the course of time, with preferred items being interacted with more frequently and in longer duration. Information gained from this study suggests preference assessments can be a time and cost-effective tool to evaluate enrichment preference and predicted efficacy.     

Environmental enrichment for captive stumptail macaques (Macaca arctoides)

Background  The behavior of animals is modified by captivity. Environmental enrichment (EE) is a program designed to enhance the welfare of confined animals by providing them with a more stimulating background. This is carried out by the implementation of a series of activities that encourages them to present behaviors typical of their species, as well as keeps them active. The aim of this study was the evaluation of the influence of the EE in the behavioral variables in a colony of 24 stumptail macaques ( Macaca arctoides ). Our hypothesis is that the application of this program will reduce aggression, stereotypes and coprophilia behaviors and, at the same time, will increase exploration and solitary play.
Methods  The behavioral frequency previous to EE was compared with that during EE implementation.
Results  Our results showed that aggression, coprophilia stereotypic behaviors and social play were significantly reduced during EE, whereas exploration was significantly enhanced. The response of the individuals according to gender was similar for both sexes.
Conclusions  Environmental enrichment programs are indispensable for captive animals' wellbeing as they reduce aggression and stress while providing animals both physical and cognitive entertainment.     

Nutritional and Health Status of Woolly Monkeys

Woolly monkeys (Lagothrix lagotricha and L. flavicauda) are threatened species in the wild and in captivity. Numerous zoological institutions have historically kept Lagothrix lagotricha spp., but only a few of them have succeeded in breeding populations. Therefore the majority of institutions that formerly kept Lagothrix lagotricha are no longer able or willing to do so. Captive populations of the species have frequent health problems, most significantly hypertension and related disorders. Researchers have conducted free-ranging dietary and behavior studies with respect to woolly monkeys, but have established no concrete link between diet or nutrients and captive health problems. The available literature we discuss indicates that researchers need to examine the link further. In addition, it is critical to the survival of the primates to be able to keep breeding populations in captivity owing to increasing natural pressures such as deforestation and hunting. Therefore, better understanding of the captive and free-ranging behavior and health parameters of the species is vital to ensure their survival and to maintain forest health and diversity. Researchers need to conduct large-scale research studies comparing the health and complete diet of individuals in the wild and captivity to resolve health problems facing the species in captivity.     

Olfactory Enrichment in California Sea Lions (Zalophus californianus): An Effective Tool for Captive Welfare?

In the wild, California sea lions (Zalophus californianus) are exposed to a wide variety of sensory information, which cannot be replicated in captive environments. Therefore, unique procedures are necessary for maintaining physiological and psychological health in nonhuman animals in captivity. The effects of introducing natural scents to captive enclosures have been investigated in a variety of species, yet they have not been examined in marine mammals. This project explored the behavioral effect of scent added to the environment, with the goal of improving the welfare of sea lions in captivity. Two scent types were introduced: (a) natural scents, found in their native environment, and (b) non-natural scents, not found in their native environment. This study examined not only scent enrichment but also the possible evolutionary underpinnings of pinniped olfaction. Scent enrichment was found to significantly impact sea lion behavior as demonstrated by a reduction in pattern swimming, an increase in habitat utilization, and a reduction in stereotypical behavior. However, there were no differences in behavior between natural and non-natural scent conditions.     

Sibling rivalry: Males with more brothers develop larger testes

When females mate with multiple partners in a reproductive cycle, the relative number of competing sperm from rival males is often the most critical factor in determining paternity. Gamete production is directly related to testis size in most species, and is associated with both mating behavior and perceived risk of competition. Deer mice, Peromyscus maniculatus, are naturally promiscuous and males invest significantly more in sperm production than males of P. polionotus, their monogamous sister‐species. Here, we show that the larger testes in P. maniculatus are retained after decades of enforced monogamy in captivity. While these results suggest that differences in sperm production between species with divergent evolutionary histories can be maintained in captivity, we also show that the early rearing environment of males can strongly influence their testis size as adults. Using a second‐generation hybrid population to increase variation within the population, we show that males reared in litters with more brothers develop larger testes as adults. Importantly, this difference in testis size is also associated with increased fertility. Together, our findings suggest that sperm production may be both broadly shaped by natural selection over evolutionary timescales and also finely tuned during early development.     

Acoustic accelerometry reveals diel activity patterns in premigratory Port Jackson sharks

Distinguishing the factors that influence activity within a species advances understanding of their behavior and ecology. Continuous observation in the marine environment is not feasible but biotelemetry devices provide an opportunity for detailed analysis of movements and activity patterns. This study investigated the detail that calibration of accelerometers measuring root mean square (RMS) acceleration with video footage can add to understanding the activity patterns of male and female Port Jackson sharks (Heterodontus portusjacksoni) in a captive environment. Linear regression was used to relate RMS acceleration output to time‐matched behavior captured on video to quantify diel activity patterns. To validate captive data, diel patterns from captive sharks were compared with diel movement data from free‐ranging sharks using passive acoustic tracking. The RMS acceleration data showed captive sharks exhibited nocturnal diel patterns peaking during the late evening before midnight and decreasing before sunrise. Correlation analysis revealed that captive animals displayed similar activity patterns to free‐ranging sharks. The timing of wild shark departures for migration in the late breeding season corresponded with elevated diel activity at night within the captive individuals, suggesting a form of migratory restlessness in captivity. By directly relating RMS acceleration output to activity level, we show that sex, time of day, and sex‐specific seasonal behavior all influenced activity levels. This study contributes to a growing body of evidence that RMS acceleration data are a promising method to determine activity patterns of cryptic marine animals and can provide more detailed information when validated in captivity.     

CORMORANT AND DARTER PREY SIZE SELECTION UNDER EXPERIMENTAL CONDITIONS

Hustler, 1995. Cormorant and Darter prey size selection under experimental conditions. Ostrich 66:109-113.

The most profitable sized cichlid fish for Reed Phalacrocorax africanus and Whitebreasted Cormorants P. carbo lucidus and Darter Anhinga melanogaster were determined experimentally. A range of sizes was fed to all three species in captivity to determine whether, given a choice, they would choose the most profitable fish. All species chose certain sizes of fish preferentially, but not in accordance with their profitability. The hunger status of the birds at the time of the experiment and the way in which the experiments were designed and carried out probably influenced the size of fish chosen by the birds.     

Determining the factors affecting the distribution of Muscari latifolium,an endemic plant of Turkey,and a mapping species distribution model

Species distribution modeling was used to determine factors among the large predictor candidate data set that affect the distribution of Muscari latifolium , an endemic bulbous plant species of Turkey, to quantify the relative importance of each factor and make a potential spatial distribution map of M. latifolium . Models were built using the Boosted Regression Trees method based on 35 presence and 70 absence records obtained through field sampling in the Gönen Dam watershed area of the Kazda?? Mountains in West Anatolia. Large candidate variables of monthly and seasonal climate, fine‐scale land surface, and geologic and biotic variables were simplified using a BRT simplifying procedure. Analyses performed on these resources, direct and indirect variables showed that there were 14 main factors that influence the species’ distribution. Five of the 14 most important variables influencing the distribution of the species are bedrock type, Quercus cerris density, precipitation during the wettest month, Pinus nigra density, and northness. These variables account for approximately 60% of the relative importance for determining the distribution of the species. Prediction performance was assessed by 10 random subsample data sets and gave a maximum the area under a receiver operating characteristic curve (AUC) value of 0.93 and an average AUC value of 0.8. This study provides a significant contribution to the knowledge of the habitat requirements and ecological characteristics of this species. The distribution of this species is explained by a combination of biotic and abiotic factors. Hence, using biotic interaction and fine‐scale land surface variables in species distribution models improved the accuracy and precision of the model. The knowledge of the relationships between distribution patterns and environmental factors and biotic interaction of M. latifolium can help develop a management and conservation strategy for this species.     

Accounting for weather and time-of-day parameters when analysing count data from monitoring programs

Problems induced by heterogeneity in species and individuals detectability are now well recognized when analysing count data. Yet, most recent techniques developed to handle this problem are still hardly applicable to many monitoring schemes, and do not provide abundance estimates at the point count scale. Here, we show how using simple weather variables can be a useful surrogate to detect variability in species detectability. We further look for a potential bias or loss in statistical power based on count data while ignoring weather and time-of-day variables. We first used the French Breeding Bird Survey to test how each of the counts of the 97 most common breeding species was influenced by weather and time-of-day variables. We assessed how the estimation of each species response to fragmentation could be influenced by correcting counts with such variables. Among 97 species, 75 were affected by at least one of the five weather and time-of-day variables considered. Despite these strong influences, the relationship between species abundance and fragmentation was not biased when not controlling counts for weather and time-of-day variables and further found no improvement in statistical power when accounting for these variables. Our results show that simple variables can be very powerful to assess how species detectability is influenced by weather conditions but they are inconsistent with any specific bias due to heterogeneous detectability. We suggest that raw count data can be used without any correction in case the sources of variation in detectability could be considered independent to the factor of interest.     

Correction to: The environment matters: season and female contact affect the behavior of captive Addax nasomaculatus male antelope

The addax antelope (Addax nasomaculatus) is a species under serious threat of extinction, as it is more abundant in captivity than in the wild. However, little is known about its basic biology. The aims of this study were to determine how locomotor, feeding, aggressive, marking, and sexual behavior of male addax allocated in all-male groups vary with season and with female contact (i.e., biostimulation). The study was conducted in captive conditions, in two groups of adult males: one with no-physical contact with females, aside from visual and olfactory interactions (CF group, n = 4), and another group completely isolated from females (IF group, n = 4). The frequency of behaviors was recorded during the daytime, 4 days per season (total time of observation = 256 h). Lying, standing, walking, aggressive, marking, grazing, and ruminating behaviors as well as water and supplement consumptions varied with season (all p < 0.05). The lying, walking, marking, grazing, and ruminating behaviors were more frequently observed for CF than IF males (all p < 0.05). Also, all behaviors, except for marking, varied with the interaction between the group and seasons (all p < 0.05). Sexual behavior was extremely scarce, so it was not possible to analyze how it varied with seasons and the group. The present study suggests that management program and housing conditions, especially in ex situ breeding plans, should consider the influence of the season and the sociosexual context on the behavior of addax males.

     

Influence of Cinnamon and Catnip on the Stereotypical Pacing of Oncilla Cats (Leopardus tigrinus) in Captivity

Nonhuman animals in captivity can experience environmental privation that results in their exhibiting abnormal behaviors. Environmental enrichment techniques can help improve their welfare. This study investigated the behavior of 8 zoo-housed oncilla cats (Leopardus tigrinus) in response to 2 odors (catnip and cinnamon) introduced individually into the animals' enclosures for 3 consecutive days. Proportion of scans spent engaging in stereotypical pacing were compared before, during, and after treatments. The addition of cinnamon reduced the proportion of pacing during and after enrichment (Wilcoxon: Z = 3.16, p < .001; Z = 3.16, p < .001, respectively), indicating a prolonged effect of the enrichment on the animals' behavior. Catnip appears to have elicited no significant difference in the stereotypic pacing before, during, or after the enrichment (Friedman: X² = 2.69; p = .260). The results highlight the potential use of cinnamon as a method of environmental enrichment for small captive-housed cats.     

Patterns of woody plant species richness in the Iberian Peninsula: environmental range and spatial scale

Aim Climate‐based models often explain most of the variation in species richness along broad‐scale geographical gradients. We aim to: (1) test predictions of woody plant species richness on a regional spatial extent deduced from macro‐scale models based on water–energy dynamics; (2) test if the length of the climate gradients will determine whether the relationship with woody species richness is monotonic or unimodal; and (3) evaluate the explanatory power of a previously proposed ‘water–energy’ model and regional models at two grain sizes. Location The Iberian Peninsula. Methods We estimated woody plant species richness on grid maps with c. 2500 and 22,500 km² cell size, using geocoded data for the individual species. Generalized additive models were used to explore the relationships between richness and climatic, topographical and substrate variables. Ordinary least squares regression was used to compare regional and more general water–energy models in relation to grain size. Variation partitioning by partial regression was applied to find how much of the variation in richness was related to spatial variables, explanatory variables and the overlap between these two. Results Water–energy dynamics generate important underlying gradients that determine the woody species richness even over a short spatial extent. The relationships between richness and the energy variables were linear to curvilinear, whereas those with precipitation were nonlinear and non‐monotonic. Only a small fraction of the spatially structured variation in woody species richness cannot be accounted for by the fitted variables related to climate, substrate and topography. The regional models accounted for higher variation in species richness than the water–energy models, although the water–energy model including topography performed well at the larger grain size. Elevation range was the most important predictor at all scales, probably because it corrects for ‘climatic error’ due to the unrealistic assumption that mean climate values are evenly distributed in the large grid cells. Minimum monthly potential evapotranspiration was the best climatic predictor at the larger grain size, but actual evapotranspiration was best at the smaller grain size. Energy variables were more important than precipitation individually. Precipitation was not a significant variable at the larger grain size when examined on its own, but was highly significant when an interaction term between itself and substrate was included in the model. Main conclusions The significance of range in elevation is probably because it corresponds to several aspects that may influence species diversity, such as climatic variability within grid cells, enhanced surface area, and location for refugia. The relative explanatory power of energy and water variables was high, and was influenced by the length of the climate gradient, substrate and grain size of the analysis. Energy appeared to have more influence than precipitation, but water availability is also determined by energy, substrate and topographic relief.     

Modelling patterns of coexistence of three congeneric headwater fishes

1. Mechanisms driving patterns of occurrence and co-occurrence among North American freshwater fishes are poorly understood. In particular, the influence of biotic interactions on coexistence among stream reaches and their effects on regional species distribution patterns is not well understood for congeneric headwater fishes.
2. Occupancy models provide a useful framework for examining patterns of co-occurrence while also accounting for imperfect detection. Occupancy models may be extended to test for evidence that a dominant species influences the occurrence of a subordinate species and thus evaluate support for the hypothesis that species interactions drive patterns of coexistence.
3. We examined patterns of occurrence and co-occurrence at the stream-reach scale among three species of darters (Percidae: Etheostomatinae) that occupy headwater streams within a Gulf Coastal Plain drainage in the south-eastern U.S.A. We assessed species occurrences at 97 sites in first- to third-order streams on one occasion each and used data from four sub-reaches sampled with equal effort at each site to estimate species-specific detection probabilities. Following sampling, a suite of habitat variables was collected at three equidistant points along each of the three transects established within a sub-reach. Coarse (stream-segment, catchment, network) scale variables were also incorporated using geospatial data. Single-species and two-species occupancy models were used to examine patterns of occupancy and coexistence.
4. The occupancy of each species was influenced by distinct habitat variables. Goldstripe darters (Etheostoma parvipinne) were constrained by a stream size gradient, groundwater input appeared to influence the occurrence of Yazoo darters (Etheostoma raneyi), and local habitat heterogeneity (e.g. variation in depth and current velocity) appeared to influence the occupancy of redspot darters (Etheostoma artesiae).
5. We found no evidence that the presence of one species influenced the occurrence of another within a stream-reach based on two-species occupancy models. Rather, species co-occurrences were best explained as independent occurrences within a stream-reach according to species-specific habitat associations.
6. Occupancy modelling may provide a suitable framework for evaluating the influence of biotic interactions among congeneric stream fishes along species-specific habitat gradients at the stream reach scale. Our study offers insight into how habitat variation can influence coexistence of potential competitors across a large river system.