How Guest Behavior Influences Zoo Animal Welfare

Introduction

For most zoo animals, the visitor presence is a normal office of their daily routine. Since the early 1970s, researchers have suggested that this visitor presence may play a part in modifying the beliefs of the animals being observed (1, 2). Equally reviewed past Davey (3) the 'visitor upshot' has been described in many early studies as a negative influence on animal beliefs, decreasing maintenance behaviors or increasing aggressive interactions. Alternatively, enquiry can as well show no observable change in beliefs with visitor presence or intensity (4, 5) and in some circumstances, the presence of visitors may be enriching (half-dozen), particularly where visitor- creature interaction has a positive outcome (2). For example, gentoo penguins (Pygoscelis papua) evidence increased puddle usage and positive increases in behavioral variety with increasing company number (7) and a long-billed corella (Cacatua tenuirostris) performed "attention-seeking" behaviors, such equally bobbing up and downwardly and dancing on the spot, directed at visitors continuing at the bird's enclosure (4).

Considerable interest has also focused on the effect of keeper presence on the behavior of zoo animals (eight). As daily providers of resources, the work of a zookeeper may be an enriching feature of the captive environment but, for some species, this human being presence within their environment could exist negative (ix). For many mammals, the human-fauna relationship that can develop betwixt an animal and its keeper may be beneficial to the animate being's welfare state (half-dozen). Experienced keepers are more probable to recognize potentially negative behavioral changes in mammalian charges compared to not-mammalian ones (ten), and the increasing recognition of a keeper by the animal reduces the stress of having humans in and around the enclosure (11, 12).

Whilst there is considerable interest in assessing both visitor and keeper effects, studies may exist limited. It is ofttimes difficult to determine a baseline beliefs for a report subject, specially in zoos that are open to the public every day (three). Evaluation of research findings may be further complicated past limited prior information on the species and researchers may find it tricky to determine which behaviors are indicative of changes in welfare state (thirteen). Methods to measure out the visitor effect include assessment of visitor number, noise and behavior (2)—different taxa will vary in their responses to these factors, creating difficulties when designing repeatable research projects (14).

Much of the existing visitor effects literature has a mammalian focus, with primates dominating (two, 15). Zoos house a multitude of non-primate, not-mammalian taxa that may also exist affected by visitors and this diversity in zoo-housed taxa means that studies assessing the visitor effect across a wider-range species would be beneficial (3) to inform husbandry practices and welfare assessment.

Every bit such, the aim of this inquiry was to decide whatever influence of human presence on a representative species of ordinarily housed zoo bird, a hornbill (Bucerotidae). Species360's Zoological Data Management System (ZIMS) database identifies over 2,600 hornbills housed in global species360-registered institutions as of August 2019 (xvi). Hornbills remain challenging to breed in captivity (17), and further research would be beneficial to identify the affect of humans on captive hornbill behavior, and thus provide evidence that may help understand whatever further influences on reproduction. The species focus for this enquiry was the black-casqued hornbill (Ceratogymna atrata), a big hornbill from Africa, known for its sophisticated cognitive capabilities (18) with a decreasing wild population tendency (19). Wild black-casqued hornbills (hereon referred to as "hornbill") are normally found in pairs (twenty), but pocket-size groups of up to v birds are frequent and congregations of upward to twoscore individuals have been found on fruiting trees (21). This species feeds on at least 19 species of fruit in the wild and also invertebrates as a supplementary nutrient source (22). Given their flexible social system and nutrition, this hornbill is a relevant report subject for analyzing the relationship betwixt variable husbandry influences (i.e., human presence), behavior, and welfare as have evolved to cope with a very heterogeneous, widely fluctuating environment. More widely, a general lack of research on captive hornbill beliefs, coupled with their poor reproductive success in zoos (23–25) but need for conservation activity due to declining wild populations (26, 27), makes study of hornbill behavior and welfare in the zoo of increasing relevance and importance.

Materials and Methods

Subjects and Study Pattern

Information collection took identify from 13th to 31st August 19 at Blackpool Zoo, Lancashire, UK and 17 days of observation were conducted in full. A pair of hornbills (both ~1 year of age) were observed for 90 h. The hornbills were housed with a pair of blue cranes (Anthropoides paradiseus); the enclosure included an indoor area measuring ~three k³ (containing feeding and drinking areas, heat lamp and perches) connected to an outdoor exhibit measuring ~20 m (length) × viii 1000 (width) and from 8 to x yard in height. The outdoor department contained various furnishings, such as natural planting and perches (see a schematic illustration of the enclosure in Supplementary Figure 1). No interaction between the hornbills and the cranes was noted during the ascertainment period, nor did the hornbills actively seek to avert the presence of the cranes.

An ethogram (Table 1) was developed using previous research from Kozlowski et al. (17). Each twenty-four hours consisted of half dozen-h of observation: x:00 to 12:00; 12:xx to 14:20; and 15:00 to 17:00. Each hour of each observation flow was considered a separate sampling result for data assay (see "Information assay"). This timeframe enabled capture of the varying numbers of visitors across each day; from when visitors first started arriving at the Zoo through to when the vast bulk go out. Due to the brusque menstruum of ascertainment, no data were nerveless during periods of time when visitors were not inside the Zoo. State behaviors (n = 90 records per bird) were recorded using instantaneous focal sampling at 1-min intervals (28), as was the location of each bird (indoor or outdoor exhibit) inside the enclosure. A total of x,740 min of behavioral information were collected per bird.

Tabular array 1. Ethogram of captive black-casqued hornbill state behaviors.

To explicate potential behavioral changes associated with the number of visitors, the observer started recording the location of each bird from the tertiary twenty-four hours onwards (n = lxxx records/bird). Visitor number was counted each minute and the mean value was used to decide groupings into loftier, medium or depression company number (loftier = hateful of 13+ visitors/minute; medium = hateful of 7–13/minute; low = hateful of 1–vii/minute) for each hour. Categorization was based how busy the viewing areas of the enclosure appeared to the observer and how much of the enclosure was visible to the observer when different numbers of people were gathered around. Visitors could look into the viewing window of the indoor enclosure merely the viewing area was pocket-sized; the inside firm kept darker and more secluded for the hornbills, who could perch away from, and higher than, the principal window so had the choice to be in or out of view (see Supplementary Figure ii). Hornbills had ad lib access to and from the indoor enclosure during the duration of the written report. The presence or absence of keepers was also recorded each minute, for each observation period. Visitor and keeper presence were recorded in areas visible to the birds (within or around their enclosure), approximate altitude of up to xx meters away from enclosure out the front end and visible side (almost outdoor surface area of enclosure) and ten meters out from back (other side of enclosure by the indoor area). The mean (±SD) number of visitors was 8.8 (±0.12), with the minimum existence one person and the maximum being 51 people. For all periods of data drove, the observer was considered a company.

Local atmospheric condition atmospheric condition (pelting, cloudy, sunshine), temperature and humidity were recorded for the kickoff of each observation hour using the Met Role website https://www.metoffice.gov.great britain. For the overall study period, the mean (±SD) temperature was 17.01°C (±0.fourteen) and humidity was eighty.24% (± 0.90). The well-nigh mutual weather status was cloudy.

Data Analysis

Data were analyzed in R studio 5. ane.2.19 (29). To analyze the potential consequence of visitors, local weather conditions (including temperature and humidity), keeper presence, and individual bird ID on state behaviors and on time spent outside compared to inside, mixed furnishings models with date blocked every bit a random cistron to account for the repeated measurements were run using the "lmertest" package in R (30). The "MuMIn" package (31) was used to summate r ² values for each model run.

To decide whatsoever effect of temperature, humidity, and weather (cloudy, raining, or sunny) on daily visitor numbers at the hornbill enclosure, a full general linear model was run. Anecdotally, zoo visitors are known to get together around an enclosure when they see a keeper working inside, and therefore Spearman's rho correlation was run on the fourth dimension spent by a keeper in the enclosure and the mean number of visitors at the enclosure for that hour of ascertainment. The aforementioned correlation was run to bank check any relationship between the temperature and humidity for each ascertainment hour.

Based on descriptive assay (Effigy 1), minutes spent preening (as a comfort behavior), out of sight (as a potential indicator of stress based on how the birds could hide themselves away in dissimilar areas around the inside and exterior enclosure), inactive (every bit measure out of limited behavioral diversity, i.e., birds spending the majority of their fourth dimension inactive may not be performing a total daily fourth dimension-action upkeep) and foraging (equally an exploratory behavior) per observation period per day were included as dependent variables. Out of sight (i.e., being away from visitors) and inactivity are noted in Nimon and Dalziel (four) as behavioral outcomes of different levels of visitor event on another species of socially and cognitively complex bird, hence their inclusion here. Temperature was included in the modeling of preening, foraging or inactivity and visitor number, and for the fourth dimension birds out of sight. The interaction between visitors and temperature was also included, too-individual bird ID, and finally engagement (every bit the random cistron).

Figure 1. Average (± standard deviation) time-activity budget for the female and male hornbill against dissimilar categories of visitor number. White bars, low visitor number; Gray bars, medium visitor number; Black confined, high visitor number. Perching is the most usually observed behavior and time spent perching is consequent betwixt these two individuals and across company number categories.

To see whether time of twenty-four hour period influenced these three behaviors and time out of sight, in conjunction with the visitor and temperature interaction, time of the ascertainment was coded (morning from 10:00 to 12:00; noon from 12:00 to thirteen:50; afternoon from xiii:50 to 17:00) and included in a farther mixed effects model, again with appointment blocked as a random factor. Time codes were based on give-and-take between the three authors as to the most practical, biologically-relevant, and optimal for capturing modify in visitor/keeper presence way of categorizing when observation occurred.

Output is presented from the anova (model proper name) part in RStudio. Postal service-hoc testing using the "lsmeans" and "pbkrtest" packages (32, 33) was run for behaviors were time lawmaking showed a significant relationship to change in activity. To unpick any bear upon of when keepers might be in with the birds during unlike times of the twenty-four hour period, and hence irresolute bird action, the mean number of minutes for each time category was calculated to run into at what times of the day keepers were in with the hornbills for longest.

Involvement from each bird (measured as the number of minutes that a bird looked in the direction of or moved toward the keeper or visitor) was included as the dependent variable in a mixed furnishings model to make up one's mind any influence of keeper presence (time in minutes at or in the enclosure), visitor number and individual bird ID, again with date blocked equally a random factor.

Significant outputs from the generalized linear models run are provided in the results section with estimate ± standard deviation, r ^two value, degrees of freedom, t value and P-value at the 5% level. For relevant non-significant results, P-values are given.

Results

State Behaviors

A fourth dimension activeness upkeep was adult to show the beliefs of both the male and female hornbill under low, medium and loftier visitor numbers (Figure i).

To investigate the relationship between visitors and weather, linear models were run to identify whatever significant predictors of increased visitors to the zoo. There is no upshot of conditions condition on company number (P = 0.731) only there is a significant influence of temperature and humidity. Significantly more visitors are nowadays on hotter days (estimate = 1.25 ± 0.259; df = 175; t-value= 4.83; P < 0.001) and significantly fewer on more boiling days (gauge = −0.198 ± 0.039; df = 175; t-value = −2.78; P = 0.006). Temperature increase showed a positive correlation with humidity (n = 26; r = 0.585; P = 0.002) and this was the justification for including temperature in the modeling of bird behavior / time out of sight and company number plus other relevant interactions (see "data analysis" section).

At that place are no pregnant effects on preening behavior for either hornbill (P = 0.956). There is an individual deviation for time being out of sight (estimate = 1.044 ± 0.416; r ² = 37%; df = 159.6; t-value= 2.51; P = 0.013), which is significantly higher in the male bird than the female bird in this case. All other predictors of fourth dimension spent out-of-sight are non-meaning. The aforementioned difference is seen for foraging, with the male spending more time foraging than the female (gauge = 3.31 ± 0.814; r ² = 28%; df = 157.ix; t-value= 4.09; P < 0.001). Again, there is no significant effect of visitors, temperature or the interaction betwixt them on time spent foraging. Finally, the individual bird also significantly predicts, with the female person hornbill spending more time inactive than the male (gauge = −4.82 ± 1.09; r ² = 28%; df = 159.6; t-value = −iv.44; P < 0.001). All other potential predictors of inactivity were non-pregnant.

Fourth dimension of day (category) does not significantly predict when hornbills would be preening [F _{(ii, 167.9)} = 0.969; r ^two = xix%; P = 0.381], foraging [F _{(ii, 166.9)} = 0.163; r ² = 28%; P = 0.849], or out-of-sight [F _{(2, 165.01)} = 2.24; r ² = 38%; P = 0.109] but information technology does predict when these birds are likely to be inactive [F _{(2, 168.iii)} = 3.two; r ² = 29%; P = 0.04]. Birds are more than likely to be inactive in the afternoon compared to in the morn (estimate = 3.91 ± 1.58; df = 169; t-ratio = 2.48; P = 0.04), irrespective of temperature^*company number (estimate = 0.101 ± 0.06; df = 172.8; t-value = one.71; P = 0.09). Keepers were likely to visit the hornbill enclosure more frequently in the forenoon but stay for shorter times (North = xxx; mean = ane.93 ± 0.14) compared to afternoon visits that were less frequent but longer in duration (North = 18; hateful = 4.11 ± 1.thirteen).

Enclosure Occupancy

Modeling predictors of time spent outside for both hornbills including individual bird ID, visitor number, temperature, interest in visitors from the birds, and the relationship visitor number^* temperature shows an overall pregnant fit (approximate = 135.6 ± 30.23; r ² = 51%; df = 98.34; t-value = 4.473; P < 0.001; Figure 2). The effect of visitor number on time spent inside or outside is meaning- an increasing number of visitors suggests less time within for the birds (guess = −7.18 ± 2.63; df = 151.84; t-value = −2.73; P = 0.007). However, as the human relationship between visitor number and temperature is besides significant, the cause of the hornbills beingness increasingly outside with college company numbers is explained by college temperatures (guess = 0.313 ± 0.150; df = 151.24; t-value = ii.09; P = 0.039). There is no individual bird difference for time spent within or outside (P = 0.189). Figure 2 illustrates the human relationship betwixt enclosure occupancy and temperature.

Effigy 2. The time (for both birds combined) spent inside or exterior (median number of minutes ± standard deviation) compared to the three categories of visitor number and average temperature for these visitor categories.

Keeper and Visitor Presence and Hornbill Interest

For 71% of all occurrences (north = xc) no keeper was present inside or nearly the enclosure (Figure 3). Using these remaining data where a keeper was nowadays, the birds' degree of involvement in the keeper and in the visitors (based on minutes of observation from the hornbills) was analyzed. As keeper presence and visitor number correlated (n = 26; r = 0.442; P = 0.024) the interaction betwixt keeper presence^*visitor number on bird interest in both was included in the model.

Figure three. The relationship betwixt the bird's interest in keepers and the visitor number (around the enclosure) and keeper fourth dimension within and around the enclosure. Every bit visitor number increases, the bird'southward interest in the keeper is shorter. The lack of human relationship betwixt visitor interest and visitor number suggest a office for the keeper in this human-animal relationship.

At that place is a significant interaction between the presence of the keeper in or near the enclosure and an increasing involvement from the bird (gauge = 0.864 ± 0.99; r ⁱⁱ = 85%; df = 9.43; t-value= 8.64; P < 0.001). There is no significant effect of bird interest in visitors (P = 0.419), visitor number (P = 0.395) and individual bird ID (P = 0.223). The interaction betwixt visitor number^*keeper presence is a significant factor (estimate = −0.026 ± 0.01; df = 27.44; t-value = −3.403; P = 0.19) on the hornbill's interest in the keeper, suggesting that birds go less interested in the keeper every bit visitor number grows (Figure 3).

When running this model for the bird'due south interest in visitors there is no effect of keeper presence (P = 0.937) and the interaction between visitor number^*keeper presence as well becomes non-significant (P = 0.546). Private bird is significant (estimate = −1.76 ± 0.783; r ² = 50%; df = 36.71; t-value = −2.25; P = 0.03) with the female bird spending more time interested in visitors than the male (overall minutes of interest per observation period from the female 3.9 ± 0.34 and for the male 2.8 ± 0.26).

Give-and-take

Overall, we identified no direct "visitor effect" on the behavior of this pair of hornbills and our results support recent findings, using a mammalian species (the band-tailed lemur, Lemur catta) that the visitor effect may be overestimated (34) if other behavioral influences are not fully considered. For these hornbills, several other variables, such equally the private characteristics of the birds themselves, had greater influences on their behavior.

Behavior

Significant differences in fourth dimension-activeness budgets were identified for these hornbills, with the male spending longer foraging and the female person more time inactive. The female hornbill was less likely to be out-of-sight compared to the male. Time of twenty-four hours significantly predicted increases in action, with the hornbills beingness more than active in the morning compared to the afternoon. Time (minutes) that a keeper spent in the enclosure may be influencing activity, with the shorter, simply more frequent forenoon visitors causing more interest from the birds in the daily husbandry routine. However, temporal changes in inactivity could be explained by the natural ecology of these birds- wild hornbills are known to use vocalization to organize social groups to movement from roosting sites to foraging sites in the early morning (25). Expanding data collection into the earlier morn and afterwards evening to capture husbandry influences on the birds (e.g., the provision of fresh food) would aid unpick this complicated, multilayered relationship.

These hornbills rarely engaged in behaviors suggestive of pair bonding (e.g., allopreening), potentially considering these birds are relatively immature and recent arrivals to this Zoo. The female also showed significantly more interest in visitors and this may exist related to the bird's inactivity and/or personality, every bit a bolder or less nervous private may be less motivated to motility away from visitors. Personality is known to affect how highly-cognitive species engage with human interactions in and around their enclosure (35, 36), then farther assessment of bird personality traits alongside of state beliefs data could be useful in explaining reactions to visitors and keepers. Well-established hornbill pairs spend more time involved in social behavior directed at their partner (17, 20). The immaturity of these study birds may accept resulted in more than interest in their surroundings compared to in each other.

There were no other meaning impacts on hornbill time-activeness budgets, aside from private deviation. Behaviors selected for farther analysis—foraging and preening—are often used as welfare indicators for captive birds (37), and based on the results presented here, in that location are no marked changes in the performance of these behaviors nether different conditions that we measured (i.e., low, moderate, and high company number). Perching, as the commonest behavior observed, was besides consistent betwixt conditions; measurement of where birds are perching (height and distance to or from visitors) could assistance further evaluate this behavior. Wild frugivorous hornbills predominantly forage in the upper and lower awning (38) so perch height and food placement may influence overall time-activity patterns of convict birds. Large species of frugivorous hornbills are known to be selective in their foraging choices and tin spend up to 60 min at a specific fruit source (39). Changes to how nutrient is presented around the enclosure, due east.g., multiple locations where birds need to piece of work for a advantage (25), may encourage more than foraging and exploration time and reduce time spent perching or inactive in large hornbill species in captivity. Black-casqued hornbills are also known to wander extensively beyond a large feeding range (40), so increased enrichment and abilities for flying in their enclosures may reduce time spent inactive and perching.

Enclosure Occupancy

Enclosure zone employ is oft linked to welfare cess for zoo-housed animals, with avoidance of specific zones a potential inference of poorer welfare (41, 42). Our model including individual bird ID, climate and company numbers, explained 51% of the observed zone utilise for the hornbills. Initial analysis suggested that higher company numbers appeared to be associated with increased use of the outdoor exhibit. However, this relationship is less assured when climatic variables are included in the model. Consequently, consideration of all factors that influence creature behavior and enclosure usage is required when attempting to quantify whatever "company effect," as other more than fundamental reasons may produce a more robust, biologically-relevant caption, of the private'southward behavior.

This enclosure may have provided sufficient species-appropriate areas for these hornbills to have the choice to move abroad from visitors, therefore no avoidance behaviors (i.due east., decreased enclosure zone occupancy or repeated, perch to perch hopping) were performed. Selection to be on or off show is known to correlate with the functioning of behaviors that indicate improved welfare (43), so the lack of visitor outcome may in part exist due to the settled nature of the two hornbills in their exhibit and their ability to "cope" with visitor numbers. Further evaluation of enclosure usage alongside of time-activity patterns is required to fully sympathise the suitability of this aviary for these hornbills, however.

The Visitor and Keeper Effect

Our results show that "visitor outcome" is more complicated than information technology may appear, and the presence of visitors alone may be not the complete causative cistron in changing the behaviors of these hornbills. Our results support Goodenough et al. (34), who testify that weather and changes in time of twenty-four hour period are stronger influences on zoo creature behavior than visitors themselves, and those of de Azevedo et al. (44) who show no visitor effect on behavior in some other common zoo bird, the greater rhea (Rhea americana). Consequently, research into beast behavior, including visitors as an independent variable must gene in temporal and climatic changes. Farther assay of visitor behavior may aid to identify the presence of possible company effects on animal welfare; for instance via assessment of changes to the soundscape effectually the enclosure caused by visitors and any accompanying beast response (14, 45). Observation of the visitors by the author of this newspaper who conducted data drove (JS) noted that as visitor number increased, the immediate vicinity was by and large noisier only overall, the hornbill'south enclosure was in a "quieter function" of the Zoo. Personal observation also noted that visitors did not generally stop talking at the enclosure and in modest to moderate groups, normal conservational noise levels were apparent. Visitors were likewise noted every bit walking by without stopping at the hornbills every bit if the enclosure had not been recognized.

There was a clear relationship between the minutes that a keeper was present around the birds and the birds' interest in the keeper. Withal, when visitor numbers were college, the hornbills reduced their focus on keepers. This relationship is further complicated by the fact that there was no significant relationship between visitor number and company interest from birds. These birds mayhap habituated to visitors (because visitors provide no benefit or threat), but that their presence remains a distraction when coupled with other stimuli. Distraction of bird behavior by man actions is noted in other literature in relation to noise levels and arroyo to nesting colonies in the wild from groups of tourists, e.1000., negative impacts on hoatzin, Opisthocomus hoazin, activity (46) and other authors investigating "lark" effects acquired past man activities suggest that species tin can habituate over time (47), therefore such mechanisms may be at play in the captive environment too. If keepers spend less fourth dimension in the enclosure when company numbers are higher, this may also impact on the bird's attention that is directed toward them. Measurement of the influence of visitor presence on keeper duties and time spent in an enclosure would be a useful follow up to this enquiry. The positive correlation betwixt visitor number and the keeper beingness present is also worthy of further investigation. Anecdotally, zoo visitors are fatigued to an enclosure when a keeper is present as "something interesting might be happening" and therefore further adding to the dynamics of the interaction between the creature on brandish, its keeper(due south) and how it perceives the influence of visitors.

Every bit providers of resources, but too invaders of space, zookeepers may be a source of both enrichment and stress (6). Unlike visitors, keepers can enter an exhibit daily and therefore habituation by the animals may be hard (eight). Anticipatory behaviors, performed based on the timing of specific aspects of husbandry (due east.one thousand., feeding), can exist indicative of underlying motivational states (48) and their performance may also impact on the keeper-animal human relationship (i.e., more interest in the keeper if a positive issue is expected). Husbandry variables influence the visitor effect on the behavior of mammalian species (49); there is considerable scope for determining such husbandry impacts on non-mammalian behavior under different company atmospheric condition to fully appreciate animal responses to the zoo environment.

Future Directions

This is a case study on a pair of hornbills of one species at one zoological institution, therefore wide-scale awarding of these results is limited. We have only i measure of individual bird characteristic (sexual practice) and farther report onto the effects of animal personality on the potential of the visitor effect is recommended, this animal personality can predict differences in responses to zoo visitors in captive mammals (36). Multiple measurement of behavior across days when visitor number is depression would provide stronger evidence for the link betwixt ecology conditions and outside enclosure usage, and how visitor presence influences this. A proximal cause of behavior change in these birds may be visitor presence and without measure of temperature effects contained of visitor presence, the human relationship remains complicated. Specialized species of birds (i.e., those evolved for detail environmental weather condition) are noted as having especially aversive reactions to visitors when prevailing environmental weather condition are not optimal (50). As is noted in mammalian inquiry, fully pinpointing behavior change caused by visitor presence and and then inferring welfare state from information technology remains a challenge (51). With taxa such as birds, where outward signs of personality and behavioral expression tin be harder to judge than in mammals, the visitor-beliefs-enclosure usage-welfare relationship could be even more challenging to unpick. Extending this research to other populations of this hornbill in other zoos would enable farther analysis of husbandry and enclosure variables on behavior patterns and aviary usage. It is possible that indirect visitor effects may exist more prevalent than current research suggests. In order to extend this question further, researchers should consider the following:

- Investigate animal behavior across a range of time periods and seasons to fully capture the influence of conditions weather condition on behavior and zone occupancy, and their relationship with visitor numbers.

- Equally zoos move away from single-species aviaries toward larger, mixed-species and/or walk-through exhibits (52) knowledge of whatever potential visitor result on enclosure usage would be relevant to animal husbandry.

- Comparing remote (e.g., trail photographic camera) and in-person data collection would enable evaluation of whatsoever observer effect on animal-to-visitor, brute-to-keeper, and animal-to-observer interaction.

Conclusion

Our written report identified no impact of visitors on hornbill behavior or enclosure use. Visitor number positively correlated with temperature and and then temperature should be factored into time to come visitor studies to avert overestimation of any visitor upshot. Individual hornbill characteristic (e.g., sex) was a meaning predictor of behaviors such as foraging and inactivity, whereas company and keeper presence and conditions conditions were not. When more visitors were present at their showroom, hornbills spent less time showing interest in their keepers, suggesting more complexity to the keeper-animal relationship in certain weather condition. Further inquiry into both visitor and observer effects, across a range of hornbill species, over unlike seasons, and in unlike exhibit styles is recommended.

Data Availability Statement

The datasets generated for this written report are available on request to the corresponding author.

Ethics Argument

This fauna study was reviewed and approved by Sparsholt College Hampshire Ethics Committee.

Author Contributions

JS: data drove and methods. PR: writing and information assay. JB: editing and fact checking plus supervision of information collection.

Funding

Funding for the open admission publication of this commodity was kindly provided by the University of Exeter's institutional Open Access Fund.

Conflict of Interest

The authors declare that the inquiry was conducted in the absence of any commercial or financial relationships that could be construed equally a potential conflict of involvement.

Supplementary Material

The Supplementary Material for this article tin be constitute online at: https://www.frontiersin.org/articles/10.3389/fvets.2020.00236/total#supplementary-fabric

Supplementary Figure i. Schematic plan (non to calibration) of the hornbill enclosure at Blackpool Zoo.

Supplementary Figure two. Hornbill indoor housing with company viewing area (photo credit: J. Scales).

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Source: https://www.frontiersin.org/articles/10.3389/fvets.2020.00236/full

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