WHAT WE KNOW

Where they live: Southeastern Tropical, Rainforest Inhabit secondary lowlands, evergreen, and semi-deciduous forests, forest edge and dry forest patches. Typically live at elevations between 1600 – 2300 feet but can be found as high as 2600 feet. Arboreal Rowe, 1996; Rylands and Mendes, 2008

WHAT WE KNOW

Social Behavior: Live in family groups, up to 8-10 individuals Usually monogamous, only dominate male and female typically breed Groups are usually comprised of a breeding pair and their offspring Daughters are usually reproductively suppressed

Wakenshaw, 1999

WHAT WE KNOW

Wild diet: Anatomical and behavioral adaptations for tree- gouging Able to gouge into tree trunks, branches, and vines to obtain gum Eat plant gums, and fruit Also eat flowers, nectar, frogs, snails, lizards, and spiders.

Passamani & Ryland, 2000; Passamani, 1998; Rowe, 1996; Rylands and Mendes, 2008

IN THE WILD

Passamani & Ryland, 2000 One year study, that included 9,013 observations of which 1848 were of feeding Group sized varied from 3 – 5. 68.6% of all feeding observations were gums 15% fruit 14.6% invertebrates 0.8% small vertebrates 1% unidentified

FEEDING CHOICES IN THE WILD

Animals eat gum and insects year around

During the wet season, Dec & Jan, selection of fruit greatly increases (43% of feeding observations) but continue to consume gums and insects

Passamani & Ryland, 2000

IMPORTANT KEY POINTS FOR APPROPRIATELY FEEDING CAPTIVE GEOFFROY’S MARMOSETS

1. Fruit will be preferentially consumed when available 2. Wild marmosets use their teeth to gouge or gnaw holes in trees and vines for gum 3. Animals are usually monogamous and the breeding pair are dominant 4. Subordinate females are reproductively suppressed

CAPTIVE DIET FORMULATION GUIDELINE ONLY

Estimated Energy Need

0.75 137-255kcal·BWkg

Nutrient Requirements of Nonhuman : Second Revised Edition, 2003

Estimated Dry Matter Intake Ability

~ 3- 4% BW (based on Common Marmosets)

Power & Myers 2009

ESTIMATED NUTRIENT NEEDS Excerpt from TABLE 11-2 Estimated Adequate Nutrient Concentrations (Dry Matter Basis) Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003

Nutrient Unit 1NRC Notations

Crude protein % 15-22 b

Calcium % 0.8

Total Phosphorus % 0.6 d

Sodium % 0.2

Vitamin D3 IU/kg 2,500 f

Vitamin C mg/kg 200 j

f There are anecdotal reports of higher vitamin D3 requirements in callitrichids under certain circumstances (seeChapter7). 1 http://www.nap.edu/catalog/9826/nutrient-requirements-of-nonhuman-primates-second-revised-edition ESTIMATED ENERGY: EXAMPLE

0.75 137-255kcal·BWkg

Animal Body Weight = 500 grams  Convert gram to kg: 500/1000 = 0.5 kg  Scale the BW: (0.5) 0.75 = 0.595  Multiply the scaled BW by need Energy  137 X 0.595 = 81 kcal lower level  255 X 0.595 = 152 kcal upper level

ESTIMATED DRY MATTER INTAKE ABILITY: EXAMPLE ~ 3- 4% BW (based on Common Marmosets)

Animal Body Weight = 500 grams

 0.035 X 500 grams = 17.5 grams Estimated Dry Matter Intake Ability

 ~ Range 15 – 20 grams Estimated Dry Matter Intake Ability

CHOOSING DIET INGREDIENTS

Base Diet

 Home made  Commercial Products

o ZuPreem Canned http://www.zupreem.com/products/marmoset-diet

o Mazuri line of Callitrichid Gel Diets http://www.mazuri.com/callitrichids.aspx

AS FED BASE DIET

Nutrient Unit 1ZuPreem 2Mazuri 5M15 Moisture % 62 60 Crude protein % 8.5 8.4 Fat % 2.5 3.12 *Carbohydrate by difference % 24 21.48 Calcium % 0.2 0.44 Sodium % No Data 0.12 Total Phosphorus % 0.2 0.256 Vitamin D3 IU/kg 1814 2658 Vitamin C mg/kg 0 258 Estimated ME kcal/g 1.52 1.36 *includes fiber 1http://www.zupreem.com/products/marmoset-diet 2 Prepared according to manufacturer instructions: http://www.mazuri.com/product_pdfs/5MI5.pdf ACTIVITY FOOD

GUM Wild Geoffroy’s Marmoset consume gums year around – 68.6% of observed feedings were on gums!!!

2 Senegalia senegal, Compostion UNIT 1 Acacia 1 Paulinia 1 Bauhinia 1 Dyctioloma Vachellia paniculata carpopodi angulosa incanensis seyal 3Mazuri 5B35* Moisture % 5.3 6.6 7.6 6.5 12.89 2 Crude Protein % 10.8 15.2 6.3 7.1 1.45 1 Fat % 2.3 2.8 2.8 3.4 0 0 Carbohydrate as soluble fiber % 79.7 73.5 81.4 81.1 82.44 90 Ash % 1.9 1.9 1.9 1.9 3.22 5 Estimated ME kcal/g 3.8 3.8 3.8 3.8 3.4 3.6 1Passamani & Ryland, 2000 2Philadelpha Zoo Analysis of Raw Gum Arabic, Midwest Laboratories June 24,2015 3 Mazuri Enrichment Gum Arabic http://www.mazuri.com/product_pdfs/5B35.pdf ACTIVITY FOODS

INSECTS Wild Geoffroy’s Marmoset consume invertebrates year around – 14.6% of observed feedings were on invertebrates!!!

4Soldier flies 5Waxworms Compostion 1Mealworms 2Crickets Acheta 3 SuperwormsZopho (lavae) Galleria Tenebrio molitor domesticus bas morio larvae Hermetia illucens mellonella Moisture % 66.36 64.94 61.3 61.2 58.5 Crude Protein % 18.9 9.3 16.9 17.5 14.1 Fat % 12 4.19 15.1 14 24.9 Carbohydrate by difference % 1.82 19.6 5.46 3.8 1.9 Ash % 0.92 1.89 1.24 3.5 0.6 Estimated ME kcal/g 1.9 1.5 2.3 2.1 2.9 1Philadelpha Zoo Analysis of mealworms as received, Midwest Laboratories June 8, 2009 2Philadelpha Zoo Analysis of Large Crickets as received, Midwest Laboratories August 10, 2010 3Philadelpha Zoo Analysis of Superworms as received , Midwest Laboratories August 10, 2011 4Finke, 2012 5Finke, 2002 LIMIT FRUIT

Fruit was consumed by wild Geoffory’s 15% of the observations; however, the majority of these observation were during only 2 months of the year. Although fruit can be used for positive re- enforcement or the delivery of medicine it should be very limited. Geoffroy’s WILL consume fruit preferentially and to their detriment. Toddes 30 years experience! POSSIBLE GOOD ALTERNATIVE TO FRUIT

Beans: Beans are soluble fiber superstars. One cup of black beans has 4.8 g of soluble fiber, while Navy beans have 4.4 g and light-red kidney beans have 4g. All beans are good choices. http://www.todaysdietitian.com/newarchives/120913p16.shtml

Nutrient Unit 1C. Black Beans 2C. Navy Beans 3C. Kidney Beans 4EO Kidney Beans Moisture % 75.6 70.45 77.96 77.96 Crude protein % 6.03 7.53 5.22 6.15 Fat % 0.29 0.43 0.36 0 Carbohydrate by difference % 16.55 20.45 14.83 18 Fiber Total Dietary % 6.9 5.1 5.3 7.7 Total Sugars % 0.23 0.28 1.85 0.9 Sodium % 0.138 0.336 0.177 0.011 Calcium % 0.035 0.047 0.029 0.029 Total Phosphorus % 0.108 0.134 0.106 0.106 Vitamin D3 IU/kg 0 0 0 0 Vitamin C mg/kg 27 7 8 8 Estimated ME kcal/g 0.91 1.13 0.81 0.77 1Basic Report: 16316, Beans, black, mature seeds, canned, low sodium 2Basic Report: 16039, Beans, navy, mature seeds, canned 3Basic Report: 16337, Beans, kidney, red, mature seeds, canned, solids and liquid, low sodium 4Eden Organic Kidney Beans Label &Yellow highlight =Basic Report: 16337, Beans, kidney, red, mature seeds, canned, solids and liquid, low sodium http://ndb.nal.usda.gov PUTTING IT ALL TOGETHER

500 gram GM needs ~ 81 – 152 kcal & can eat ~17.5 grams DM

VERY General Kcal Guideline  For non-reproductive animals lower end  Reproductive middle (injured, sick etc…)  Lactation upper end GENERAL MAINTENANCE DIET Nutritent 17.5 g DM Protein g 2.6 - 3.85 Calcium g 0.14 Phosphorus g 0.105 Vitamin D3 IU 44 Vitamin C mg 3.5 SAMPLE APPROPRIATE DIET

500 gram animal at maintenance Maintenance % Kcal Kcal Grams Base Diet 72% 60 39 Apples 8% 7 13 Carrots 5% 4 10 Insects 5% 4 3 Yogurt/Gum arabic 5% 4 3 Keepers Choice - NO FRUIT (kcal) 5% 4 5 Total Kcal 83 75 SAMPLE APPROPRIATE DIET REVIEW

Nutrient Unit Mazuri ZuPreem Apples Carrots Mealworms PZ Gum Mix EO Kidney Beans Total As Fed Est Need Moisture g 23.68 24.5 11.5 8.6 2.2 0.7 4.0 51.6

Dry g 15.79 15.0 2.0 1.1 1.1 1.2 1.2 21.6 17.5 Crude protein g 3.32 3.4 0.0 0.1 0.6 0.0 0.3 4.5 2.6 - 3.85 Fat g 1.23 1.0 0.0 0.0 0.4 0.0 0.0 1.5 Carbohydrate by difference g 8.48 9.5 1.9 0.9 0.1 0.9 0.9 14.2

Total Dietary Fiber g 0.17 0.592 0.323 0.273 0.067 0.804 0.400 2.5 Total Sugars g 5.21 1.399 0.462 0.000 0.132 0.047 2.0 Sodium g 0.05 0.000 0.007 0.002 0.001 0.001 0.01 0.04 Calcium g 0.05 0.079 0.001 0.004 0.001 0.008 0.002 0.09 0.14 Total Phosphorus g 0.10 0.079 0.001 0.003 0.008 0.001 0.006 0.10 0.11 Vitamin D3 IU 104.92 72 0.000 0.000 0.000 0.000 0.000 72 44 Vitamin C mg 10.18 0.000 0.062 0.058 0.000 0.000 0.042 0.161 3.5 Estimated ME kcal 53.68 60 7 4 4 4 4 83 81-152

Vitamin C supplement required

SAMPLE PROBLEM DIET

500 gram animal at maintenance

Maintenance % Kcal Kcal Grams Base Diet 44% 60 39 Apples 44% 60 115 Carrots 3% 4 10 Insects 3% 4 3 Yogurt/Gum arabic 3% 4 3 Keepers Choice - NO FRUIT (kcal) 3% 4 5 Total Kcal 136 177 SAMPLE PROBLEM DIET REVIEW

Nutrient Unit Mazuri ZuPreem Apples Carrots Mealworms PZ Gum Mix EO Kidney Beans Total As Fed Est Need Moisture g 23.68 24.5 98.7 8.6 2.2 0.7 4.0 138.8

Dry g 15.79 15.0 16.7 1.1 1.1 1.2 1.2 36.4 17.5 Crude protein g 3.32 3.4 0.3 0.1 0.6 0.0 0.3 4.7 2.6 - 3.85 Fat g 1.23 1.0 0.2 0.0 0.4 0.0 0.0 1.6 Carbohydrate by difference g 8.48 9.5 15.9 0.9 0.1 0.9 0.9 28.3

Total Dietary Fiber g 0.17 0.592 2.769 0.273 0.067 0.804 0.400 4.9 Total Sugars g 5.21 11.988 0.462 0.000 0.132 0.047 12.6 Sodium g 0.05 0.001 0.007 0.002 0.001 0.001 0.01 0.04 Calcium g 0.05 0.079 0.007 0.004 0.001 0.008 0.002 0.10 0.14 Total Phosphorus g 0.10 0.079 0.013 0.003 0.008 0.001 0.006 0.11 0.11 Vitamin D3 IU 104.92 72 0.000 0.000 0.000 0.000 0.000 72 44 Vitamin C mg 10.18 0.000 0.531 0.058 0.000 0.000 0.042 0.630 3.5 Estimated ME kcal 53.68 60 60 4 4 4 4 136 81-152 GEOFFROY’S WILL CONSUME FRUIT PREFERENTIALLY TO ALL OTHER DIETARY ITEMS

FRUIT MUST BE LIMITED IN THE DIET ACTUAL CONSUMPTION

Maintenance % Kcal Kcal Grams Base Diet 3% 2 1 Apples 77% 60 115 Carrots 5% 4 10 Insects 5% 4 3 Yogurt/Gum arabic 5% 4 2 Keepers Choice - NO FRUIT (kcal) 5% 4 5 Total Kcal 78 137 ACTUAL CONSUMPTION

Nutrient Unit Mazuri ZuPreem Apples Carrots Mealworms PZ Gum Mix EO Kidney Beans Total As Fed Est Need Moisture g 0.79 0.8 98.7 8.6 2.2 0.7 4.0 115.2

Dry g 0.53 0.5 16.7 1.1 1.1 1.2 1.2 21.9 17.5 Crude protein g 0.11 0.1 0.3 0.1 0.6 0.0 0.3 1.5 2.6 - 3.85 Fat g 0.04 0.0 0.2 0.0 0.4 0.0 0.0 0.7 Carbohydrate by difference g 0.28 0.3 15.9 0.9 0.1 0.9 0.9 19.1

Total Dietary Fiber g 0.01 0.020 2.769 0.273 0.067 0.804 0.400 4.3 Total Sugars g 0.17 11.988 0.462 0.000 0.132 0.047 12.6 Sodium g 0.00 0.001 0.007 0.002 0.001 0.001 0.01 0.04 Calcium g 0.00 0.003 0.007 0.004 0.001 0.008 0.002 0.02 0.14 Total Phosphorus g 0.00 0.079 0.013 0.003 0.008 0.001 0.006 0.11 0.11 Vitamin D3 IU 3.50 2 0.000 0.000 0.000 0.000 0.000 2 44 Vitamin C mg 0.34 0.000 0.531 0.058 0.000 0.000 0.042 0.630 3.5 Estimated ME kcal 1.79 2 60 4 4 4 4 78 81-152 DIET COMPARISON

Offered Offered Expected Consumed Nutrient Unit Low Fruit High Fruit High Fruit Est Need

Dry g 21.6 36.4 21.9 17.5 Crude protein g 4.5 4.7 1.5 2.6 - 3.85 Fat g 1.5 1.6 0.7 Carbohydrate by difference g 14.2 28.3 19.1 Total Dietary Fiber g 2.5 4.9 4.3 Total Sugars g 2.0 12.6 12.6 Sodium g 0.01 0.01 0.01 0.04 Calcium g 0.09 0.10 0.02 0.14 Total Phosphorus g 0.10 0.11 0.11 0.11 Vitamin D3 IU 72 72 2 44 Vitamin C mg 0.16 0.63 0.63 3.5 Estimated ME kcal 83 136 78 81-152 DIET PRESENTATION

Presentation of the food is AS important as the food itself First morning Feed - ONLY base diet, establish how much of the base diet your group needs to consume 20 -25 grams/animal works well for most groups offered either Mazuri or ZuPreem Once the amount of base diet needed is consumed begin offering the activity foods Best to offer activity foods as well as additional base diet over at LEAST 2 feedings so a minimum of 3 food offerings/day. MAKE THE ANIMALS WORK FOR ALL THEIR FOOD INCLUDING THE BASE DIET

OTHER

It is not unusual for subordinate females to become very heavy – may have to do with suppressed ovulation but we don’t know Target feeding at risk animals their base diet is highly recommended Weigh your animals OFTEN at least once a month – best way to identify issues early and address them before they become problems Consider the diets of other species in the exhibit – only combine dietary compatible animals Giardia parasite as well bacterial pathogens and GI autoimmune diseases MAY be diet related GUM

Wild Geoffroy’s Marmoset consume gums year around – 68.6% of observed feedings were on gums!!!

2 Senegalia senegal, Compostion UNIT 1 Acacia 1 Paulinia 1 Bauhinia 1 Dyctioloma Vachellia paniculata carpopodi angulosa incanensis seyal 3Mazuri 5B35* Moisture % 5.3 6.6 7.6 6.5 12.89 2 Crude Protein % 10.8 15.2 6.3 7.1 1.45 1 Fat % 2.3 2.8 2.8 3.4 0 0 Carbohydrate as soluble fiber % 79.7 73.5 81.4 81.1 82.44 90 Ash % 1.9 1.9 1.9 1.9 3.22 5 Estimated ME kcal/g 3.8 3.8 3.8 3.8 3.4 3.6 1Passamani & Ryland, 2000 2Philadelpha Zoo Analysis of Raw Gum Arabic, Midwest Laboratories June 24,2015 3 Mazuri Enrichment Gum Arabic http://www.mazuri.com/product_pdfs/5B35.pdf SOLUBLE FIBER

Soluble fiber absorbs water In humans:  Soluble fiber attaches to cholesterol particles and takes them out of the body, helping to reduce overall cholesterol levels  Contributes to gut fill or the feeling of being satiated  Aids in healthy bowel movements, absorbs water as it passes through the gut and contributes to stool bulk and helps prevent constipation  Is protective against diabetes – because it is not well absorbed it does not contribute to blood sugar spikes which is a risk factor for both type 2 diabetes and heart disease  Gums are β-linked polysaccharides that require microbial fermentation**

PRIMATE MICROBIOME PROJECT HTTP://WWW.PRIMATEMICROBIOME.ORG/

ASSOCIATIONS BETWEEN NUTRITION, GUT MICROBIAL COMMUNITIES, AND HEALTH IN NONHUMAN PRIMATES Jonathan Clayton, University of Minnesota Primate gastrointestinal tract is home to trillions of bacteria

. Digestion and metabolism . Immune system development . Pathogen resistance

Shifts in the microbiome are correlated with GI autoimmune diseases such as:

. Diabetes . Crohn’s disease . Ulcerative colitis Clayton, 2015

GOAL OF THE PRIMATE MICROBIOME PROJECT

Compare the microbiome wild and captive animals within the same species

Determine whether shifts in the microbiota are linked with health (e.g., gastrointestinal) in captivity.

Hopefully develop predictive biomarkers for certain primate diseases, including those linked to diet. Clayton, 2015

CITED

Rowe, N. 1996. The Pictoral Guide to Living Primates. East Hampton, New York: Pogonias Press. Rylands, A., S. Mendes. 2008. "2008 IUCN Red List of Threatened Species" (On-line). geoffroyi. Available at :www.iucnredlist.org. Wakenshaw, V. 1999. The Management and Husbandry of Geoffroy’s Marmoset. International Zoo News, 46(1): 0. Available at: http://www.zoonews.ws/IZN/290/IZN-290.html Passamani, M. and Rylands, A. B. 2000. Feeding behavior of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic forest fragment of south-eastern Brazil. Primates 41: 27-38. Available at: http://www.researchgate.net/profile/Marcelo_Passamani/publication/225400128_Feeding_behavior_of_G eoffroy's_marmoset_(Callithrix_geoffroyi)_in_an_Atlantic_forest_fragment_of_South- eastern_Brazil/links/00b7d53b6a9a71bfbc000000.pdf Passamani, M. 1998. Activity Budget of Geoffroy's Marmoset (Callithrix geoffroyi) in an Atlantic Forest in Southeastern Brazil. American Journal of Primatology, 46: 333-340. Available at: http://www.ncbi.nlm.nih.gov/pubmed/9839906 Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003. Available at: http://www.nap.edu/catalog/9826/nutrient-requirements-of-nonhuman-primates-second-revised-edition Power & Myers ..2009. Digestion in the (Callithrix jacchus), a gummivore-frugivore. American Journal of Primatology, 71(12):957-63. Available at : http://www.ncbi.nlm.nih.gov/pubmed/19725117 Finke. 2012, Complete Nutrient Content of Four Species of Feeder insects. Zoo Biology 00:1-15. Available at: http://www.timberlinefisheries.com/v/vspfiles/assets/images/finke_2012_complete%20nutrient%20conte nt%20of%20four%20species%20of%20feeder%20insects.pdf Finke. 2002. Complete Nutrient Composition of commercially raised invertebrates used as food for insectivores. Zoo Biology 21:269-295. Available at : http://onlinelibrary.wiley.com/doi/10.1002/zoo.10031/abstract Clayton. 2015. Associations between nutrition, gut microbial communities, and health in nonhuman primates. 8th European Zoo Nutrition Conference, Arnhem, Netherlands

WEBSITES REFERENCED http://www.zupreem.com/products/marmoset-diet http://www.mazuri.com/callitrichids.aspx http://www.primatemicrobiome.org http://ndb.nal.usda.gov/ http://www.todaysdietitian.com/newarchives/120913p1 6.shtml