2021 Zoo Atlanta Research Review

In 2021, Zoo Atlanta’s team published 11 peer-reviewed articles on various lines of our research programs and collaborations. This brings our institutional total up to a minimum of 391 publications since 1978, when we started keeping records. I was pleasantly surprised to see how productive we were, given the pandemic situation have been enduring. The publishing process typically is delayed owing to the review process and such that when a paper is published in one year, the actual hard work that went into it often took place two or more years previously. So, we will have to see if we hit a covid-induced productivity slump maybe in 2022 or so.

Listed below are the complete citations (in some cases, internetlinks to the publications are listed). Also, here are summaries of our published works in 2021. Of special note for 2021 is that our team published in the journal Animal Cognition and Proceedings of the National Academy of Sciences; these journals generally are considered to be among the most prestigious in all the sciences. Also of significance are the keepers and vet technicians that published this year—a trend that we most certainly want to continue to encourage! It is great to see some new names on our list this year.

Big news! Dr. Marieke Gartner, Associate Curator of Animal Welfare, has joined the faculty in the Department of Psychology at Emory University as an Adjunct Professor. This department has a renowned program in animal behavior and Marieke’s position there, as part of her role at the Zoo, will bring enormous benefits both to Emory and the Zoo.

We had far too many collaborating institutions to be listed here. But I’ll note that we had a good number of international collaborations, and local highlights include Georgia State University and Georgia Tech.

2020 update: we had four publications that are dated 2020 but did not appear in actual print until a few months into 2021. So, those were not reflected in the 2020 Annual Research Review, but I want to list them here so that our hard-working colleagues get proper credit!

Carl, N. J., H. A. Stewart, and J. S. Paul. 2020. Unprovoked mouth gaping behavior in extant Crocodylia. Journal of Herpetology 54:418–426.

Cloutier Barbour, C., M. D. Danforth, H. Murphy, M. M. Sleeper, and I. Kutinsky, I. 2020. Monitoring great ape heart health through innovative electrocardiogram technology: training methodologies and welfare implications. Zoo Biology 39:443–447.

Hooper, S., and A. Schulz. 2020. Proboscidea Morphology. In: Vonk J., Shackelford T. (eds) Encyclopedia of Animal Cognition and Behavior. Springer, Cham. https://doi.org/10.1007/978-3-319-47829-6_1320-1

Emmel, E. S., S. Rivera, F. Cabrera, S. Blake, and S. L. Deem. 2020. Field anesthesia and gonadal morphology of immature Western Santa Cruz tortoises (Chelonoidis porteri). Journal of Zoo and Wildlife Medicine 51:848–855.

Brief Overview of Research at Zoo Atlanta

Zoo Atlanta’s contributions to the world of primate behavioral research, and especially those of western lowland gorillas and orangutans, is renowned and dates back to the late 1970s. The arrival of giant pandas in 1999 launched our giant panda research program, and around 2000, our herpetology research program began to formalize.

Through efforts of Zoo staff and collaborations with researchers at other institutions and academia, our entire animal population continues to help further our knowledge of the basic biology of these animals, as well as informing advancements in animal welfare, veterinary care, and conservation.

2021 Publications

Rieser, J. M., T.-D. Li, J. L. Tingle, D. I. Goldman, and J. R. Mendelson III. 2021. Functional consequences of convergently evolved microscopic skin features on snake locomotion. Proceedings of the National Academy of Sciences USA 118 No. 6 e2018264118             https://doi.org/10.1073/pnas.2018264118

da Silva, H. R., and J. R. Mendelson III. 2021. Inguinal fat bodies in bufonid frogs: 20 years on, and overlooked key references.  Herpetological Review 52:3–6.

Linhoff, L. J., P. S. Soorae, G. Harding, M. A. Donnelly, J. M. Germano, D. A. Hunter, M. McFadden, J. R. Mendelson III, A. P. Pessier, M. J. Sredl, and M. E. Eckstut. 2021. IUCN Guidelines for Amphibian Reintroductions and Other Conservation Translocations, First edition. Gland, Switzerland: IUCN. 78pp.

Sethna, J. M, M. Haire, and J. R. Mendelson III. 2021. Natural History Notes: Chelydra serpentina (Common Snapping Turtle) and Trachemys scripta (Pond Slider) and Terrapene carolina (Eastern box turtle). Anticipatory behavior. Herpetological Review 52:388–389.

Aguilar, L. A. B., S. J. Divers, M. C. M. Barozzi, G. Walth, A. Weyna, R. Radisic, N. L. Gottdenker, and K. P. Gendron. 2021.  Effect of positioning on coelomic radiography with and without contrast in the green iguana (Iguana iguana). Journal of Herpetological Medicine and Surgery 31:73–81.

Sosnowski, M. J., L. A. Drayton, L. Prétôt, J. Carrigan, T. S. Stoinski, and S. F. Brosnan. 2021. Western lowland gorillas (Gorilla gorilla gorilla) do not show an aversion to inequity in a token exchange task. American Journal of Primatology DOI: 10.1002/ajp.23326

Gartland, K. N., J. Carrigan, and F. J. White. 2021. Preliminary relationship between overnight separation and wounding in bachelor groups of western lowland gorillas (Gorilla gorilla gorilla). Applied Animal Behaviour Science 241:105388.

Kozlowski, C. P., K. L. Bauman, A. D. Franklin, J. M. Sahrmann, M. Gartner, E. Baskir, S. Hanna, K. LaMattina, A. Seyfried, and D. M. Powell. 2021. Glucocorticoid production, activity levels, and personality traits of fennec foxes (Vulpes zerda) managed for different roles in zoos. Journal of Applied Animal Welfare Science 2021:1–18.

Pilney Jr., B. 2021. Spatial use and activity budgets of Bornean orangutans (Pongo pygmaeus) within a zoological setting. Animal Keepers’ Forum 48:185–189.

Salmi, R., C. R. Jones, and J. Carrigan. 2021. Who is there? Captive western gorillas distinguish human voices based on familiarity and nature of previous interactions. Animal Cognition: https://doi.org/10.1007/s10071-021-01543-y

Tyner, K. 2021. An experimental approach to assess pacing behavior in slender-tailed meerkats. Animal Keepers’ Forum 48:126–129.
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2021 Summaries:

Title: Functional consequences of convergently evolved microscopic skin features on snake locomotion.
Zoo-team authors: Joe Mendelson
Snakes have specialized microstructures on their belly scales that are presumed to play a role in friction and locomotion, but the structures have been very poorly studied. This study used specialized microscopy and cutting-edge mathematical models to understand the functionality of these structures and identified highly specialized structures never before observed in sidewinding vipers. In a remarkable case of convergent evolution, the unrelated sidewinding vipers of Africa and the familiar sidewinder of North America were very similar in structure and function.

Title: An experimental approach to assess pacing behavior in slender-tailed meerkats.
Zoo-team authors: Katie Tyner
The Zoo’s meerkats were showing some evident pacing behavior associated with their reflections in the glass separating the two social groups. One individual (Scarlet) seemed to be showing stereotypical pacing behavior when she could see her reflection, and less so when her reflection was blocked by a visual barrier. These behaviors were interpreted as her interest in observing, or perhaps desiring to join, the group on the other side. This work is a fine example of applying basic scientific principles to inform animal welfare.

Title: IUCN Guidelines for Amphibian Reintroductions and Other Conservation Translocations, First edition.
Zoo-team authors: Joe Mendelson
The IUCN recruited a multi-national team of researchers and conservationists to draft a summary of best-practices in introductions and translocations of amphibians for conservation programs. This volume will encourage state-of-the-art practices in conservation of critically endangered amphibians.

Title: Who is there? Captive western gorillas distinguish human voices based on familiarity and nature of previous interactions.
Zoo-team authors: Jodi Carrigan
The ability to recognize conspecifics by their voice signals is of crucial importance to social animals, especially where visibility is limited, because it allows for discrimination between familiar and unfamiliar individuals. Animals may also benefit from an ability to recognize and use the information coded into the auditory signals of other species. Companion species such as dogs, cats, and horses are able to discriminate between familiar and unfamiliar human voices; however, whether this ability is widespread across vertebrates is still unknown. We tested whether western gorillas living at Zoo Atlanta were able to discriminate between the voices of subgroups of people: e.g., unfamiliar individuals and familiar individuals. Gorillas responded more often to the voices of unfamiliar than to those of familiar individuals. This indicates that gorillas can recognize different voices among individuals of a different species.

Title: Spatial use and activity budgets of Bornean orangutans (Pongo pygmaeus) within a zoological setting.
Zoo-team authors: Bret Pilney
Using basic observation techniques we mapped the time-scale by which individual orangutans used or did not use various physical areas or structures of their habitat. The results clearly indicated individual differences in space and structure usage among the orangutans, and also identified areas and structured evidently that are never used. This information reveals yet more evidence for individual differences, preferences perhaps, among the orangutans and reveals important information regarding potential future habitat designs or modifications.       

Title: Glucocorticoid production, activity levels, and personality traits of fennec foxes (Vulpes zerda) managed for different roles in zoos. 
Zoo-team authors: Marieke Gartner
Glucocorticoid concentrations, activity, and personality were assessed for zoo-housed fennec foxes in order to determine whether animals managed as ambassadors differed from exhibit or off-exhibit animals. Glucocorticoid concentrations did not differ in relation to role or handling. Hand-reared foxes were more sociable, and, at one institution, ambassador foxes were more sociable than foxes in other roles. These results suggest that management for ambassador programs is not associated with changes in glucocorticoid production and be associated with greater sociability.

Title: Preliminary relationship between overnight separation and wounding in bachelor groups of western lowland gorillas (Gorilla gorilla gorilla). 
Zoo-team authors: Jodi Carrigan
Despite no significant difference in wounding between bachelor and mixed-sex groups of western lowland gorillas (Gorilla gorilla gorilla) in zoological settings, anecdotal concerns around the frequency and severity of wounding in bachelor groups have perpetuated opinions of all-male units as inherently less stable. Previous experience suggested that overnight housing conditions could be an important influencing factor on wounding rates. Our survey data found a significant negative correlation between group duration and wounding rate such that wounding rate was lower in groups that were together longer if and only if groups were separated overnight. Groups that have been together for longer had significantly higher rates of wounding when housed together overnight than when housed separately overnight. Finally, we found that mature silverbacks housed socially overnight sustain significantly more wounds than mature silverbacks housed separately overnight. Based on our analyses, overnight housing conditions have a significant impact on wounding particularly when paired with long-term (> 7 years) group social history. We recommend that groups with long social histories or primarily mature members be separated overnight should housing facilities allow. This study is an important contribution to our knowledge of welfare in the context of crucially important bachelor groups in zoo settings.

Title: Inguinal fat bodies in bufonid frogs: 20 years on, and overlooked key references.
Zoo-team authors: Joe Mendelson
Accessory fat storage organs in toads were reported as new discoveries in 1999. This report updates our still-limited knowledge of the function of these strange organs, and—taking advantage of advanced search abilities on the internet—reports a handful of very old (e.g., 1758) references and illustrations of the organs. The story of the discovery of these organs underscores both how much remains to be discovered in global biodiversity, and also the important power of modern search algorithms on the internet. 

Title: Western lowland gorillas (Gorilla gorilla gorilla) do not show an aversion to inequity in a token exchange task.
Zoo-team authors: Jodi Carrigan
Although individuals in some species refuse foods they normally accept if their partner receives a more preferred one, this is not true across all species. The cooperation hypothesis proposes that this species‐level variability evolved because inequity aversion is a mechanism to identify situations in which cooperation is not paying off, and that species regularly observed cooperating should be more likely to be averse to inequity. We tested zoo‐housed western lowland gorillas on a token exchange task in which subjects received either the same food reward or a less‐preferred reward for the same or more effort than their partner. Gorillas were significantly more likely to refuse in all conditions in which they received a low‐value food reward after completing an exchange, regardless of what their partner received, suggesting that gorillas were not inequity averse, but instead would not work for a low‐value reward. This study is an important contribution to our knowledge of the complexities of gorilla social behavior, and forms an important data set for comparisons with other species of primates, toward our understanding of the evolution of sociality in the great apes.

Title: Effect of positioning on coelomic radiography with and without contrast in the green iguana (Iguana iguana).
Zoo-team authors: Laura Aguilar
We used green iguanas to compare the radiographic appearance of the internal organs. Five radiographic views were imaged on each animals and, one week later, the same radiographic projections were obtained after oral administration of barium. We found that specific views were best for visualizing different organs. For example, one particular view was best for examining one aspect of the heart, while another was best for observing the lungs. This study demonstrates that radiographic beam orientation and patient position result in obvious radiographic differences of the iguanid coelom and that projections are not interchangeable; thus, this is an important contribution to the still-understudied realm of reptile veterinary care.

Title: Natural History Notes: Chelydra serpentina (Common Snapping Turtle) and Trachemys scripta (Pond Slider) and Terrapene carolina (Eastern box turtle). Anticipatory behavior.
Zoo-team authors: Melanie Haire, Joe Mendelson
While providing food for recently rehabilitated and released river otters in the wild on a regular daily time schedule, we noticed that multiple individuals of box turtles, snapping turtles, and sliders had learned to anticipate the location and timing of the appearance of fish intended for the otters—congregating at the site before the arrival of the provisioner. This is a remarkable example of learned anticipatory behavior and memory in multiple species of free-ranging turtles.

Joe Mendelson, PhD
Director of Research