1

2

Welcome to NIU!

On behalf of the MPIG executive committee and the NIU organizing committee, we are pleased to welcome you to the 2019 MPIG conference hosted by Northern

Illinois University.

We wish to acknowledge the following generous sponsors for their financial support:

NIU Department of Anthropology

NIU Institute for the Study of the Environment, Sustainability and Energy

NIU College of Liberal Arts and Sciences

NIU Division of Research and Innovation Partnerships

3

SCHEDULE OF EVENTS ________________________________________________________________

Friday, October 4th

Registration 4:00 - 5:45pm Cole Hall Atrium

Welcome by MPIG President Dr Katie Amato 5:45 - 6:00pm

Cole Hall

Distinguished Primatologist Award and Presentation – Dr. Susan Ford Professor of Anthropology Southern Illinois University

6:00 - 7:00pm Cole Hall

Reception 7:00 - 9:30pm Cole Hall Atrium

Saturday, October 5th

Registration and Breakfast 8:00 - 9:00am Cole Hall Atrium

Poster Setup 8:00 - 8:45am

Cole Hall Atrium

Morning Podium Session 9:00 - 12:00pm Cole Hall

Lunch (on your own) 12:15 - 1:30pm

Poster Session 1:30 - 3:00pm

Cole Hall Atrium

Afternoon Podium Session 3:00 - 4:30pm Cole Hall

Social – Eduardo's Mexican Restaurant, DeKalb 7:00 - 10:00pm

4

Podium Sessions (9:00 – 12:00pm, 3:00 – 4:30pm)

9:00 – 9:15 Opening Remarks

9:15 – 9:30 1. Preference assessments as a tool to evaluate environmental enrichment Jocelyn M. Woods1, Erin Lane2, Lance J. Miller1, 2

1Animal Welfare Research, Chicago Zoological Society, Brookfield, IL, USA, 2San Diego Zoo Institute for Conservation Research, Escondido, CA, USA

9:30 – 9:45 2. Seasonal variation of microbiota and metabolome in fecal sample of golden snub-nosed monkeys (Rhinopithecus roxellanae)

Yan Zeng1*, Xueqin Ni1, Dong Zeng1, Lili Niu2, Jiabo Deng2, Weichao Zheng3, Yuanying Fan4, Yang Li1, Limin Kan3 1College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, China, 2Chengdu Wildlife Institute, Chengdu Zoo, 3Sichuan Tangjiahe National Nature Reserve, Guangyuan, China, 4Cangxi National Forest Park Administration, Sichuan, China, *zengyan1689@gmail.com

9:45 – 10:00 3. Auditory enrichment for captive red howler monkeys (Alouatta seniculus) using numeric odds to simulate choice.

Maggie Ramont1, Holly Farmer1,2, Emile Prins3 1Zoo Conservation Biology MSc program, Plymouth University, Plymouth, UK, 2Research Department, Wild Planet Trust/Paignton Zoo, Paignton, UK, 3Zoological Research, Gaia Zoo, Kerkrade, NL

10:00 – 10:15 4. Novel application of point-of-care technology for real-time health monitoring in Platyrrhines

Alexandra Sacco1,2*, Gideon Erkenswick3,4, April K. Binder2,5, Ana Priscila Peralta Aguilar3, Raul Bello6,7, Mrinalini Watsa1,3, 1Department of Anthropology, Washington University, St. Louis, MO, 2Primate Behavior Program, Central Washington University, Ellensburg, WA, 3Field Projects International, St. Louis, MO, 4Department of Infectious Diseases, Washington University School of Medicine, St. Louis, MO, 5 Department of Biological Sciences, Central Washington University, Ellensburg, WA, 6Taricaya Rescue Center, Puerto Maldonado, Perú, 7Kawsay Biological Station, Madre de Dios, Perú *alexandra.sacco@wustl.edu

10:15 – 10:45 COFFEE BREAK (ATRIUM)

5

10:45 – 11:00 5. Immunofunction and reproductive effort in wild chimpanzees: Field evidence for immunomodulation by gonadal steroids

Jacob D. Negrey1* 1Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, WI, USA, *negrey@wisc.edu

11:00 – 11:15 6. Constructing an expanded social niche: A captive chimpanzee social

network inclusive of human caregivers Jake A. Funkhouser1,2*, Jessica A. Mayhew2,3, John B. Mulcahy2,3,4, and Lori K. Sheeran2,3

1Anthropology Department, Washington University in St. Louis, St. Louis, MO, USA, 2Primate Behavior Program, Central Washington University, Ellensburg, WA, USA, 3Department of Anthropology and Museum Studies, Central Washington University, Ellensburg, WA, USA, 4Chimpanzee Sanctuary Northwest, Cle Elum, WA, USA, *jakefunkhouser@wustl.edu

11:15 – 11:30 7. Evaluating the impact of sustainable land-use changes on perceptions of wildlife conservation around Kibale National Park in western Uganda

Lev A. Kolinski1, Krista M. Milich1 1Department of Anthropology, Washington University in St. Louis

11:30 – 11:45 8. Shifting agriculture’s effects on crowned lemur and Sanford’s lemur ecology in a Malagasy forest fragment

Benjamin Z. Freed1 1Department of Anthropology, Sociology, and Social Work, Eastern Kentucky University, Richmond, KY, USA, *Benjamin.Freed@eku.edu

11:45 – 12:00 9. Anthropogenic food enhancement alters the timing of reproductive onset among wild savanna monkeys

Alicia M. Rich1, Stacy-Anne R. Parke1, Maryjka B. Blaszczyk2, Jennifer Danzy Cramer3, Joseph Lorenz4, Nelson B. Freimer5, J. Paul Grobler6, Trudy R. Turner7, Christopher A. Schmitt1 1Department of Anthropology, Boston University, Boston MA, 2Department of Anthropology, University of Texas Austin, Austin TX, 3Department of Sociology and Anthropology, American Public University, Charles Town, WV, 4Department of Anthropology and Museum Studies, Central Washington University, Ellensburg, WA, 5Brain Research Institute, University of California Los Angeles, Los Angeles, CA, 6Department of Genetics, University of the Free State, Bloemfontein, FS, South Africa, 7University of Wisconsin Milwaukee, Milwaukee, WI

6

12:00 – 12:15 10. Voices of the Forest: A short film on the Black Howler Monkey (Alouatta pigra) conservation efforts in southern Mexico

Jorge Ramos-Luna1,2*, Juan Carlos Serio-Silva1,2, Francisca Vidal-García1,2, Daniela Alicia Torres Anaya1,2 1Red de Biología y Conservación de Vertebrados, Instituto de Ecología, A.C., Xalapa, Veracruz, México, 2Grupo de Estudios Transdisciplinarios en Primatología, Xalapa, Veracruz, México, * jor_ge_94@hotmail.com

12:15 – 1:30 LUNCH (ON YOUR OWN)

1:30 – 3:00 POSTER SESSION (ATRIUM)

3:00 – 3:15 11. Sperm morphological differences in two species of wild howler monkey (Alouatta palliata & A. pigra)

Molly A. Hirst1, Alba Z. Rodas-Martínez2, Marcella D. Baiz1,3, Liliana Cortés-Ortiz1 1Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 2División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, 86150 Villahermosa, Tab., México, 3Department of Biology, Pennsylvania State University, State College, PA

3:15 – 3:30 12. Socioecological Predictors of Health Profiles in Western Lowland Gorillas Kristena Cooksey1, Crickette Sanz1,2, Jean Marie Massamba2, Thierry Fabrice Ebombi2, Prospère Teberd2, Espoir Magema2, Gaston Abea2, Juan Salvador Ortega Peralejo2, Ivonne Kienast2, Colleen Stephens1, David Morgan2,3 1Department of Anthropology, Washington University in Saint Louis, Saint Louis, MO, U.S.A.;2Wildlife Conservation Society, Congo Program, Brazzaville, Republic of Congo; 3Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, U.S.A.

3:30 – 3:45 13. Folivore rules and frugivore rules: Variation in diet, foraging effort and nutritional intake in the frugivorous brown lemur (Eulemur fulvus) and a sympatric folivore (Propithecus diadema)

Irwin, Mitchell T1,3*, Rahalinarivo, Vololonirina2, Raharison, Jean-Luc3, Ramorasata, Bruno3, Ranaivoarisoa, Jean-Freddy2, Randrianasy, Jeannot2, Rothman, Jessica M4,5 1Department of Anthropology, Northern Illinois University, DeKalb, IL, USA, 2Mention Anthropobiologie et Développment Durable, University of Antananarivo, Antananarivo, Madagascar, 3ONG SADABE, Antananarivo, Madagascar, 4Department of Anthropology, Hunter College, 5Graduate Center, CUNY *mirwin@niu.edu

7

3:45 – 4:00 14. Evaluating the sensitivity hypothesis: Are spider monkeys (Ateles geoffroyi) an ideal indicator species compared to sympatric primates in Eastern Costa Rica?

Michelle A. Rodrigues1*, Tracie McKinney2, Jill D. Pruetz3, Stacy M. Lindshield4

1Beckman Institute for Science and Technology, University of Illinois, Urbana-Champaign, IL, USA, 2University of South Wales, Pontypridd, Wales, UK, 3Texas State University-San Marcos, San Marcos, TX, USA, 4Department of Anthropology, Purdue University, West Lafayette, IN, USA, *michellespidermonkey@gmail.com

4:00 – 4:15 15. Interactions among microbial communities in the gut of long-tailed macaques (Macaca fascicularis) in Southeast Asia

Chissa-Louise Rivaldi1*, Audrey Arner2, Hope Hollocher1 1Department of Biological Sciences, University of Notre Dame, 2Pennsylvania State University, *crivaldi@nd.edu

4:15 – 4:30 16. Effects of Environment and Relatedness on the Gut Microbiome of Ugandan red colobus monkeys

Tabor Whitney1, Maria J. Ruiz-Lopez2, Diana M. Christie1,2, Colin A. Chapman3,4, Tony L. Goldberg5,6, Nelson Ting1,2 1Department of Anthropology, University of Oregon, Eugene, OR, USA, 2Institute of Ecology and Evolution, University of Oregon, Eugene, OR, USA, 3Department of Anthropology and McGill School of Environment, Montreal, Quebec, Canada, 4Makerere University Biological Field Station, Fort Portal, Uganda, 5Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, USA, 6Global Health Institute, University of Wisconsin-Madison, Madison, WI, USA

Poster Session (1:30 – 3:00) 1. The effect of nocturnal competitors on common marmoset monkey (Callithrix jacchus) exudate feeding behavior

Lauren Gapp1; C.J. Vinyard2; L.C.O. Melo3; M.A.B. de Oliveira3; C.L. Thompson1

1Department of Biomedical Sciences, Grand Valley State University, 2Department of Anatomy & Neurobiology, Northeast Ohio Medical University, 3Departamento de Morfologia e Fisiologia Animal, Universidade Federal Rural de Pernambuco

2. Preliminary findings regarding the impact of zoo visitors on Japanese macaques’ (Macaca fuscata) performance on a touchscreen task

Sarah M. Huskisson*, Stephen R. Ross, and Lydia M. Hopper

8

Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, *shuskisson@lpzoo.org

3. Chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla gorilla), and Japanese macaque (Macaca fuscata) performance on a touchscreen risk preference task

Jesse G. Leinwand*, Crystal L. Egelkamp, Sarah M. Huskisson, Lydia M. Hopper Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, USA, *jleinwand@lpzoo.org

4. Differences in relationships between female Alouatta palliata with and without infants in Costa Rica

Christina Doelling1,2*, Laura Bolt2,3

1School of Professional Studies, Northwestern University, Evanston, IL, United States, 2Maderas Rainforest Conservancy, Limon Province, Costa Rica, 3Department of Anthropology, University of Toronto, Toronto, Ontario, Canada, *crdoelling@gmail.com

5. The link between pediatric respiratory viruses and disease in wild chimpanzees in Kibale National Park, Uganda

Taylor E. Weary*, Tony L. Goldberg Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, Wisconsin, *weary@wisc.edu

6. Evaluating novel welfare assessment methods in a sanctuary setting: linking thermal images of sanctuary-housed chimpanzees and their behavior

Benjamin Lake1,2, Lydia M. Hopper1, Stephen R. Ross1, Amy L. Fultz2

1Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, USA, 2Chimp Haven, Keithville, LA

7. Apes in film: A study of the effect of ape representations on audience perceptions of ape behavior and human attributes.

Emma Cieslik*, Kelly Boyer Ontl** Department of Anthropology, Ball State University, Muncie, IN, USA, *eocieslik@bsu.edu, **kmontl@bsu.edu

8. Variation in biomarkers of energetic condition of wild mother Bornean orangutans (Pongo pygmaeus wurmbii)

Timothy D. Bransford1,2,3*, Sri Suci Utami Atmoko4, Erin R. Vogel2,3 1Department of Anthropology, Northern Illinois University, USA, 2Department of Anthropology, Rutgers University, New Jersey, USA, 3The Center for Human Evolutionary Studies, Rutgers University, USA, 4Universitas Nasional, Jakarta, Indonesia, *tbransford.anthro@gmail.com

9. A comparison of wild and zoo activity budgets for five species of primates

9

Natasha K. Wierzal, Katherine A. Cronin, Jason D. Wark Animal Welfare Science Program, Lincoln Park Zoo, Chicago, IL

10. What costs do red colobus monkeys experience when forming mixed-species groups with Diana monkeys?

Joseph Geherty, W. Scott McGraw

Department of Anthropology, The Ohio State University, Columbus, OH, USA

11. New enamel 13C data from wild Ugandan chimpanzees (Pan troglodytes schweinfurthii)

permits the establishment of a hominoid-specific diet-to-enamel 13C offset value: Implications for fossil hominin dietary reconstructions

Maire Malone, John Kingston Department of Anthropology, University of Michigan, Ann Arbor, MI, USA

12. Prevalence of Cryptosporidium and Giardia infections amongst lemurs, humans, domestic mammals and invasive rats in Tsinjoarivo, Madagascar

Laurie A. Spencer1, Mitchell T. Irwin2 1Department of Biological Sciences, Northern Illinois University, DeKalb, IL, USA, 2Department of Anthropology, Northern Illinois University, DeKalb, IL, USA

13. Primate microbial endocrinology: An uncharted frontier

Kathryn M. Benavidez1, Michael D. Wasserman1,2,3 1Department of Anthropology, Indiana University, Bloomington, IN, USA, 2Center for the Integrative Study of Animal Behavior, Indiana University, Bloomington, IN, USA, 3Human Biology Program, Indiana University, Bloomington, IN, USA

14. Primate limb bone structure: Are gross behavioral categories less informative than number of loading cycles?

Tessa H. Cannon, W. Scott McGraw The Ohio State University, Department of Anthropology, Columbus, OH

15. The temporal and atmospheric context of howling behavior among mantled howler monkeys (Alouatta palliata) at La Suerte Biological Field Station

Emily L. Kosnik Grand Valley State University

16. Standing’s Lost Sunken Forest: A new excavation of the famous subfossil site of Ampasambazimba, Central Madagascar

Karen E. Samonds1*, Mitchell T. Irwin2 1 Department of Biological Sciences, Northern Illinois University, Dekalb, IL, USA, 2

Department of Anthropology, Northern Illinois University, Dekalb, IL, USA, *ksamonds@niu.edu

10

11

Gettin

g to

Eduard

o’s:

Leav

e campus to

the so

uth

and tu

rn left o

nto

Lin

coln

Hig

hw

ay. E

duard

o’s w

ill be o

n th

e

right sid

e of th

e street at th

e corn

er of L

inco

ln H

igh

way

and 2

nd S

t. It is 1 m

ile from

the

conferen

ce loca

tion (5

min

ute d

rive, 2

0 m

inute w

alk

), and street p

arkin

g is free.

12

PODIUM ABSTRACTS 1. Preference assessments as a tool to evaluate environmental enrichment

Jocelyn M. Woods1, Erin Lane2, Lance J. Miller1, 2

1Animal Welfare Research, Chicago Zoological Society, Brookfield, IL, USA, 2San Diego Zoo Institute for Conservation Research, Escondido, CA, USA

Preference assessments are a valuable tool which have been used to determine favorite items in humans and nonhuman animals. In the past, these assessments were predominantly used to evaluate preference in humans with behavioral disorders to utilize favorites as positive reinforcers for behavioral management. More recent research has conducted preference assessments in nonhuman animals ranging from red-billed hornbills to Western lowland gorillas for similar purposes. Not surprisingly, the majority of nonhuman animal preference studies have been conducted with primates to evaluate food preference for training purposes. The present study sought to expand the utilization of preference assessment by using it as a tool to formally evaluate preference of environmental enrichment in Sumatran tigers (Panthera tigris sumatrae, n=3), cheetahs (Acinonyx jubatus, n=2), and African lions (Panthera leo, n=3). To determine if their established preferences could predict long-term interaction with enrichment, the behavior of the African lions with enrichment items over the course of thirty, 24-hour trials was examined. General estimating equations revealed a 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 percent of hours interacted with the item in Study 2. The results support the idea that preference assessments can be used to predict the amount of interaction with enrichment over the course of time, with preferred items being interacted with more frequently and in longer duration. In the future, a similar study design that monitors which enrichment item was first approached could be implemented as a time and cost-effective way to empirically evaluate the efficacy of environmental enrichment in nonhuman primates. 2. Seasonal variation of microbiota and metabolome in fecal sample of golden snub-nosed monkeys (Rhinopithecus roxellanae)

Yan Zeng1*, Xueqin Ni1, Dong Zeng1, Lili Niu2, Jiabo Deng2, Weichao Zheng3, Yuanying Fan4, Yang Li1, Limin Kan3 1College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, China, 2Chengdu Wildlife Institute, Chengdu Zoo, 3Sichuan Tangjiahe National Nature Reserve, Guangyuan, China, 4Cangxi National Forest Park Administration, Sichuan, China, *zengyan1689@gmail.com

The metabolic activity of the mammalian gut microbiota plays a crucial role in the digestion and absorption of host nutrients. This is particularly true for primates such as the golden snub-nosed monkey (Rhinopithecus roxellanae), a folivorous primate with marked seasonal dietary variation. However, the metabolic activity of the golden monkey gut microbiota remains unknown. Here, we examined the composition and function of the fecal microbiota of wild and

13

captive golden monkeys across seasons by using 16S rRNA amplicon sequencing, metagenomics, and metabolomics. We observed significant seasonal variation of microbiota and metabolites. For example, in autumn and winter, Firmicutes, Verrucomicrobia, and Rumiococcaceae were in higher abundance in wild individuals. In spring and summer, Gammaproteobacteria dominated in captive individuals. Additionally, acetate and glucose were important metabolites in the wild individuals in summer. Notably, glutamate, a major metabolite involved in the metabolism of D-Glutamine and D-glutamate, was obtained from captive monkeys in winter. These data indicate that there are more beneficial microbiome and metabolites found in wild golden monkeys with seasonal differences. Therefore, we need to improve the dietary composition of captive golden monkeys based on nutritional requirements. 3. Auditory enrichment for captive red howler monkeys (Alouatta seniculus) using numeric odds to simulate choice.

Maggie Ramont1, Holly Farmer1,2, Emile Prins3 1Zoo Conservation Biology MSc program, Plymouth University, Plymouth, UK, 2Research Department, Wild Planet Trust/Paignton Zoo, Paignton, UK, 3Zoological Research, Gaia Zoo, Kerkrade, NL

Howling and other territorial responses are integral to the behavioral repertoire of wild red howler monkeys (Alouatta seniculus) but are performed less often in captivity. Our study focuses on evaluating the use of conspecific calls as a source of ecologically relevant auditory enrichment by 1) comparing the behavioral responses of three captive groups to four different auditory stimuli, and 2) comparing their behavioral responses to conspecific calls from different sized groups to determine whether they evaluate group size and factor their odds of winning against the simulated rivals in a vocal “battle”. We recorded self-directed behaviors (SDBs) and territorial behaviors using continuous sampling methods and analyzed our results using generalized linear models (GLMs). Results showed conspecific calls and calls from another Alouatta species elicited significantly more SDBs and territorial behavior, supporting the conclusion that they are the most ecologically relevant to our focal groups. Results also highlighted significant differences in behaviors performed during conspecific calls from different sized groups, suggesting that captive red howler monkeys can evaluate their “numeric odds” of winning a territorial howl bout and adjust their behavior accordingly. These results highlight the importance of using ecologically relevant stimuli in auditory enrichment, and the importance of applying that stimuli in the proper context to not only elicit natural behavior but also to provide choice and control in the performance of those natural behaviors in captivity; more research is necessary to explore the potential to increase welfare in captive populations using these methods.

14

4. Novel application of point-of-care technology for real-time health monitoring in Platyrrhines

Alexandra Sacco*1,2, Gideon Erkenswick3,4, April K. Binder2,5, Ana Priscila Peralta Aguilar3, Raul Bello6,7, Mrinalini Watsa1,3 1Department of Anthropology, Washington University, St. Louis, MO, 2Primate Behavior Program, Central Washington University, Ellensburg, WA, 3Field Projects International, St. Louis, MO, 4Department of Infectious Diseases, Washington University School of Medicine, St. Louis, MO, 5 Department of Biological Sciences, Central Washington University, Ellensburg, WA, 6 Taricaya Rescue Center, Puerto Maldonado, Perú 7 Kawsay Biological Station, Madre de Dios, Perú *alexandra.sacco@wustl.edu

There is a growing need for real-time health monitoring methods in the Neotropics as non-human primates confiscated from the illegal wildlife trade are overcrowding rescue centers where they are likely exposed to novel pathogens. Their eventual rehabilitation and release exposes wild conspecifics to these pathogens as a result of a critical deficiency in health screening requirements and lack of baseline health data available. We utilized an affordable point-of-care (POC) device designed for use in humans, the Keto-Mojo, to evaluate blood chemistry in free-ranging emperor tamarins (Saguinus imperator), saddleback tamarins (Leontocebus weddelli), and brown titi monkeys (Plecturocebus toppini) in the Madre de Dios Department of southeast Perú, as well as captive Peruvian spider monkeys (Ateles chamek), black-headed night monkey (Aotus nigriceps), Colombian red howler monkeys (Alouatta seniculus), and yellow-tailed woolly monkeys (Oreonax flavicauda) housed at Taricaya Reserva Ecológica in Puerto Maldonado, Perú. Additionally, we utilized multireagent urinary dipsticks to evaluate nutritional condition in free-ranging S. imperator and L. weddelli. The Keto-Mojo reliably recorded blood glucose, hematocrit, hemoglobin, and ketones in all study species. Blood samples analyzed in duplicate showed no significant variation, suggesting that this device produces results with high reliability. The results from the urinary dipsticks indicated that the normal ranges of urinary parameters for S. imperator and L. weddelli fell within the range of humans, as their “normal” was considered clinically healthy for human urine. While both POC technologies are designed for use in humans, our results suggest that they can be effectively applied to primate health monitoring initiatives and facilitate the establishment of reference health data. 5. Immunofunction and reproductive effort in wild chimpanzees: Field evidence for immunomodulation by gonadal steroids

Jacob D. Negrey1* 1Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, WI, USA, *negrey@wisc.edu

In primates and other mammals, gonadal steroid hormones are hypothesized to mediate trade-offs between immunofunction and reproduction. However, evidence for immunomodulation by gonadal steroids in free-ranging mammalian populations is mixed, owing not only to difficulty measuring immune challenge but also inter-individual differences in basal and reactive analyte

15

concentrations. To test this hypothesis in wild chimpanzees (Pan troglodytes schweinfurthii), I assessed within-individual variation in urinary gonadal steroids—testosterone in males, and estradiol, estrone, and pregnanediol in females—as predictors of urinary neopterin, a biomarker of innate immune challenge. I also tested if the relationship between gonadal steroids and neopterin differed between apparently healthy and severely ill or injured individuals. I analyzed 654 urine samples from 79 adult chimpanzees (45 females, 34 males) in the Ngogo community of Kibale National Park, Uganda. In apparently healthy males, urinary testosterone significantly positively predicted neopterin; in females, estradiol and estrone, but not pregnanediol, positively predicted neopterin. Testosterone exhibited the strongest correlation with neopterin (rrm = 0.39), followed by estrone (rrm = 0.34). During illness and injury, chimpanzees exhibited higher neopterin. In contrast, ill and injured males exhibited significantly lower testosterone, while females exhibited significantly lower estrone and pregnanediol. These results support a trade-off between innate immunofunction and reproductive effort modulated, in part, by gonadal sex steroids: reproductive investment incurs immune costs, and severe immune challenge necessitates downregulated reproductive investment. Furthermore, these results support experimental studies of other mammalian species indicating that testosterone exerts stronger immunosuppressive effects than do some ovarian hormones, and that ovarian hormones vary in their immunomodulatory effects. 6. Constructing an expanded social niche: A captive chimpanzee social network inclusive of human caregivers

Jake A. Funkhouser1,2*, Jessica A. Mayhew2,3, John B. Mulcahy2,3,4, and Lori K. Sheeran2,3

1Anthropology Department, Washington University in St. Louis, St. Louis, MO, USA, 2Primate Behavior Program, Central Washington University, Ellensburg, WA, USA, 3Department of Anthropology and Museum Studies, Central Washington University, Ellensburg, WA, USA, 4Chimpanzee Sanctuary Northwest, Cle Elum, WA, USA, *jakefunkhouser@wustl.edu

In a captive environment, it is difficult to provide opportunities for chimpanzee-typical social group composition, diversity, and overall structure (e.g., fission-fusion). In these situations, captive individuals are often regarded as living in closed social niches (i.e., fixed composition, few opportunities to forge novel relationships). For chimpanzees specifically, there is a growing need to meet the species’ social requirements within the constraints of captivity for individuals housed in expanding sanctuaries, zoos, rehabilitation centers, and laboratories. In this investigation, we expand on the current literature regarding captive chimpanzee social networks by uniquely expanding their social niche to consider human caregivers as potential social partners. We collected nearest neighbor associations with grooming and agonistic interactions between captive chimpanzees (Pan troglodytes; N=7) and with their human caregivers (N=6) at Chimpanzee Sanctuary Northwest (CSNW) in Washington, USA from June to August 2017. By analyzing these multidimensional social networks through multiple statistical measures, our results indicate that human caregivers act as integrated – rather than isolate – actors in the chimpanzees’ expanded social niche. Further, our results illuminate interindividual differences in the type and strength of chimpanzee-human relationships. These results cast

16

substantial weight when considering all possible constituent actors in captive chimpanzees’ social niches, whether that be the size, composition, diversity, context, or opportunities across multiple social networks. Such holistic considerations of captive social systems must now include the possibility of human caregivers (or other individuals) as potentially impactful social partners within these social niches. Our discussion bears influence on understanding the mechanisms that underlie the construction of interindividual and interspecific social relationships, as well as address captive welfare, health, translocation, and husbandry protocols across nonhuman primate settings. 7. Evaluating the impact of sustainable land-use changes on perceptions of wildlife conservation around Kibale National Park in western Uganda

Lev A. Kolinski1, Krista M. Milich1 1Department of Anthropology, Washington University in St. Louis

Around Kibale National Park (KNP) in western Uganda, communities regularly face the threat of crop raiding from wildlife, including from a variety of endangered species such as African elephants (Loxodonta africana), common chimpanzees (Pan troglodytes), and red colobus monkeys (Piliocolobus tephrosceles), as well as other nonhuman primates including olive baboons (Papio anubis). These frequent negative interactions with wildlife lead many community members to resent the park and the animals that live in it. To mitigate these issues, community members around KNP partnered with researchers to start a participatory action research project: Conservation to Coexist. The project involves testing four sustainable land-use changes: digging and maintaining trenches around the park border, installing beehive fences in swampy areas where trenches could not be dug, planting tea as a buffer, and growing garlic as a cash crop. While there is quantitative data to show that crop raiding frequency has decreased as a result of Conservation to Coexist’s land-use changes, little has been done to examine any changes in community members’ perceptions of the park and biodiversity conservation. Using surveys, we interviewed both Conservation to Coexist participants and nonparticipants living in households bordering KNP to determine the impact of sustainable land-use changes on attitudes towards KNP, wildlife officials, animal species, and environmental conservation. We found that there is a positive correlation between participation in Conservation to Coexist and perceived benefits form living near KNP. We also found that respondents who participated in Conservation to Coexist reported more positive feelings about the Uganda Wildlife Authority, the organization that oversees KNP. With these results, we discuss ways of improving future conservation initiatives.

17

8. Shifting agriculture’s effects on crowned lemur and Sanford’s lemur ecology in a Malagasy forest fragment

Benjamin Z. Freed1 1Department of Anthropology, Sociology, and Social Work, Eastern Kentucky University, Richmond, KY, USA, *Benjamin.Freed@eku.edu

Perhaps even more than in rain forests, the ranging, feeding behavior, and predator protection of primate communities may vary greatly with how close to humans primates in forest fragments live. We collected behavioral data on two crowned lemur groups (Eulemur coronatus) and one Sanford’s lemur group (Eulemur sanfordi) in a forest fragment they share with local farmers. We compare the lemurs’ dry season ecology between 2016 (in the presence of two neighboring farmers, n=140 hours) and 2017 (in the presence of one neighboring farmer, n=240 hours). At least seven other farming families lived within three kilometers of these lemurs. In both years, both lemur species relied on clumped arboreal resources (Ficus) and superabundant unripened fruit from the bush, Lantana camara. After one of the two farmers moved, whereas crowned groups ranged similarly, five of 2016’s six Sanford’s groups shifted their home ranges away from the abandoned farm. Compared with 2016 results, one crowned group and the Sanford’s group spent more daytime resting (more than 77% of each day), while presumably eating Ceiba nectar nocturnally. Finally, predator pressure increased, as fewer people actively prevented the trapping of lemurs. These results point to a close association between humans (of certain traditions) and lemurs, and may also be evidence of greater behavioral flexibility than previously observed in a larger rain forest.

Funding for this work was provided by Eastern Kentucky University's Faculty Mini-Grant program and it’s Education Abroad Office. 9. Anthropogenic food enhancement alters the timing of reproductive onset among wild savanna monkeys

Alicia M. Rich1, Stacy-Anne R. Parke1, Maryjka B. Blaszczyk2, Jennifer Danzy Cramer3, Joseph Lorenz4, Nelson B. Freimer5, J. Paul Grobler6, Trudy R. Turner7, Christopher A. Schmitt1 1Department of Anthropology, Boston University, Boston MA, 2Department of Anthropology, University of Texas Austin, Austin TX, 3Department of Sociology and Anthropology, American Public University, Charles Town, WV, 4Department of Anthropology and Museum Studies, Central Washington University, Ellensburg, WA, 5Brain Research Institute, University of California Los Angeles, Los Angeles, CA, 6Department of Genetics, University of the Free State, Bloemfontein, FS, South Africa, 7University of Wisconsin Milwaukee, Milwaukee, WI

Proximity to anthropogenically food-enhanced landscapes can have a large effect on the fitness of synanthropic wildlife. This issue is of immediate relevance because anthropogenic habitats increasingly dominate nonhuman primate landscapes. Given their ubiquity on both farms and nature reserves, South African vervet monkeys (Chlorocebus pygerythrus) provide an excellent model system to test these effects. We investigated whether free-ranging vervets on a private

18

farm in !Gariep Dam with access to ample anthropogenic foods show predicted patterns of early reproductive maturation compared to wild-foraging vervets in Soetdoring Nature Reserve. Vervets in !Gariep show significantly thicker skin folds (above umblicus, p < 0.001; subscapular, p < 0.001; subrailiac, p < 0.01) than in Soetdoring, suggesting increased fat deposition. In males, logistic regression models show significantly larger relative testis volume at peri-pubescent ages in !Gariep compared to Soetdoring (age category 5: β=0.637, p=0.05; age category 6: β=0.942, p<0.05), suggesting early reproductive maturation. Ordinal logistic regressions of parity status based on nipple length in females similarly suggest an earlier onset of reproduction, with younger age categories (4 and 5) in !Gariep showing signs of parity (age category 4: β=42.137, p<0.001; age category 5: β=43.094, p<0.001), but not in Soetdoring. These results are consistent with a positive effect of anthropogenic food-enhancement on body fat deposition, potentially linked to an earlier onset of reproductive maturation. Further investigation into primate responses to cultivated resources will inform our understanding of the broader effects of food enhancement on developmental plasticity. 10. Voices of the Forest: A shorfilm on the Black Howler Monkey (Alouatta pigra) conservation efforts in southern Mexico

Jorge Ramos-Luna1,2*, Juan Carlos Serio-Silva1,2, Francisca Vidal-García1,2, Daniela Alicia Torres Anaya1,2 1Red de Biología y Conservación de Vertebrados, Instituto de Ecología, A.C., Xalapa, Veracruz, México, 2Grupo de Estudios Transdisciplinarios en Primatología, Xalapa, Veracruz, México, * jor_ge_94@hotmail.com

In the southern state of Tabasco, Mexico, black howler monkeys (Alouatta pigra) are in constant antropogenic pressures due to the loss of their habitat. In order to mitigate the impact of these threats, the “Grupo de Estudios Transdisciplinarios en Primatología” has established the “Estación de Investigación Primatológica y Vida Silvestre” as a base of operation for research projects in the municipality of Balancán. For over a decade, this station has allowed for the development of a multitude of research projects, conservation education interventions and field courses, focused on the ecology, behaviour, human interaction and conservation of this primate species. Due to the close relation that the research group has mantained through the years with the owners of the land in which the station was built (the Tejero family), a wildlife documentary shortfilm was filmed to portray the impact that the different primatological activities surrounding the station have had on the locals. Technical aspects: Length: 14:47 minutes Country of production: Mexico Language: Spanish with English subtitles Production date: 09/March/2019 Link: https://youtu.be/eeau11J6DLg

19

11. Sperm morphological differences in two species of wild howler monkey (Alouatta palliata & A. pigra)

Molly A. Hirst1, Alba Z. Rodas-Martínez2, Marcella D. Baiz1,3, Liliana Cortés-Ortiz1 1Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 2División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, 86150 Villahermosa, Tab., México, 3Department of Biology, Pennsylvania State University, State College, PA

Sperm morphological variation is highly species-specific, resulting from the rapid evolution of sperm traits partly due to intense pressures from sexual selection via sperm competition. This is particularly evident in polyandrous taxa where sperm from multiple males compete for access to a female’s ovum. In polyandrous taxa, there is greater selective pressure for males to evolve sperm traits such as larger midpiece size and tail length, which are directly correlated with swimming speed and the likelihood of the sperm reaching an ovum. We sought to determine the extent of species-specific differences in sperm morphology between two closely-related howler monkey species (Alouatta palliata & A. pigra) that diverged ~3MA and that have different mating systems. Because A. palliata groups are more polyandrous, we expected sperm morphological differences to manifest in traits such as larger midpiece size and longer tails in this species. To address this, we collected semen and prepared sperm slides for four wild individuals with known non-admixed genotypes; two A. palliata and two A. pigra. We photographed sperm with a Celestron digital microscope camera and used ImageJ to measure ten morphometric parameters from the head, midpiece, and tail of 100 sperm per individual. Using a linear mixed model, we assessed variation in sperm morphometric parameters between species and within individuals. With the limited sample size, we found evidence of individual variation in several parameters, but species-specific variation was only significant in the midpiece length in A. palliata, suggesting selection for greater mitochondrial load and thus faster sperm in this species. Future analyses will include additional non-admixed individuals as well as their hybrids to elucidate patterns of variation in sperm morphology in this system. 12. Socioecological Predictors of Health Profiles in Western Lowland Gorillas

Kristena Cooksey1, Crickette Sanz1,2, Jean Marie Massamba2, Thierry Fabrice Ebombi2, Prospère Teberd2, Espoir Magema2, Gaston Abea2, Juan Salvador Ortega Peralejo2, Ivonne Kienast2, Colleen Stephens1, David Morgan2,3 1Department of Anthropology, Washington University in Saint Louis, Saint Louis, MO, U.S.A.;2Wildlife Conservation Society, Congo Program, Brazzaville, Republic of Congo; 3Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, U.S.A.

Socioecological factors are linked to health outcomes, overall health profiles, and disease transmission in primates. Due to their close phylogenetic relatedness to humans, great apes are particularly susceptible to anthropogenic disease infection. Infectious diseases have been documented in wild gorilla populations that have manifested varying patterns of disease prevalence that may be attributable to differences in social groupings and patterns of intergroup contact. We assess a suite of potential socioecological predictors of health

20

incidences across four groups of western lowland gorilla (Gorilla gorilla gorilla) in northern Republic of Congo. Observational health assessments were conducted during daily follows of focal gorilla groups in the Goualougo and Djeke Triangles from April 2014 to July 2019. While overall presence of disease was relatively low, we detected several respiratory episodes and chronic health issues within the focal population. Based on the observed dynamics of disease spread, we discuss probable mechanisms of transmission within and between groups. Further, we suggest that identification of the specific predictors and modes of disease transmission can be used to mitigate some specific health risks. Recommendations for best practices and management protocols are presented as they relate to improving health profiles in gorillas. 13. Folivore rules and frugivore rules: Variation in diet, foraging effort and nutritional intake in the frugivorous brown lemur (Eulemur fulvus) and a sympatric folivore (Propithecus diadema)

Irwin, Mitchell T1,3*, Rahalinarivo, Vololonirina2, Raharison, Jean-Luc3, Ramorasata, Bruno3, Ranaivoarisoa, Jean-Freddy2, Randrianasy, Jeannot2, Rothman, Jessica M4,5 1Department of Anthropology, Northern Illinois University, DeKalb, IL, USA, 2Mention Anthropobiologie et Développment Durable, University of Antananarivo, Antananarivo, Madagascar, 3ONG SADABE, Antananarivo, Madagascar, 4Department of Anthropology, Hunter College, 5Graduate Center, CUNY *mirwin@niu.edu

Many socioecological models divide primates following broad dietary categories (frugivores, folivores, insectivores) but primatologists have rarely tested assumptions about the homogeneity of those groups, especially across taxa. We also know little about which particular nutrients drive foraging choices, and how this varies across clades and diet types. We studied the diet and food chemistry of the folivorous sifaka (Propithecus diadema) at Tsinjoarivo, Madagascar, and sympatric, frugivorous brown lemurs (Eulemur fulvus). Sifakas prefer fruits when available, and achieve highest nutritional intakes in fruit-rich months. Sifakas’ feeding effort and intakes crash during high-folivory lean season months (possibly because leaves cause higher PSM burdens), while brown lemurs remain frugivorous and increase feeding effort, presumably “sticking to fruit” despite lower fruit availability and/or quality. The species’ foods are surprisingly similar in fiber (~40% NDF), and available protein (AvailN, 4.7 vs. 5.6%), but brown lemur foods are higher in water-soluble sugars (11.6 vs 6.0%). Considering leaves only (14% of brown lemur diet; 54% of sifaka diet), niche separation is extreme. Sifakas consumed 83 species and brown lemurs consumed 54; 27 were nominally shared, but no shared species contributed >0.2% of feeding time for both species – they don’t eat each other’s’ leaves. Brown lemur leaves were higher in AvailN, NDF and simple sugars, but lower in tannins (i.e. higher quality). Such a difference may be expected in averages if sifakas had a broader range of tolerance, but strangely, sifakas never ate the highest-quality leaves consumed by brown lemurs. Further research is necessary to examine which nutrients are prioritized by lemurs, why sympatric species differ so drastically in leaf selection, and to compare lemur dietary strategies to those of monkeys and apes.

21

14. Evaluating the sensitivity hypothesis: Are spider monkeys (Ateles geoffroyi) an ideal indicator species compared to sympatric primates in Eastern Costa Rica?

Michelle A. Rodrigues1*, Tracie McKinney2, Jill D. Pruetz3, Stacy M. Lindshield4

1Beckman Institute for Science and Technology, University of Illinois, Urbana-Champaign, IL, USA, 2University of South Wales, Pontypridd, Wales, UK, 3Texas State University-San Marcos, San Marcos, TX, USA, 4Department of Anthropology, Purdue University, West Lafayette, IN, USA, *michellespidermonkey@gmail.com

Geoffroy’s spider monkeys (Ateles geoffroyi) have rapidly declined and are now one of the Top 25 most endangered primates. Throughout their range, members of the Ateles genus are considered indicator species due to their frugivorous diet, need for large tracts of forest, and status as a preferred game animal in some locations. However, primates may vary in their responses to anthropogenic land usage. Here, we examine the population size and distribution of spider monkeys living under different complexes of anthropogenic land usage in comparison to sympatric howler (Alouatta palliata) and capuchin monkeys (Cebus imitator). We found that spider monkeys thrived in a large private reserve where monkeys were protected within a mosaic landscape of primarily agricultural usage. Spider monkeys had a population density of 22.6 individuals/km2, capuchin monkeys had a density of 30.4 individuals/km2, and howler monkeys had a density of 50.2 individuals/km2. Conversely, at a coastal site that had a mosaic of protected land and unprotected land subject to peri-urban development related to the tourism industry, howler monkeys thrived (density=12.0 individuals/km2), but spider monkeys (0.9 individuals/km2) and capuchin monkeys (1.1 individuals/km2) were found at low densities. We conclude that spider monkeys can serve as an important indicator of ecosystem health within a complex of anthropogenic land usage, but that capuchin monkeys are sensitive to disturbance as well. Rather than using a single indicator species, assessing the response of multiple species to disturbance may be more useful in assessing the impact of different types of working landscape usage in couple human-natural systems. 15. Interactions among microbial communities in the gut of long-tailed macaques (Macaca fascicularis) in Southeast Asia

Chissa-Louise Rivaldi1*, Audrey Arner2, Hope Hollocher1 1Department of Biological Sciences, University of Notre Dame, 2Pennsylvania State University, *crivaldi@nd.edu

Host-associated microbial communities influence a range of important biological functions, including host development, metabolism, and immune defenses. Several factors govern the assemblage of different microbial communities, such as host traits, environment, diet, and interactions with eukaryotic gut parasites – a relationship that is understudied. It has been hypothesized that parasite infections can have profound influences on prokaryotic richness and diversity through the action of different ecological mechanisms (e.g. top-down processes as mediated through host immune responses and bottom-up processes governed by competition and resource flux through the gut). Here we characterize the prokaryotic and eukaryotic members of the gut microbial communities of long-tailed macaques on the islands of Singapore

22

and Bali using amplicon sequencing, focusing on the variation found within and between sampling sites. We then identify the prokaryotic taxa associated with the presence of the protozoan Blastocystis, and computationally infer the functional roles of these taxa. Delineating potential ecological interactions between prokaryotic microbiota and eukaryotic parasites presents a path forward for understanding how prokaryotic community structure may serve to block or enhance the invasion of the gut by more pathogenic organisms, which has important implications for coinfection dynamics and primate health. 16. Effects of Environment and Relatedness on the Gut Microbiome of Ugandan red colobus monkeys

Tabor Whitney1, Maria J. Ruiz-Lopez2, Diana M. Christie1,2, Colin A. Chapman3,4, Tony L. Goldberg5,6, Nelson Ting1,2 1Department of Anthropology, University of Oregon, Eugene, OR, USA, 2Institute of Ecology and Evolution, University of Oregon, Eugene, OR, USA, 3Department of Anthropology and McGill School of Environment, Montreal, Quebec, Canada, 4Makerere University Biological Field Station, Fort Portal, Uganda, 5Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, USA, 6Global Health Institute, University of Wisconsin-Madison, Madison, WI, USA

The gut microbiome consists of microbial communities that reside in the gastro-intestinal tract of living organisms. Variation in this system has been linked to health outcomes in human and animal models by affecting digestion, immune system development, and pathogen invasion. However, we still lack a complete understanding of the factors that shape gut microbiome variation, particularly in wild primates. The central aim of this research is to determine which factors are predicting inter-individual variation in the gut microbiome of Ugandan red colobus monkeys (Piliocolobus tephrosceles). We sequenced the 16S rRNA hypervariable V-4 region to characterize the gut microbiome from 102 genotyped individuals across eight social groups inhabiting different forest types within Kibale National Park and its surrounding area. We assessed the effect of shared environment, geographical distance, genetic relatedness, and forest type on both alpha and beta diversity of the red colobus monkeys. We found that all four factors have a significant role in predicting gut microbiome composition, or beta diversity, with environmental factors playing a larger role than relatedness. We also found that social groups residing in disturbed forests have a significantly lower alpha diversity than those residing in undisturbed forests. Our research thus reinforces the role that environment plays in shaping within-species gut microbial variation with potential implications for the conservation of threatened populations in disturbed landscapes.

23

POSTER ABSTRACTS 1. The effect of nocturnal competitors on common marmoset monkey (Callithrix jacchus) exudate feeding behavior

Lauren Gapp1; C.J. Vinyard2; L.C.O. Melo3; M.A.B. de Oliveira3; C.L. Thompson1

1Department of Biomedical Sciences, Grand Valley State University, 2Department of Anatomy & Neurobiology, Northeast Ohio Medical University, 3Departamento de Morfologia e Fisiologia Animal, Universidade Federal Rural de Pernambuco

Marmoset monkeys obtain food by gouging holes in trees to stimulate exudate secretion. Although marmosets are among the few mammalian species who consume exudate, there is limited evidence that they may face competition from nocturnal foragers such as possums and rodents. We studied wild common marmoset monkeys (Callithrix jacchus) at Tapacurá Field Station in Brazil and used camera traps to monitor animal visits at exudate feeding sites. We assessed revisitation rates and latency between feeding visits to identify if marmosets changed their feeding behavior in the presence of nocturnal foragers. We documented nocturnal visits to exudate holes from four non-primate species. Marmosets had higher revisitation rates for feeding sites that were shared with other species compared to sites that were not. Across all feeding sites, marmosets had significantly higher revisitation rates and smaller time spans between feeding visits after a nocturnal forager had visited the night before. These trends remained the same when examining competition at our single feeding site with nocturnal foragers, however were no longer significant. Marmoset exudate consumption varied among sites, with the shared site having a higher baseline exudate production. This provides some evidence that marmoset monkeys change their feeding behavior when a nocturnal forager is present. However, our results suggest that the negative effects of competition may be ameliorated by high food volume at sites shared with these nocturnal foragers. 2. Preliminary findings regarding the impact of zoo visitors on Japanese macaques’ (Macaca fuscata) performance on a touchscreen task

Sarah M. Huskisson*, Stephen R. Ross, and Lydia M. Hopper

Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, *shuskisson@lpzoo.org

Zoos are large-scale forums for research, education, and engagement, but the presence of visitors can influence the animals they house. Given the public-facing nature of Lincoln Park Zoo’s cognitive research program and that guests can closely gather around the testing area, we sought to evaluate the impact of visitors on the performance of four Japanese macaques (Macaca fuscata) in a touchscreen match-to-sample task. Previous work has demonstrated some negative influence of zoo visitors on primate behavior, however, data is mixed. Since we have not seen evidence of such an impact at Lincoln Park Zoo, we predicted that monkeys’ performance would not change with increasing visitors and activity. The number of visitors (categorized as 0-19, 20-40, and 41+) and visitor activity (calm, moderate, frenetic) were recorded at the beginning of each monkey’s test session. The monkeys completed an average of

24

10.1 trials/session (s.d.=2.66) and, to date, have completed 4587 trials. Subjects completed the majority of trials under the “moderate” activity condition (47%) and when there were 20-40 guests present (58%). Using a generalized linear mixed model analysis, we found the monkeys’ accuracy was lowest when activity levels were moderate and there were 0-40 visitors (p=0.03). We also saw a tendency for monkeys’ average response latencies to decrease with increasing activity and increasing visitor counts. These initial findings seem to contradict our initial hypotheses though expanding our sample size will confirm if these trends are valid. Building from this preliminary data, we may better understand the nuanced ways that zoo visitors impact monkeys’ emotional and cognitive states and thus be better equipped to accommodate animal needs in variable environments. 3. Chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla gorilla), and Japanese macaque (Macaca fuscata) performance on a touchscreen risk preference task

Jesse G. Leinwand*, Crystal L. Egelkamp, Sarah M. Huskisson, Lydia M. Hopper Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, USA, *jleinwand@lpzoo.org

Despite most humans being risk averse, we sometimes act against our own economic interests, such as when gambling. To explore the evolutionary origins of this, and inspired by the manual “Primate Gambling Task,” we developed a touchscreen risk preference task for use with primates. We tested 12 zoo-housed primates (chimpanzees, gorillas, Japanese macaques) in three payout conditions in which they could receive differently-valued foods at variable ratios (we determined each subject’s relative food valuations through previously-administered preference tests). In each trial, subjects saw pairs of stimuli representing either high value, high variance (HV), or low value, low variance (LV) payoffs. Selecting the LV always yielded a reward, whereas selecting the HV resulting in either the most-preferred reward or no reward. Considering reward-quality net payoff, in the 60-10 condition, LV>HV; in the 50-50 condition, HV>LV; and in the 90-20 condition, LV=HV. Subjects completed 100 trials per condition, with conditions counterbalanced across subjects. We calculated subjects’ cumulative performance index (CPI) across trials to determine whether they learned to preferentially select the HV or LV, and ran GLMMs to further assess choices by trial and individual. CPIs indicated that all subjects, regardless of species, either showed no learning or learned to prefer the LV option. However, GLMMs revealed that trial order was not significant for any species, though the rate at which the gorillas and macaques, but not chimpanzees, selected the LV did vary by subject, highlighting individual variation in risk preference. Overall, we found substantial intra- and inter-species differences, and our results suggest that touchscreens are an effective method for testing primates’ risk preferences, though quantitatively-different food rewards may be more appropriate for risk preference research.

25

4. Differences in relationships between female Alouatta palliata with and without infants in Costa Rica

Christina Doelling1,2*, Laura Bolt2,3

1School of Professional Studies, Northwestern University, Evanston, IL, United States, 2Maderas Rainforest Conservancy, Limon Province, Costa Rica, 3Department of Anthropology, University of Toronto, Toronto, Ontario, Canada, *crdoelling@gmail.com

For group-living animals with bisexual dispersal, adult social bonds are likely to be strongest between males and females. Mantled howler monkeys (Alouatta palliata) live in social groups where adults engage in alloparenting and infanticide. Females with infants were expected to have closer bonds with males than other females to prevent infanticide. We predicted that females with infants would have males in close proximity and as nearest neighbors more often than females without infants. We collected 20 hours of focal data on howler monkeys at La Suerte Biological Station, Costa Rica, in January 2019. We used 30-min focal point sampling, with points taken each 2 minutes for nearest neighbor sex and distance. We found that females with infants had males as nearest neighbors less often than expected, while other females had males as neighbors more than expected (p< 0.05). Females with infants were in closer proximity to all female nearest neighbors than males (p< 0.05), while females without infants were closer to males and females with infants than other females (p< 0.05). Females with infants may seek close proximity to other females due to the adaptive benefits of alloparenting. 5. The link between pediatric respiratory viruses and disease in wild chimpanzees in Kibale National Park, Uganda

Taylor E. Weary*, Tony L. Goldberg Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, Wisconsin, *weary@wisc.edu

Respiratory disease is one of the leading causes of death among wild chimpanzees (Pan troglodytes schweinfurthii) of the Kanyawara community living in Kibale National Park. Over the past 30 years, respiratory disease has accounted for 59% of deaths of known causes and 27% of all deaths, and outbreaks have led to mortality rates of up to 10%. Several studies have identified the causative agents as “common cold” viruses that generally circulate among human children without causing serious disease. We are investigating how these benign pediatric human viruses are transmitted to chimpanzees in Kibale so that we may better protect them from future outbreaks. We are collecting nasal swabs from children in local communities as well as adults living and working in the park, using a prospective cohort study design to be conducted over the course of one year. Using highly multiplexed PCR assays for common human respiratory disease pathogens, we will compare the viruses we detect in human nasal swabs to viruses we detect in time-matched chimpanzee fecal samples in order to determine if respiratory viruses in the human and chimpanzee populations are epidemiologically linked. The results from this study may have significant implications for the conservation of endangered great ape species as we aim to understand and prevent “reverse zoonotic” transmission of potentially lethal human pathogens to our closest relatives.

26

6. Evaluating novel welfare assessment methods in a sanctuary setting: linking thermal images of sanctuary-housed chimpanzees and their behavior

Benjamin Lake1,2, Lydia M. Hopper1, Stephen R. Ross1, Amy L. Fultz2

1Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, USA, 2Chimp Haven, Keithville, LA

A typical method to assess animal welfare is through the use of behavioral observations. However, in recent years a range of novel non-invasive methods for welfare assessment have been evaluated, including measures of mood, physiological function, and, more recently, using thermal imaging cameras. We evaluated the feasibility of augmenting typical behavioral monitoring with thermal imaging. Considering primates, researchers have used thermal imaging to assess apparent emotional responses to conspecifics’ vocalizations and enrichment but, to date, no study has directly combined thermal imaging measures with behavioral observations to formally evaluate the potential of this tool to monitor chimpanzee (Pan troglodytes) welfare on a regular, real time basis. Building on methodological progress in both laboratory and wild settings, we aim to evaluate if, and how, data from a thermal camera (FLIR E60) might be used to monitor the welfare of sanctuary-housed chimpanzees. In combination with behavioral data (ZooMonitor). We are monitoring four chimpanzee groups (N=30) at Chimp Haven, the federal chimpanzee sanctuary in Louisiana, who live in several different kinds of enclosures ranging from multi-acre forested yards to more moderately-sized meshed-in enclosures. Importantly, thermal imaging data are collected in conjunction with focal follow data, matching thermal photos to every behavioral interval data point. We aim to determine the potential of thermal data to be sensitive to acute and chronic changes in response to everyday events, ranging from disruptions in social groups to the distribution of enrichment. Empirical evaluation of novel assessment tools helps progress our ability to monitor the welfare of animals in a range of settings, and provides new opportunities to enhance their management and care. 7. Apes in film: A study of the effect of ape representations on audience perceptions of ape behavior and human attributes.

Emma Cieslik*, Kelly Boyer Ontl** Department of Anthropology, Ball State University, Muncie, IN, USA, *eocieslik@bsu.edu, **kmontl@bsu.edu

In Western society, animal representations in film evoke powerful questions about the human/animal divide. A prime example is the depiction of apes as fictional characters and actors in twentieth and twenty-first century film. This study examined the portrayals of nonhuman great apes in King Kong (2005), Project Nim (2011), and War for the Planet of the Apes (2017) and their influence on audience perceptions of apes and “humanness.” The authors analyzed the three films and discovered three prevalent features – violence, mercy, and theory of mind. Next, we explored the audience’s responses to the films by coding 745 critic reviews for the three films from the film review website Rotten Tomatoes® to determine the frequency of reviews discussing apes, whether or not these apes and the humans they engage with are shown in a positive or negative light, and how these three films represent the author’s three

27

features of violence, mercy, and theory of mind. The results showed that while critics did view the apes as violent or monstrous in the first film, Kong’s tender relationship with human Ann as well as Caesar and Nim’s struggle to fend off human combatants and experimenters affected how audiences discussed the “humanness” of the apes. This is critical because the way that ape representations influence audience’s understanding of apes may impact public support for the Great Ape Rights movement, an Animal Liberation effort to create legislation extending human rights to nonhuman apes, as well as conservation efforts and use of nonhuman great ape in medical experimentation. 8. Variation in biomarkers of energetic condition of wild mother Bornean orangutans (Pongo pygmaeus wurmbii)

Timothy D. Bransford1,2,3*, Sri Suci Utami Atmoko4, Erin R. Vogel2,3 1Department of Anthropology, Northern Illinois University, USA, 2Department of Anthropology, Rutgers University, New Jersey, USA, 3The Center for Human Evolutionary Studies, Rutgers University, USA, 4Universitas Nasional, Jakarta, Indonesia, *tbransford.anthro@gmail.com

Primate mothers face numerous energetic costs during lactation, including milk production/transfer, infant carrying, and vigilance. Orangutans face these challenges while lactating for up to eight years in a habitat with unpredictable fruit availability. By combining multiple biomarkers from noninvasive urine collection, we can start to explore how a mother’s energetic condition varies across the period of infant dependency. Here, we ask if concentrations of urinary C-peptide (energy balance), urea (nitrogen catabolism/metabolism), and ketone bodies (fat catabolism) vary in wild mother Bornean orangutans (Pongo pygmaeus wurmbii) at Tuanan Research Station. Specifically, we test if these biomarkers vary with fruit availability, age of infant, and macronutrient intake. We find that a mother’s urea concentration has an inverse relationship with fruit availability (p = 0.029, F = 4.88), and her ketone production is affected by both the age of her infant (p = 0.002, z = -2.97) and total nonstructural carbohydrate intake (p = 0.021, z = -2.30), with fruit availability impacting the magnitude. While a mother’s urinary C-peptide concentration is inversely correlated with total nonstructural carbohydrate intake (p = 0.030, F = 3.99), the direction of the relationship between her infant’s age and C-peptide concentrations depends on fruit availability (p < 0.03, F > 4.74). These results suggest that, overall, a mother orangutan is in her worst energetic condition during low fruit periods while she has a younger infant. This changes as fruit availability increases, when a mother with a younger infant maintains a higher energy balance but is more likely to utilize available fat stores.

28

9. A comparison of wild and zoo activity budgets for five species of primates Natasha K. Wierzal, Katherine A. Cronin, Jason D. Wark Animal Welfare Science Program, Lincoln Park Zoo, Chicago, IL

Comparing zoo-housed animals’ activity budgets to those of wild conspecifics is one way to assess the extent to which animals express their natural behavioral repertoire, which may have implications for animal welfare. We compared the percent of time spent inactive, foraging, locomoting, engaging in other solitary behaviors, and engaging in social behaviors to values reported in the literature for five primate species: golden-headed lion tamarins (Leontopithecus chrysomelas, N = 2), white-faced saki monkeys (Pithecia pithecia, N = 2), black-and-white colobus monkeys (Colobus guereza, N = 8), Bolivian gray titi monkeys (Callicebus donacophilus, N = 3), and crowned lemurs (Eulemur coronatus, N = 6). Data were collected by trained volunteers at Lincoln Park Zoo using the ZooMonitor app. We conducted ten-minute sessions on focal subjects with instantaneous sampling at one-minute intervals, resulting in between 44 and 318 hours of observation for each species. In general, compared to their wild counterparts, zoo-housed primates spent more time inactive, and less time feeding and locomoting. However, zoo-housed primates spent more time performing social behaviors and other solitary than their wild counterparts. Based on these results, we can identify enrichment and behavioral husbandry strategies to promote more time exploring the habitat and foraging. Determining how to best evaluate and enhance the welfare of animals in human care is challenging, and here we explore an approach that prioritizes a focus on mismatches between captive and wild behavior as potential indicators for opportunities to enhance welfare. Future work will determine if minimizing this mismatch is associated with other indicators of improved welfare. 10. What costs do red colobus monkeys experience when forming mixed-species groups with Diana monkeys?

Joseph Geherty, W. Scott McGraw

Department of Anthropology, The Ohio State University, Columbus, OH, USA Primates which form mixed-species groups experience a net benefit outweighing the costs of forming these groups. Benefits typically come in the form of decreased predation risks due to increased vigilance by all individuals of the group. However, costs due to decreased travel and foraging efficiencies can also result from these multi-species associations. This net benefit is witnessed in red colobus monkeys (Piliocolobus badius) when they form a mixed-species group with Diana monkeys (Cercopithecus diana). It has been documented that both species benefit from increased predator detection. However, the costs for this association is less understood. Red colobus monkeys have been shown to travel further when with Diana monkeys, but not much is known about how foraging behaviors are affected by this association. In order to observe how foraging behavior might change, one red colobus group was followed continuously from July to August, 2019 in the Tai Forest. Behavioral data were taken using fifteen minute scans with the group center marked using GPS. Additionally, travel routes were recorded using GPS points to track the path taken by the group. Red colobus monkeys travelled for longer periods of time while in association with Diana monkeys. Travel bouts ended with foraging

29

activity more frequently when red colobus monkeys travelled without Diana monkeys present. In travel bouts ending with foraging activity, red colobus monkeys more frequently foraged for preferred foods such as young fruit when Diana monkeys were not present compared to foraging more frequently for mature leaves when associated with Diana monkeys. This would indicate that red colobus monkeys might forgo their preferred foods and foraging activity in order to maintain the mixed-species group with Diana monkeys.

11. New enamel 13C data from wild Ugandan chimpanzees (Pan troglodytes schweinfurthii)

permits the establishment of a hominoid-specific diet-to-enamel 13C offset value: Implications for fossil hominin dietary reconstructions

Maire Malone, John Kingston Department of Anthropology, University of Michigan, Ann Arbor, MI, USA

Changes in diet, whether ontogenetic, seasonal, or across evolutionary time, have played a critical role in hominoid and hominin evolution. One of the main sources of information about diet in the fossil record is the biogenic signal in the bioapatite of tooth enamel. The stable

carbon isotope (13C) values of the enamel of extant taxa, and knowledge of their diets, have been used as a comparative guide for interpreting the isotopic signature and diet of fossil organisms. The diets of fossil hominins, however, have previously been reconstructed by using comparative isotopic data from controlled feeding studies of large bodied ruminant herbivores, which have very different digestive processes than those of hominoids and a diet-to-enamel

apatite 13C offset of 14‰. In the absence of controlled feeding studies in modern hominoids,

an offset value between the 13C of hominoid dietary inputs and the resulting enamel outputs has been elusive. Here we present isotopic analyses of enamel apatite from the M2s, P4s, and M3s of a sample of eight Ugandan chimpanzees (Pan troglodytes schweinfurthii) from Kibale National Park, Uganda, obtained via traditional drilling methods and analyzed using GC-IRMS. Highlighted within this sample are the values from individuals from the Ngogo community, where dietary contents, percent of feeding time spent on each item, and those items’ isotopic

values have been previously documented. A preliminary “total dietary” 13C input value is

proposed based upon these data, resulting in a diet-to- 13Cenamel apatite offset value of 12.2‰ for

the Ngogo chimpanzees. This new hominoid diet-to-enamel 13C offset value will allow more precise reconstructions of past diets, permitting more in-depth interpretations of the relationships between diet, climate, and behavior of fossil hominins.

30

12. Prevalence of Cryptosporidium and Giardia infections amongst lemurs, humans, domestic mammals and invasive rats in Tsinjoarivo, Madagascar

Laurie A. Spencer1, Mitchell T. Irwin2 1Department of Biological Sciences, Northern Illinois University, DeKalb, IL, USA, 2Department of Anthropology, Northern Illinois University, DeKalb, IL, USA

Cryptosporidium and Giardia are ubiquitous enteric protozoan pathogens that infect humans, domestic animals, and wildlife worldwide. These pathogens cause gastroenteritis in their hosts, often being fatal in immunocompromised individuals. Few studies have been conducted on these parasites in Madagascar. This project provides a baseline study of these pathogens in a cross-species sample of humans and other mammals in Tsinjoarivo, Madagascar. Fecal samples were collected from two diurnal lemur species (Propithecus diadema and Hapalemur griseus), humans, domestic mammals (cattle, pigs and dogs), and invasive rats. The fecal samples were tested for Cryptosporidium and Giardia utilizing immunofluorescence assay. No lemurs were positive for Cryptosporidium or Giardia infection, but Cryptosporidium was found in humans (10%), cattle (20%), pigs (20%), dogs (15%) and invasive rats (38%), and Giardia was found in humans (10%), pigs (40%), dogs (29%) and invasive rats (53%). I assessed possible risk factors for humans: age, sex, household size, gastrointestinal symptoms, frequency of forest entry, and contact with lemurs, domestic mammals and invasive rats. All infected human subjects were ≤13 years old, but no risk factors were statistically significant. Potential infection risk factors for domestic mammals were also examined (age and group size), with no significant results found. I detected coinfections of Cryptosporidium and Giardia in humans (6%), pigs (20%), dogs (15%) and invasive rats (33%). As human populations increase in Madagascar, the human-wildlife encounters also increase, making it critical to understand this interface. The results of this study document zoonotic health concerns in Madagascar and can aid public health and conservation efforts by adding to our understanding of infection risks for sympatrically living humans, wildlife and domestic animals. 13. Primate microbial endocrinology: An uncharted frontier

Kathryn M. Benavidez1, Michael D. Wasserman1,2,3 1Department of Anthropology, Indiana University, Bloomington, IN, USA, 2Center for the Integrative Study of Animal Behavior, Indiana University, Bloomington, IN, USA, 3Human Biology Program, Indiana University, Bloomington, IN, USA

Gut microbial communities communicate bidirectionally with the brain through endocrine, immune, and neural signaling, influencing the physiology and behavior of hosts. The emerging field of microbial endocrinology offers innovative perspectives and methods to analyze host-microbe relationships with relevance to primate ecology, evolution, and conservation. Herein we briefly summarize key findings from microbial endocrinology and explore how applications of a similar framework could inform our understanding of primate stress and reproductive physiology and behavior. We conclude with three guiding hypotheses to further investigate endocrine signaling between gut microbes and the host: 1) host-microbe communication systems promote microbe-mediated stability, in which the microbes are using endocrine

31

signaling from the host to maintain a functioning habitat for their own fitness, 2) host-microbe communication systems promote host-mediated stability, in which the host uses the endocrine system to monitor microbial communities and alter these communities to maintain stability, or 3) host-microbe systems are simply the product of coincidental cross-talk between the host and microbes due to similar molecules from shared ancestry. Utilizing theory and methodology for studying relationships between the microbiome, hormones, and behavior of wild primates is an uncharted frontier with many promising insights when applied to primatology. 14. Primate limb bone structure: Are gross behavioral categories less informative than number of loading cycles?

Tessa H. Cannon, W. Scott McGraw The Ohio State University, Department of Anthropology, Columbus, OH

Historically, the relationship between primate limb structure and behavior has been investigated through the examination of gross behavioral frequencies of positional behavior such as jumping, climbing, quadrupedalism, and terrestrial or arboreal movement. However, recent analysis of jaw and tooth structure in multiple primate species has been shown to have a closer correlation to number of loading cycles, or the amount of chewing in which an individual engages, than to the hardness of food in the diet. This suggests that bone structure may be more heavily informed by number of forces, rather than the peak force, exerted on the bone. In this study, we counted the number of steps taken by a single adult female in three primate species in Tai National Forest in Cote d’Ivoire: the western red colobus (Piliocolobus badius), Diana monkey (Cercopithecus diana), and sooty mangabey (Cercocebus atys). The limb bones of these three species possess differences in both shape and material properties, while their positional behavior and movement patterns have significant overlap. The goal of these analyses is to not only compare number of steps taken per hour between species, but also to relate this data to home range, foraging dynamics, movement pathways, and anatomy, to determine which variables most greatly influence limb bone structure. 15. The temporal and atmospheric context of howling behavior among mantled howler monkeys (Alouatta palliata) at La Suerte Biological Field Station

Emily L. Kosnik Grand Valley State University

Though howler monkeys (Alouatta spp.) are widely studied, the function of their loud calls remains a topic of much debate among primatologists. At La Suerte Biological Research Station in Costa Rica I examined the relationship between howling behavior and precipitation, and the relationship between howling behavior and time of day in mantled howler monkeys (A. palliata). I predicted I would find a link between precipitation and an increase in howling behavior, and that most howling behavior would occur in the early mornings. Over a 6-day collection period in January 2019, I conducted 27 hours of all-occurrences sampling of howling behavior. During my sampling period, howling did not occur more frequently during samples

32

where it rained. However, it did occur most frequently in the early mornings. Based on the timing when howling behavior occurred and the frequency of howls within the samples, my findings support current research indicating that howler monkey vocalizations are contextually relative while also serving primarily as mechanisms of intergroup spacing. 16. Standing’s Lost Sunken Forest: A new excavation of the famous subfossil site of Ampasambazimba, Central Madagascar

Karen E. Samonds1*, Mitchell T. Irwin2 1 Department of Biological Sciences, Northern Illinois University, Dekalb, IL, USA, 2

Department of Anthropology, Northern Illinois University, Dekalb, IL, USA, *ksamonds@niu.edu

Madagascar is famed for its extraordinary living animals, and lemurs are the most studied and well-known; with more than 90% threatened with extinction, they are considered the most endangered mammal group. Habitat loss has caused extensive reductions in living species, as well as recent extinctions: Madagascar’s Late Pleistocene and Holocene subfossil record has yielded 17 giant extinct lemurs, the largest of which, Archaeoindris fontoynontii, is the largest primate ever known from Madagascar (~160 kg). Archaeoindris stands out not only because of its gorilla-like size, but also because it is known from few specimens, and is reconstructed as living in an environment no longer found in Madagascar – a mosaic of closed humid forest, open woodland and savannah. The only known locality of Archaeoindris is the subfossil site Ampasambazimba, which was discovered in the early 20th century, and described as a “sunken forest” of subfossil logs and seeds. Despite recent attempts to rediscover this specific locality and more elements of Archaeoindris, the original collection site has remained elusive. We present here the result of recent excavations at Ampasambazimba, which yielded crocodiles, hippos, elephant birds, giant tortoises, and primates. Lemurs recovered include Mesopropithecus pithecoides, Pachylemur jullyi, Megaladapis grandidieri, and one bone within the size range of Archaeoindris. A high density of perfectly-preserved subfossil wood and seeds was recovered – these include seeds of Ramy (Canarium), a tree currently restricted to eastern rainforest, ~130 km away. The rediscovery of this sunken forest offers a new opportunity to understand the context and ecology of Archaeoindris and its faunal community. Future work aims to return to Ampasambazimba to reconstruct the sequence of forest, wetland and savanna ecosystems across recent millennia.