A simple assay for measuring tannin-protein precipitation capacity offers insights into the diet and food choice of black howler monkeys (Alouatta pigra).
anti‐nutritional
assay
consumption
herbivores
precipitation
Journal
American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949
Informations de publication
Date de publication:
07 May 2024
07 May 2024
Historique:
revised:
05
04
2024
received:
02
03
2023
accepted:
27
04
2024
medline:
8
5
2024
pubmed:
8
5
2024
entrez:
8
5
2024
Statut:
aheadofprint
Résumé
Phenolics, like tannins, are plant-specialized metabolites that play a protective role against herbivory. Tannins can reduce palatability and bind with proteins to reduce digestibility, acting as deterrents to feeding and impacting nutrient extraction by herbivores. Some assays measure tannin and total phenolics content in plants but lack determination of their biological effects, hindering the interpretation of tannin function in herbivory and its impacts on animal behavior and ecology. In this study, we successfully applied the radial diffusion assay to assess tannin protein precipitation (PP) capacity and evaluate the anti-nutritional effects of tannins in food plants (n = 24) consumed by free-ranging black howler monkeys (Alouatta pigra) in Tabasco, Mexico. We found PP rings in five plant species consumed by the monkeys. The mature fruit of Inga edulis was the most consumed food plant, despite having a high tannin PP capacity (56.66 mg tannic acid equivalent/g dry matter). These findings highlight the presence of tannins in the black howler diet and provide insight into the primates' resilience and potential strategies for coping with anti-nutritional aspects of the diet.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23638Subventions
Organisme : Universidad Popular Autonoma de Puebla (UPAEP)
Organisme : Universidad Autonoma de Yucatan
Organisme : Instituto de Ecología A. C.
Informations de copyright
© 2024 Wiley Periodicals LLC.
Références
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3–4), 227–266. https://doi.org/10.1163/156853974X00534
Amato, K. R., & Garber, P. A. (2014). Nutrition and foraging strategies of the black howler monkey (Alouatta pigra) in Palenque National Park, Mexico. American Journal of Primatology, 76(8), 774–787. https://doi.org/10.1002/ajp.22268
Amato, K. R., Leigh, S. R., Kent, A., Mackie, R. I., Yeoman, C. J., Stumpf, R. M., Wilson, B. A., Nelson, K. E., White, B. A., & Garber, P. A. (2015). The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microbial Ecology, 69, 434–443. https://doi.org/10.1007/s00248-014-0554-7
Aristizábal, J. F. (2013). Estrategias de forrajeo y características nutricionales de la dieta del mono aullador negro (Alouatta pigra) en un ambiente fragmentado. [Unpublished MSc Thesis]. Instituto de Ecología, A. C., Xalapa, Veracruz, Mexico.
Aristizabal, J. F., Rothman, J. M., García‐Fería, L. M., & Serio‐Silva, J. C. (2017). Contrasting time‐based and weight‐based estimates of protein and energy intake of black howler monkeys (Alouatta pigra). American Journal of Primatology, 79(4), 1–8. https://doi.org/10.1002/ajp.22611
Asquith, T. N., & Butler, L. G. (1985). Use of dye‐labeled protein as spectrophotometric assay for protein precipitants such as tannin. Journal of Chemical Ecology, 11, 1535–1544. https://doi.org/10.1007/BF01012199
Bailey, D. W., Gross, J. E., Laca, E. A., Rittenhouse, L. R., Coughenour, M. B., Swift, D. M., & Sims, P. L. (1996). Mechanisms that result in large herbivore grazing distribution patterns. Journal of Range Management, 49(5), 386–400. https://doi.org/10.2307/4002919
Barry, T. N., & Manley, T. R. (1984). The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep: 2. Quantitative digestion of carbohydrates and proteins. British Journal of Nutrition, 51(3), 493–504. https://doi.org/10.1079/BJN19840055
Beaune, D., Hohmann, G., Serckx, A., Sakamaki, T., Narat, V., & Fruth, B. (2017). How bonobo communities deal with tannin rich fruits: Re‐ingestion and other feeding processes. Behavioural Processes, 142, 131–137. https://doi.org/10.1016/j.beproc.2017.06.007
Behie, A. M., & Pavelka, M. S. M. (2012). Food selection in the black howler monkey following habitat disturbance: Implications for the importance of mature leaves. Journal of Tropical Ecology, 28(2), 153–160. https://doi.org/10.1017/S0266467411000678
Bennick, A. (2002). Interaction of plant polyphenols with salivary proteins. Critical Reviews in Oral Biology and Medicine: An Official Publication of the American Association of Oral Biologists, 13(2), 184–196. https://doi.org/10.1177/154411130201300208
Bernays, E. A., & Cornelius, M. (1992). Relationship between deterrence and toxicity of plant secondary compounds for the alfalfa weevil Hypera brunneipennis. Entomologia Experimentalis et Applicata, 64, 289–292. https://doi.org/10.1111/j.1570-7458.1992.tb01619.x
Bridgeman, L. L. (2012). The feeding ecology of Yucatán black howler monkeys (Alouatta pigra) in mangrove forest, Tabasco, Mexico. [Unpublished doctoral dissertation]. Washington University in St. Louis. Saint Louis, Missouri.
Bryant, J. P., Wieland, G. D., Clausen, T., & Kuropat, P. (1985). Interactions of snowshoe hare and felt leaf willow in Alaska. Ecology, 66(5), 1564–1573. https://doi.org/10.2307/1938018
Carrai, V., Borgognini‐Tarli, S. M., Huffman, M. A., & Bardi, M. (2003). Increase in tannin consumption by sifaka (Propithecus verreauxi verreauxi) females during the birth season: A case for self‐medication in prosimians? Primates, 44, 61–66. https://doi.org/10.1007/s10329-002-0008-6
Chapman, C. A., & Chapman, L. J. (2002). Foraging challenges of red colobus monkeys: Influence of nutrients and secondary compounds. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 133(3), 861–875. https://doi.org/10.1016/S1095-6433(02)00209-X
Chivers, D. J., & Hladik, C. M. (1980). Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet. Journal of Morphology, 166(3), 337–386. https://doi.org/10.1002/jmor.1051660306
Coley, P. D. (1983). Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs, 53(2), 209–234. https://doi.org/10.2307/1942495
Crockett, C. M. (1998). Conservation biology of the genus Alouatta. International Journal of Primatology, 19(3), 549–578. https://doi.org/10.1023/A:1020316607284
Davies, A. G., Bennett, E. L., & Waterman, P. G. (1988). Food selection by two South‐east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biological Journal of the Linnean Society, 34(1), 33–56. https://doi.org/10.1111/j.1095-8312.1988.tb01947.x
DeGabriel, J. L., Moore, B. D., Foley, W. J., & Johnson, C. N. (2009). The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology, 90(3), 711–719. https://doi.org/10.1890/08-0940.1
Dias, P. A. D., & Rangel‐Negrín, A. (2015). Diets of howler monkeys. In M. Kowalewski, P. A. Garber, L. Cortés‐Ortíz, & D. Youlatos (Eds.), Howler monkeys: behavior, ecology, and conservation (pp. 21–56). Springer, New York.
Dominy, N. J., & Lucas, P. W. (2001). Ecological importance of trichromatic vision to primates. Nature, 410(6826), 363–366. https://doi.org/10.1038/35066567
Dschaak, C. M., Williams, C. M., Holt, M. S., Eun, J. S., Young, A. J., & Min, B. R. (2011). Effects of supplementing condensed tannin extract on intake, digestion, ruminal fermentation, and milk production of lactating dairy cows. Journal of Dairy Science, 94(5), 2508–2519. https://doi.org/10.3168/jds.2010-3818
Duncan, A. J., Hartley, S. E., & Iason, G. R. (1994). The effect of monoterpene concentrations in Sitka spruce (Picea sitchensis) on the browsing behaviour of red deer (Cervus elaphus). Canadian Journal of Zoology, 72(10), 1715–1720. https://doi.org/10.1139/z94-231
Dunn, J. C., Cristóbal‐Azkarate, J., & Veà, J. J. (2010). Seasonal variations in the diet and feeding effort of two groups of howlers in different sized forest fragments. International Journal of Primatology, 31(5), 887–903. https://doi.org/10.1007/s10764-010-9436-0
Espinosa Gómez, F., Santiago García, J., Gómez Rosales, S., Wallis, I. R., Chapman, C. A., Morales Mávil, J., Canales‐Espinosa, D., & Hernández Salazar, L. (2015). Howler monkeys (Alouatta palliata mexicana) produce tannin‐binding salivary proteins. International Journal of Primatology, 36(6), 1086–1100. https://doi.org/10.1007/s10764-015-9879-4
Espinosa‐Gómez, F. C., Serio‐Silva, J. C., Santiago‐García, J. D., Sandoval‐Castro, C. A., Hernández‐Salazar, L. T., Mejía‐Varas, F., Ojeda‐Chávez, J., & Chapman, C. A. (2018). Salivary tannin‐binding proteins are a pervasive strategy used by the folivorous/frugivorous black howler monkey. American Journal of Primatology, 80(2), e22737. https://doi.org/10.1002/ajp.22737
Estrada, A., Mendoza, A., Castellanos, L., Pacheco, R., Van Belle, S., García, Y., & Muñoz, D. (2002). Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque, Chiapas, Mexico. American Journal of Primatology, 58(2), 45–55. https://doi.org/10.1002/ajp.10051
Freeland, W. J., & Janzen, D. H. (1974). Strategies in herbivory by mammals: The role of plant secondary compounds. The American Naturalist, 108(961), 269–289. https://doi.org/10.1086/282907
De la Fuente, M. F., Souto, A., Albuquerque, U. P., & Schiel, N. (2022). Self‐medication in nonhuman primates: A systematic evaluation of the possible function of the use of medicinal plants. American Journal of Primatology, 84(11), e23438. https://doi.org/10.1002/ajp.23438
Ganzhorn, J. U. (1989). Primate species separation in relation to secondary plant chemicals. Human Evolution, 4, 125–132. https://doi.org/10.1007/BF02435441
Ganzhorn, U. (1988). Food partitioning among Malagasy primates. Oecologia, 75(3), 436–450. https://doi.org/10.1007/BF00376949
Gedir, J. V., Sporns, P., & Hudson, R. J. (2005). Extraction of condensed tannins from cervid feed and feces and quantification using a radial diffusion assay. Journal of Chemical Ecology, 31, 2761–2773. https://doi.org/10.1007/s10886-005-8392-1
Glander, K. E. (1981). Feeding patterns in mantled howling monkeys. In A. Kamil & T. D. Sargent, (Eds.), Foraging behavior: Ecological, ethological, and psychological approaches (pp. 231–259). Garland Press.
Glander, K. E. (1982). The impact of plant secondary compounds on primate feeding behavior. American Journal of Physical Anthropology, 25(S3), 1–18. https://doi.org/10.1002/ajpa.1330250503
Goltenboth, R. (1976). Non human primates (apes, monkeys and prosimians). In H. G. Klos & E. M. Lang (Eds.), The handbook of zoo medicine (pp. 46–85). Van Nostrand Reinhold.
Guimarães Leitão, G., Lopes Mensor, L., Amaral, L. F. G., Floriano, N., Garcia Limeira, V. L., Sousa Menezes, F. D., & Guimarães Leitão, S. (1999). Phenolic content and antioxidant activity: A study on plants eaten by a group of Howler monkeys (Alouatta fusca). In G. G. Gross, R. W. Hemingway, T. Yoshida, & S. J. Branham (Eds.), Plant polyphenols 2 basic life sciences (vol 66, pp. 883–895). Springer.
Hagerman, A. E. (1987). Radial diffusion method for determining tannin in plant extracts. Journal of Chemical Ecology, 13(3), 437–449. https://doi.org/10.1007/BF01880091
Hagerman, A. E., & Butler, L. G. (1980). Determination of protein in tannin‐protein precipitates. Journal of Agricultural and Food Chemistry, 28(5), 944–947. https://doi.org/10.1021/jf60231a010
Hassanpour, S., MaheriSis, N., & Eshratkhah, B. (2011). Plants and secondary metabolites (Tannins): A review. International Journal of Forest, Soil and Erotion, 1(1), 47–53. agris.fao.org/agris-search/search.do?recordID=DJ2012080632
Huffman, M. A. (2003). Animal self‐medication and ethno‐medicine: Exploration and exploitation of the medicinal properties of plants. Proceedings of the Nutrition Society, 62(2), 371–381. https://doi.org/10.1079/PNS2003257
Iason, G. (2005). The role of plant secondary metabolites in mammalian herbivory: Ecological perspectives. Proceedings of the Nutrition Society, 64(1), 123–131. https://doi.org/10.1079/PNS2004415
IUCN. (2022). The IUCN red list of threatened species. Version 2022‐2. https://www.iucnredlist.org
Kaur, C., & Kapoor, H. C. (2002). Anti‐oxidant activity and total phenolic content of some Asian vegetables. International Journal of Food Science & Technology, 37(2), 153–161. https://doi.org/10.1046/j.1365-2621.2002.00552.x
Kelln, B. M., Penner, G. B., Acharya, S. N., McAllister, T. A., & Lardner, H. A. (2021). Impact of condensed tannin‐containing legumes on ruminal fermentation, nutrition, and performance in ruminants: A review. Canadian Journal of Animal Science, 101(2), 210–223. https://doi.org/10.1139/cjas-2020-0096
Kool, K. M. (1992). Food selection by the silver leaf monkey, Trachypithecus auratus sondaicus, in relation to plant chemistry. Oecologia, 90, 527–533. https://doi.org/10.1007/BF01875446
Lindroth, R. L., & Batzli, G. O. (1983). Detoxication of some naturally occuring phenolics by prairie voles: A rapid assay of glucuronidation metabolism. Biochemical Systematics and Ecology, 11(4), 405–409. https://doi.org/10.1016/0305-1978(83)90045-5
Lucas, P. W., Beta, T., Darvell, B. W., Dominy, N. J., Essackjee, H. C., Lee, P. K. D., Osorio, D., Ramsden, L., Yamashita, N., & Yuen, T. D. B. (2001). Field kit to characterize physical, chemical and spatial aspects of potential primate foods. Folia Primatologica, 72(1), 11–25. https://doi.org/10.1159/000049914
Makkar, H. P. S., Blümmel, M., Borowy, N. K., & Becker, K. (1993). Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. Journal of the Science of Food and Agriculture, 61(2), 161–165. https://doi.org/10.1002/jsfa.2740610205
Mallott, E. K., Skovmand, L. H., Garber, P. A., & Amato, K. R. (2022). The faecal metabolome of black howler monkeys (Alouatta pigra) varies in response to seasonal dietary changes. Molecular Ecology, 31(15), 4146–4161. https://doi.org/10.1111/mec.16559
Martin, J. S., & Martin, M. M. (1983). Tannin assays in ecological studies precipitation of ribulose‐1,5‐bisphosphate carboxylase/oxygenase by tannic acid, quebracho, and oak foliage extracts. Journal of Chemical Ecology, 9, 285–294. https://doi.org/10.1007/BF00988046
McArthur, C., Robbins, C. T., Hagerman, A. E., & Hanley, T. A. (1993). Diet selection by a ruminant generalist browser in relation to plant chemistry. Canadian Journal of Zoology, 71(11), 2236–2243. https://doi.org/10.1139/z93-314
Milton, K. (1979). Factors influencing leaf choice by howler monkeys: A test of some hypotheses of food selection by generalist herbivores. The American Naturalist, 114(3), 362–378. https://doi.org/10.1086/283485
Milton, K. (1981). Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. American Anthropologist, 83(3), 534–548. https://doi.org/10.1525/aa.1981.83.3.02a00020
Milton, K., & McBee, R. H. (1983). Rates of fermentative digestion in the howler monkey, Alouatta palliata (Primates: Ceboidea). Comparative Biochemistry and Physiology Part A: Physiology, 74(1), 29–31. https://doi.org/10.1016/0300-9629(83)90706-5
Milton, K., Van Soest, P. J., & Robertson, J. B. (1980). Digestive efficiencies of wild howler monkeys. Physiological Zoology, 53(4), 402–409. https://doi.org/10.1086/physzool.53.4.30157878
Min, B. R., Barry, T. N., Attwood, G. T., & McNabb, W. C. (2003). The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: A review. Animal Feed Science and Technology, 106, 3–19. https://doi.org/10.1016/S0377-8401(03)00041-5
Moore, B. D., Andrew, R. L., Külheim, C., & Foley, W. J. (2014). Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytologist, 201(3), 733–750. https://doi.org/10.1111/nph.12526
Moore, B. D., & Foley, W. J. (2005). Tree use by koalas in a chemically complex landscape. Nature, 435, 488–490. https://doi.org/10.1038/nature03551
Morrogh‐Bernard, H. C., Foitová, I., Yeen, Z., Wilkin, P., De Martin, R., Rárová, L., Doležal, K., Nurcahyo, W., & Olšanský, M. (2017). Self‐medication by orangutans (Pongo pygmaeus) using bioactive properties of Dracaena cantleyi. Scientific Reports, 7(1), 16653. https://doi.org/10.1038/s41598-017-16621-w
Mowry, C. B., Decker, B. S., & Shure, D. J. (1996). The role of phytochemistry in dietary choices of Tana River red colobus monkeys (Procolobus badius rufomitratus). International Journal of Primatology, 17, 63–84. https://doi.org/10.1007/BF02696159
Norconk, M. A., & Conklin‐Brittain, N. L. (2004). Variation on frugivory: The diet of Venezuelan white‐faced sakis. International Journal of Primatology, 25, 1–26. https://doi.org/10.1023/B:IJOP.0000014642.68751.ed
Osborne, N. J. T., & McNeill, D. M. (2001). Characterisation of Leucaena condensed tannins by size and protein precipitation capacity. Journal of the Science of Food and Agriculture, 81(11), 1113–1119. https://doi.org/10.1002/jsfa.920
Palma, A. C., Vélez, A., Gómez‐Posada, C., López, H., Zárate, D. A., & Stevenson, P. R. (2011). Use of space, activity patterns, and foraging behavior of red howler monkeys (Alouatta seniculus) in an Andean Forest fragment in Colombia. American Journal of Primatology, 73(10), 1062–1071. https://doi.org/10.1002/ajp.20973
Pavelka, M. S. M., & Knopff, K. H. (2004). Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: Does degree of frugivory influence activity level? Primates, 45, 105–111. https://doi.org/10.1007/s10329-003-0072-6
Peterson, B. G., & Carl, P. (2019). PerformanceAnalytics: Econometric tools for performance and risk analysis. R package version 1.5.3. https://CRAN.R-project.org/package=PerformanceAnalytics
Pfister, J. A., Provenza, F. D., Manners, G. D., Gardner, D. R., & Ralphs, M. H. (1997). Tall larkspur ingestion: Can cattle regulate intake below toxic levels. Journal of Chemical Ecology, 23, 759–777. https://doi.org/10.1023/B:JOEC.0000006409.20279.59
Price, M. L., Van Scoyoc, S., & Butler, L. G. (1978). A critical evaluation of the vanillin reaction as an assay for tannin in sorghum grain. Journal of Agricultural and Food Chemistry, 26(5), 1214–1218. https://doi.org/10.1021/jf60219a031
R Core Team. (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Australia. https://www.R-project.org/
Rautio, P., Bergvall, U. A., Karonen, M., & Salminen, J. P. (2007). Bitter problems in ecological feeding experiments: Commercial tannin preparations and common methods for tannin quantifications. Biochemical Systematics and Ecology, 35(5), 257–262. https://doi.org/10.1016/j.bse.2006.10.016
Remis, M. J., Dierenfeld, E. S., Mowry, C. B., & Carroll, R. W. (2001). Nutritional aspects of western lowland gorilla (Gorilla gorilla gorilla) diet during seasons of fruit scarcity at Bai Hokou, Central African Republic. International Journal of Primatology, 22, 807–836. https://doi.org/10.1023/A:1012021617737
Rickard, J. E. (1986). Tannin levels in cassava, a comparison of methods of analysis. Journal of the Science of Food and Agriculture, 37(1), 37–42. https://doi.org/10.1002/jsfa.2740370106
Righini, N., Garber, P. A., & Rothman, J. M. (2017). The effects of plant nutritional chemistry on food selection of Mexican black howler monkeys (Alouatta pigra): The role of lipids. American Journal of Primatology, 79(4), 1–15. https://doi.org/10.1002/ajp.22524
Robbins, C. T., Hagerman, A. E., Austin, P. J., McArthur, C., & Hanley, T. A. (1991). Variation in mammalian physiological responses to a condensed tannin and its ecological implications. Journal of Mammalogy, 72(3), 480–486. https://doi.org/10.2307/1382130
Rothman, J. M., Dusinberre, K., & Pell, A. N. (2009). Condensed tannins in the diets of primates: A matter of methods? American Journal of Primatology, 71(1), 70–76. https://doi.org/10.1002/ajp.20623
Rothman, J. M., Pell, A. N., & Bowman, D. D. (2009). How does diet quality affect the parasite ecology of mountain gorillas? In M. A. Huffman & C. A. Chapman (Eds.), Primate parasite ecology: The dynamics and study of host‐parasite relationships (pp. 441–462). Cambridge University Press.
Roy, S. N., & Mukherjee, S. (1979). Influence of food tannins on certain aspects of iron metabolism: Part 3: Heme synthesis and haematopoiesis in normal and anemic rats. Indian Journal of Biochemistry & Biophysics, 16(3), 151–157.
Salminen, J. P., & Karonen, M. (2011). Chemical ecology of tannins and other phenolics: We need a change in approach. Functional Ecology, 25(2), 325–338. https://doi.org/10.1111/j.1365-2435.2010.01826.x
Scalbert, A. (1992). Quantitative methods for the estimation of tannins in plant tissues. In R. W. Hemingway & P. E. Laks, (Eds.), Plant polyphenols. Basic life sciences (vol 59, pp. 259–280). Springer.
Schofield, P., Mbugua, D. M., & Pell, A. N. (2001). Analysis of condensed tannins: A review. Animal Feed Science and Technology, 91(1–2), 21–40. https://doi.org/10.1016/S0377-8401(01)00228-0
Silanikove, N., Gilboa, N., & Nitsan, Z. (2001). Effect of polyethylene glycol on rumen volume and retention time of liquid and particulate matter along the digestive tract in goats fed tannin‐rich carob leaves (Ceratonia siliqua). Small Ruminant Research, 40(1), 95–99. https://doi.org/10.1016/S0921-4488(00)00209-1
Silver, S. C., Ostro, L. E. T., Yeager, C. P., & Dierenfeld, E. S. (2000). Phytochemical and mineral components of foods consumed by black howler monkeys (Alouatta pigra) at two sites in Belize. Zoo Biology, 19(2), 95–109. https://doi.org/10.1002/1098-2361(2000)19:2<95:AID-ZOO1>3.0.CO;2-D
Silver, S. C., Ostro, L. E. T., Yeager, C. P., & Horwich, R. (1998). Feeding ecology of the black howler monkey (Alouatta pigra) in northern Belize. American Journal of Primatology, 45(3), 263–279. https://doi.org/10.1002/(SICI)1098-2345(1998)45:3<263::AID-AJP3>3.0.CO;2-U
Simmen, B. (1994). Taste discrimination and diet differentiation among New World primates. In D. J. Chivers & P. Langer, (Eds.), The digestive system in mammals: Food, form and function (pp. 150–165). Cambridge University Press.
Simmen, B., Josseaume, B., & Atramentowicz, M. (1999). Frugivory and taste responses to fructose and tannic acid in a prosimian primate and a didelphid marsupial. Journal of Chemical Ecology, 25, 331–346. https://doi.org/10.1023/A:1020850914167
Simmen, B., Tarnaud, L., Marez, A., & Hladik, A. (2014). Leaf chemistry as a predictor of primate biomass and the mediating role of food selection: A case study in a folivorous lemur (Propithecus verreauxi). American Journal of Primatology, 76(6), 563–575. https://doi.org/10.1002/ajp.22249
Singleton, V. L., & Rossi, J. A. (1965). Colorimetry of total phenolics with phosphomolybdic‐phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16(3), 144–158.
Sorensen, J. S., McLister, J. D., & Dearing, M. D. (2005). Novel plant secondary metabolites impact dietary specialists more than generalists (Neotoma spp.). Ecology, 86(1), 140–154. https://doi.org/10.1890/03-0669
Stapley, J., Foley, W. J., Cunningham, R., & Eschler, B. (2000). How well can common brushtail possums regulate their intake of Eucalyptus toxins? Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 170, 211–218. https://doi.org/10.1007/s003600050277
Struhsaker, T. T., Cooney, D. O., & Siex, K. S. (1997). Charcoal consumption by Zanzibar red colobus monkeys: Its function and its ecological and demographic consequences. International Journal of Primatology, 18(1), 61–72. https://doi.org/10.1023/A:1026341207045
Thurau, E. G., Rahajanirina, A. N., & Irwin, M. T. (2021). Condensed tannins in the diet of folivorous diademed sifakas and the gap between crude and available protein. American Journal of Primatology, 83(3), e23239. https://doi.org/10.1002/ajp.23239
Villalba, J. J., Provenza, F. D., & Bryant, J. P. (2002). Consequences of the interaction between nutrients and plant secondary metabolites on herbivore selectivity: Benefits or detriments for plants? Oikos, 97(2), 282–292. https://doi.org/10.1034/j.1600-0706.2002.970214.x
Welker, B. J. (2004). Proximate mechanisms governing feeding behavior and selectivity in mantled howler monkeys, Alouatta palliata. [Unpublished doctoral dissertation]. Buffalo: State University of New York.
Welker, B. J., König, W., Pietsch, M., & Adams, R. P. (2007). Feeding selectivity by mantled howler monkeys (Alouatta palliata) in relation to leaf secondary chemistry in Hymenaea courbaril. Journal of Chemical Ecology, 33(6), 1186–1196. https://doi.org/10.1007/s10886-007-9292-3
Windley, H. R., Starrs, D., Stalenberg, E., Rothman, J. M., Ganzhorn, J. U., & Foley, W. J. (2022). Plant secondary metabolites and primate food choices: A meta‐analysis and future directions. American Journal of Primatology, 84(8), e23397. https://doi.org/10.1002/ajp.23397
Wrangham, R. W., Conklin‐Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. International Journal of Primatology, 19, 949–970. https://doi.org/10.1023/A:1020318102257
Wrangham, R. W., & Waterman, P. G. (1983). Condensed tannins in fruits eaten by chimpanzees. Biotropica, 15(3), 217–222. https://doi.org/10.2307/2387832
Yamashita, N. (2008). Chemical properties of the diets of two lemur species in southwestern Madagascar. International Journal of Primatology, 29, 339–364. https://doi.org/10.1007/s10764-008-9232-2