Applying Behavioral and Physiological Measures to Assess the Relative Impact of the Prolonged COVID-19 Pandemic Closure on Two Mammal Species at the Oregon Zoo: Cheetah (A. jubatus) and Giraffe (G. c. reticulata and G. c. tippelskirchii)

Abstract

The effect of visitor presence on zoo animals has been explored in numerous studies over the past two decades. However, the opportunities for observations without visitors have been very limited at most institutions. In 2020, the Oregon Zoo was closed, in response to the global SARS-CoV-2 (COVID-19) pandemic, from 15 March 2020 to 12 July 2020, resulting in approximately four consecutive months without visitor presence. This study aimed to quantify potential behavioral and hormonal changes expressed during two transition periods in zoo visitor attendance: the initial time period before and after closure in March 2020 and time before and after reopening in July 2020. Fecal glucocorticoid metabolite (fGM) concentrations of resident giraffes (n = 2) and cheetahs (n = 2) were tracked using enzyme immunoassay (EIA) analyses. Average fGM concentrations during the two transition periods were compared using a two-way mixed ANOVA. Additionally, twice-weekly scan sampling was used to quantify behavioral observations across the transitions, which were analyzed as individual behavior proportions. Individual behavior proportions were compared across the Zoo’s opening status and time of day using Kruskal–Wallis (H) tests. The results of our analyses showed the following outcomes: (1) significant increases in fGM concentrations for cheetahs and giraffes between the transition periods but not within them; (2) a significant increase in time spent ‘not visible’ in the cheetahs in the second transition period; and (3) increased vigilance behaviors in the giraffes immediately after the Zoo’s closure. However, the changes observed in fGM concentrations may be more strongly correlated with concomitant social changes (giraffes) and some medical events (cheetahs) rather than with the Zoo’s opening status. Nevertheless, this study was able to quantify differences in behavioral frequencies and fGM concentration in cheetahs and giraffes at the Oregon Zoo during the times of transition between visitor’s presence and absence. The results indicate that, while there was a possible, but relatively minor impact of the presence and absence of visitors on some behaviors, the differences observed in fGM concentration may have been more affected by some of the concomitant social changes and medical events that happened during the same period than by the presence or absence of visitors.

Comparing Space Use and Fecal Glucocorticoid Concentrations during and after the COVID-19 Closure to Investigate Visitor Effects in Multiple Species

“…In Japanese macaques, there was no difference between the closure and reopening on the number of cognitive trials animals chose to participate in, the number of trials they completed per session, or their accuracy on the tasks [11]. Physiologically, neither cheetahs (Acinonyx jubatus) nor giraffes (G. c. reticulata, G. tippelskirchi) showed significant differences in fecal glucocorticoid levels between matched open and closed periods [22].…”

The Impact of COVID-19 Zoo Closures on Behavioural and Physiological Parameters of Welfare in Primates

“…Despite some limitations in terms of study designs, research undertaken during the COVID-19-pandemic-enforced zoo closures has brought a new perspective on the experiences of zoo animals. A mixed behavioural response has been observed across species: slender-tailed meerkats (Suricata suricatta) engaged in more alert behaviour and fewer positive social interactions during closures than open periods [24] and giraffe (Giraffa camelopardalis tippelskirchi) reduced vigilance when visitors returned to zoos following the closure period [25]. Chinese goral (Nemorhaedus griseus) engaged in more environmental interactions when the zoo was closed to the public, red kangaroos (Macropus rufus) increased inactivity, spent more time in proximity to one another, and reduced their space use when the zoo reopened [26], and amphibians (common toad, Bufo bufo; common frog, Rana temporaria; smooth newt, Lissotriton vulgaris; pool frog, Pelophylax lessonae; golden mantilla, Mantella aurantiaca; golden poison dart frog, Phyllobates terribilis) were less visible when zoo visitors returned [27].…”

Is Chimpanzee (Pan troglodytes) Wounding Frequency Affected by the Presence Versus Absence of Visitors? A Multi-Institutional Study

“…Finally, discussions of wounding and welfare should be informed by the addition of physiological measures when possible. Due to the post-hoc nature of this study, the addition of physiological markers of welfare, such as fGM concentrations, was not possible, but, similar to Fink et al [49], future studies might consider ways to include such measures.…”

“…The initial wave of the SARS-CoV-2 (COVID-19) pandemic in early 2020 forced zoos to close for the first prolonged period of time in the United States (U.S.) and globally. Since then, several visitor effect studies of various zoo-housed taxa have been published due to the unique opportunity these closures provided [17,[25][26][27][49][50][51][52][53]. Greater flamingos (Phoenicopterus roseus) showed no behavioral changes between the open and closed conditions, while Chilean flamingos (P. chilensis) showed a decrease in three out of eight observed behaviors (activity, movement, and feeding) when the zoo reopened; however, these changes were partially attributed to weather [27].…”

“…Only one COVID-related study [49] utilized a physiological measure in addition to behavioral markers of change between the open and closed conditions. Results showed an increase in fecal glucocorticoid metabolite (fGM) concentrations of cheetahs (Acinonyx jubatus) and giraffes (Giraffa camelopardalis reticulata and G. c. tippelskirchi) as the zoo transitioned from closed to open.…”