PISTAS DULCES-ÁCIDAS EN LA DIETA DEL MONO AULLADOR (ALOUATTA PALLIATA AEQUATORIALIS) DEL PARQUE NACIONAL SOBERANÍA, PANAMÁ

Jeami Newbold; Adyani Arias; Pedro G. Méndez-Carvajal; Karol M. Gutiérrez-Pineda

doi:10.48204/j.scientia.v34n2.a5332

Submitted July 16, 2024

Published 2024-07-18

Artículos

Vol. 34 No. 2 (2024): Scientia

SWEET-ACID TRACKS IN THE DIET OF THA HOWLER MONKEY (ALOUATTA PALLIATA AEQUATORIALIS) OF SOBERANIA NATIONAL PARK, PANAMA

Jeami Newbold⁺⁻
Adyani Arias ⁺⁻
Pedro G. Méndez-Carvajal⁺⁻
Karol M. Gutiérrez-Pineda ⁺⁻

DOI https://doi.org/10.48204/j.scientia.v34n2.a5332

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DOI: 10.48204/j.scientia.v34n2.a5332

Published: 2024-07-18

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Newbold, J., Arias , A., Méndez-Carvajal, P. G., & Gutiérrez-Pineda , K. M. (2024). SWEET-ACID TRACKS IN THE DIET OF THA HOWLER MONKEY (ALOUATTA PALLIATA AEQUATORIALIS) OF SOBERANIA NATIONAL PARK, PANAMA. Scientia, 34(2), 60–82. https://doi.org/10.48204/j.scientia.v34n2.a5332

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

Abstract

Some primate species use sweet-sour qualities to determine the presence of carbohydrates and avoid compounds that prevent adequate nutrient intake. Our objective was to evaluate the effects of sucrose and pH on the acceptance of plant parts (PV) by Alouatta palliata aequatorialis in Soberanía National Park. We located individuals through direct and indirect trail search. We conducted 76 focal animals (AF) to evaluate the frequency of acceptance of the PVs (leaves, fruits, petioles and stipules), which were subsequently collected to be identified. We also collected the evaluated PVs (accepted/rejected) to measure sucrose using a refractometer and pH with test strips. We obtained that AF fed mainly on fruits (36.4%), leaves (33.9%) and petioles (29.7%) of 10 plant species. The consumed PV presented a percentage of sucrose (Brix%) between 4.3 to 14.3 (x? 9.1±SD3.2), with a difference between them (F:10.1668, df:2, p:0.0003). The pH presented a range of 4 to 7 (x?:5.5±SD:0.9), with differences between the PVs (Chⁱ²:10.77, gl:2, p:0.0046). There was no dependence in the frequency of acceptance of PV with respect to sucrose (p:0.07191) and pH (p:0.3621). This supports that howler monkeys may use these qualities as an indication, but without any effect on acceptance. To complete this research, we propose that astringent and bitter qualities be evaluated to determine their effect on acceptance.

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References

Altman, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3–4), 227–266.
ANAM Autoridad Nacional del Ambiente (1999). Plan de Manejo Ambiental del Parque Nacional Soberanía. República de Panamá. 193 pp
Balcells, C. D., & Baró, J. J. V. (2009). Developmental stages in the howler monkey, subspecies Alouatta palliata mexicana: a new classification using age-sex categories. Neotropicales primates, 16(1), 1–8. https://doi.org/10.1896/044.016.0101
Behie, A. M., Pavelka, M. S. M., & Chapman, C. A. (2010). Sources of variation in fecal cortisol levels in howler monkeys in Belize. American Journal of Primatology, 72(7), 600–606. https://doi.org/10.1002/ajp.20813
Blandón, A. M., & Ochoa Aguirre, T. P. (2015). Determinación de la concentración de pH en hojas de cultivares clonales Spondias purpurea L, en el arboretum Alain Meyrat de la Universidad Nacional Agraria [Tesis doctoral] Universidad nacional Agrarria, Managua, Nicaragua.
Carrión, J. F., Víquez, K. E., Mendieta, J. A., Carrasquilla, L., & Vergara, C. (2013). Caracterización florística y estructural de una parcela de bosque semicaducifolio en el parque nacional Soberanía, Panamá. Tecnociencia, 15(2), 71-84.
Dias, P. A., & Rangel-Negrín, A. (2015). Diets of Howler Monkeys Howler Monkeys, 21–56. https://doi.org/10.1007/978-1-4939-1960-4_2
Dominy, N. J. (2004). Fruits, fingers, and fermentation: The sensory cues available to foraging primates. Integrative and Comparative Biology, 44(4), 295–303. https://doi.org/10.1093/icb/44.4.295
Dominy, N. J., Lucas, P. W., Osorio, D., & Yamashita, N. (2004). The sensory of primates food perception. Evolutionary Anthropology, 10, 171–186.
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
Empresa de Transmisión Eléctrica S.A, (2018). Clima anual de la República de Panamá. http://www.hidromet.com.pa/documentos.php?sec=14.
Felíx, M. G. (2000). Comparación de la capacidad de fijación de dióxido de carbono en los bosques de los parques nacionales Soberanía, Chagres y Camino de Cruces [Tesis de maestría] Universidad de Panamá, Panamá.
Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009). Nutritional goals of wild primates. Functional Ecology, 23(1), 70–78. https://doi.org/10.1111/j.1365-2435.2008.01526.x
Fernández, V. A. (2014). Ecología nutricional del mono aullador negro y dorado (Alouatta caraya) en el límite sur de su distribución [Tesis doctoral]. Universidad de Buenos Aires.
Fuentes, E., Estrada, A., Franco, B., Magaña, M., Decena, Y., Muñoz, D., & Garcia, Y. (2003). Reporte preliminar sobre el uso de recursos alimenticios por una tropa de monos aulladores, Alouatta palliata, en el parque la venta, Tabasco, México”. Neotropical Primates, 11(1), 24–28.
García, A. Á., & Pérez-Urria Carril, E. (2009). Metabolismo secundario de plantas”. Reduca (Biología). Serie Fisiología Vegetal, 2(3), 119–145.
Glander, K. E. (1980). Reproduction and population growth in free?ranging mantled howling monkeys. American Journal of Physical Anthropology, 53(1), 25-36.
Glander, K. E. (1992). Dispersal patterns in Costa Rican Mantled Howling Monkeys. Int. J. Primatol, 13(4), 415–435.
Hladik. C. M (1993) Fruits of the rain forest and taste perception as a result of evolutionary interactions. Tropical Forests, People and Food: Biocultural interactions and applications to development., pp.73-82 UNESCO-Parthenon Paris.
Hladik, C. M. (1967). Surface relative du tractus digestif de quelques primates, morphologie des villosites intestinales et correlations avec le regime alimentaire. Mammalia, 31(1). https://doi.org/10.1515/mamm.1967.31.1.120
Hladik, C. M., Pasquet, P., & Simmen, B. (2002). New perspectives on taste and primate evolution: the dichotomy in gustatory coding for perception of beneficent versus noxious substances as supported by correlations among human thresholds”. American Journal of Physical Anthropology, 117(4), 342–348.
Hladik, C. M., Pasquet, P., & Simmen, B. (2004). Cultural o biológico: ¿qué significado tienen umbrales gustativos en términos evolutivos? En A. Millán-Fuertes, L. Cantarero, X. Medina, & M. M. J. Montejano (Eds.), Arbitrario cultural. Racionalidad e irracionalidad del comportamiento comensal. Homenaje a Igor de Garine (pp. 475–488).
Hostettmann, K., Gupta, M. P., Marston, A., & Ferreira, E. (2008). Manual de estrategias para el aislamiento de productos naturales bioactivos. Programa iberoamericano de Ciencia y Tecnología. CYTED.
Laska, M., Scheuber, H.-P., Sanchez, E. C., & Rodriguez Luna, E. (1999). Taste difference thresholds for sucrose in two species of nonhuman primates. American Journal of Primatology, 48(2), pp.153–160. https://doi.org/10.1002/(sici)1098-2345(1999)48:2<153::aid-ajp6>3.0.co;2-7
Mendez-Carvajal, P. (2012). Population study of Coiba howler monkeys (Alouatta coibensis coibensis) and Coiba Capuchin monkeys (Cebus capucinus imitator), Coiba island National Park, republic of panama. Journal of primatology, vol.1. no.2, pp, 1-5. https://doi.org/10.4172/2167-6801.1000104
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. (1980). The foraging strategy of howler monkeys. A study in primate economics. Columbia University Press., New York, 1980, pp. 165.
Milton, K. (1990). Calidad dietética y regulación demográfica de una población de monos aulladores Alouatta palliata En E. G. Leigh, A. S. Rand, & D. M. Winsor (Eds.), Smithsonian (pp. 357–373).
Milton, K. (1999). Nutritional characteristics of wild primate foods: Do the diets of our closest living relatives have lessons for us? Nutrition, 15(6), 488-498.
Milton, Katharine, Armitage, D. W., & Sousa, W. P. (2019). Successional loss of two key food tree species best explains decline in group size of Panamanian howler monkeys (Alouatta palliata). Biotropica, 51(4), 600–614. https://doi.org/10.1111/btp.12679
Nagy, K. A., & Milton, K. (1979). Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata)”. Ecology, 60(3), 475–480.
Pablo-Rodríguez, M., Hernández-Salazar, L. T., Aureli, F., & Schaffner, C. M. (2015). The role of sucrose and sensory systems in fruit selection and consumption of Ateles geoffroyi in Yucatan, Mexico”. Journal of Tropical Ecology, 31(03), 213–219. https://doi.org/10.1017/s0266467415000085
Pozo-Montuy, G., & Serio-Silva, J. C. (2006). Comportamiento alimentario de monos aulladores negros (Alouatta pigra Lawrence, Cebidae) en hábitat fragmentado en Balacán, Tabasco, México”. Acta zoológica mexicana, 22(3), 53–66.
Quintana-Morales, P. C. (2015). Influencia de la disponibilidad y distribución del alimento en la dinámica intergrupal del mono aullador de manto (Alouatta palliata); Instituto de Neuroetología.
Sánchez-Solano, K. G., Reynoso-Cruz, J. E., Guevara, R., Morales-Mávil, J. E., Laska, M., & Hernández-Salazar, L. T. (2022). Non-visual senses in fruit selection by the mantled howler monkey (Alouatta palliata). Primates; Journal of Primatology, 63(3), 293–303. https://doi.org/10.1007/s10329-022-00984-4
Serio-Silva, J., Rico-Gray, V., Hernandez-Salazar, L., & Espinosa-Gómez, R. (2002). The role of Ficus (Moraceae) in the diet and nutrition of a troop of Mexican howler monkeys, Alouatta palliata mexicana, released on an island in southern Veracruz, Mexico”. Journal of Tropical Ecology, 18(06), 913–928. https://doi.org/10.1017/s0266467402002596

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[1] Altman, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3–4), 227–266.

[2] ANAM Autoridad Nacional del Ambiente (1999). Plan de Manejo Ambiental del Parque Nacional Soberanía. República de Panamá. 193 pp

[3] Balcells, C. D., & Baró, J. J. V. (2009). Developmental stages in the howler monkey, subspecies Alouatta palliata mexicana: a new classification using age-sex categories. Neotropicales primates, 16(1), 1–8. https://doi.org/10.1896/044.016.0101

[4] Behie, A. M., Pavelka, M. S. M., & Chapman, C. A. (2010). Sources of variation in fecal cortisol levels in howler monkeys in Belize. American Journal of Primatology, 72(7), 600–606. https://doi.org/10.1002/ajp.20813

[5] Blandón, A. M., & Ochoa Aguirre, T. P. (2015). Determinación de la concentración de pH en hojas de cultivares clonales Spondias purpurea L, en el arboretum Alain Meyrat de la Universidad Nacional Agraria [Tesis doctoral] Universidad nacional Agrarria, Managua, Nicaragua.

[6] Carrión, J. F., Víquez, K. E., Mendieta, J. A., Carrasquilla, L., & Vergara, C. (2013). Caracterización florística y estructural de una parcela de bosque semicaducifolio en el parque nacional Soberanía, Panamá. Tecnociencia, 15(2), 71-84.

[7] Dias, P. A., & Rangel-Negrín, A. (2015). Diets of Howler Monkeys Howler Monkeys, 21–56. https://doi.org/10.1007/978-1-4939-1960-4_2

[8] Dominy, N. J. (2004). Fruits, fingers, and fermentation: The sensory cues available to foraging primates. Integrative and Comparative Biology, 44(4), 295–303. https://doi.org/10.1093/icb/44.4.295

[9] Dominy, N. J., Lucas, P. W., Osorio, D., & Yamashita, N. (2004). The sensory of primates food perception. Evolutionary Anthropology, 10, 171–186.

[10] 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

[11] Empresa de Transmisión Eléctrica S.A, (2018). Clima anual de la República de Panamá. http://www.hidromet.com.pa/documentos.php?sec=14.

[12] Felíx, M. G. (2000). Comparación de la capacidad de fijación de dióxido de carbono en los bosques de los parques nacionales Soberanía, Chagres y Camino de Cruces [Tesis de maestría] Universidad de Panamá, Panamá.

[13] Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009). Nutritional goals of wild primates. Functional Ecology, 23(1), 70–78. https://doi.org/10.1111/j.1365-2435.2008.01526.x

[14] Fernández, V. A. (2014). Ecología nutricional del mono aullador negro y dorado (Alouatta caraya) en el límite sur de su distribución [Tesis doctoral]. Universidad de Buenos Aires.

[15] Fuentes, E., Estrada, A., Franco, B., Magaña, M., Decena, Y., Muñoz, D., & Garcia, Y. (2003). Reporte preliminar sobre el uso de recursos alimenticios por una tropa de monos aulladores, Alouatta palliata, en el parque la venta, Tabasco, México”. Neotropical Primates, 11(1), 24–28.

[16] García, A. Á., & Pérez-Urria Carril, E. (2009). Metabolismo secundario de plantas”. Reduca (Biología). Serie Fisiología Vegetal, 2(3), 119–145.

[17] Glander, K. E. (1980). Reproduction and population growth in free?ranging mantled howling monkeys. American Journal of Physical Anthropology, 53(1), 25-36.

[18] Glander, K. E. (1992). Dispersal patterns in Costa Rican Mantled Howling Monkeys. Int. J. Primatol, 13(4), 415–435.

[19] Hladik. C. M (1993) Fruits of the rain forest and taste perception as a result of evolutionary interactions. Tropical Forests, People and Food: Biocultural interactions and applications to development., pp.73-82 UNESCO-Parthenon Paris.

[20] Hladik, C. M. (1967). Surface relative du tractus digestif de quelques primates, morphologie des villosites intestinales et correlations avec le regime alimentaire. Mammalia, 31(1). https://doi.org/10.1515/mamm.1967.31.1.120

[21] Hladik, C. M., Pasquet, P., & Simmen, B. (2002). New perspectives on taste and primate evolution: the dichotomy in gustatory coding for perception of beneficent versus noxious substances as supported by correlations among human thresholds”. American Journal of Physical Anthropology, 117(4), 342–348.

[22] Hladik, C. M., Pasquet, P., & Simmen, B. (2004). Cultural o biológico: ¿qué significado tienen umbrales gustativos en términos evolutivos? En A. Millán-Fuertes, L. Cantarero, X. Medina, & M. M. J. Montejano (Eds.), Arbitrario cultural. Racionalidad e irracionalidad del comportamiento comensal. Homenaje a Igor de Garine (pp. 475–488).

[23] Hostettmann, K., Gupta, M. P., Marston, A., & Ferreira, E. (2008). Manual de estrategias para el aislamiento de productos naturales bioactivos. Programa iberoamericano de Ciencia y Tecnología. CYTED.

[24] Laska, M., Scheuber, H.-P., Sanchez, E. C., & Rodriguez Luna, E. (1999). Taste difference thresholds for sucrose in two species of nonhuman primates. American Journal of Primatology, 48(2), pp.153–160. https://doi.org/10.1002/(sici)1098-2345(1999)48:2<153::aid-ajp6>3.0.co;2-7

[25] Mendez-Carvajal, P. (2012). Population study of Coiba howler monkeys (Alouatta coibensis coibensis) and Coiba Capuchin monkeys (Cebus capucinus imitator), Coiba island National Park, republic of panama. Journal of primatology, vol.1. no.2, pp, 1-5. https://doi.org/10.4172/2167-6801.1000104

[26] 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

[27] Milton, K. (1980). The foraging strategy of howler monkeys. A study in primate economics. Columbia University Press., New York, 1980, pp. 165.

[28] Milton, K. (1990). Calidad dietética y regulación demográfica de una población de monos aulladores Alouatta palliata En E. G. Leigh, A. S. Rand, & D. M. Winsor (Eds.), Smithsonian (pp. 357–373).

[29] Milton, K. (1999). Nutritional characteristics of wild primate foods: Do the diets of our closest living relatives have lessons for us? Nutrition, 15(6), 488-498.

[30] Milton, Katharine, Armitage, D. W., & Sousa, W. P. (2019). Successional loss of two key food tree species best explains decline in group size of Panamanian howler monkeys (Alouatta palliata). Biotropica, 51(4), 600–614. https://doi.org/10.1111/btp.12679

[31] Nagy, K. A., & Milton, K. (1979). Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata)”. Ecology, 60(3), 475–480.

[32] Pablo-Rodríguez, M., Hernández-Salazar, L. T., Aureli, F., & Schaffner, C. M. (2015). The role of sucrose and sensory systems in fruit selection and consumption of Ateles geoffroyi in Yucatan, Mexico”. Journal of Tropical Ecology, 31(03), 213–219. https://doi.org/10.1017/s0266467415000085

[33] Pozo-Montuy, G., & Serio-Silva, J. C. (2006). Comportamiento alimentario de monos aulladores negros (Alouatta pigra Lawrence, Cebidae) en hábitat fragmentado en Balacán, Tabasco, México”. Acta zoológica mexicana, 22(3), 53–66.

[34] Quintana-Morales, P. C. (2015). Influencia de la disponibilidad y distribución del alimento en la dinámica intergrupal del mono aullador de manto (Alouatta palliata); Instituto de Neuroetología.

[35] Sánchez-Solano, K. G., Reynoso-Cruz, J. E., Guevara, R., Morales-Mávil, J. E., Laska, M., & Hernández-Salazar, L. T. (2022). Non-visual senses in fruit selection by the mantled howler monkey (Alouatta palliata). Primates; Journal of Primatology, 63(3), 293–303. https://doi.org/10.1007/s10329-022-00984-4

[36] Serio-Silva, J., Rico-Gray, V., Hernandez-Salazar, L., & Espinosa-Gómez, R. (2002). The role of Ficus (Moraceae) in the diet and nutrition of a troop of Mexican howler monkeys, Alouatta palliata mexicana, released on an island in southern Veracruz, Mexico”. Journal of Tropical Ecology, 18(06), 913–928. https://doi.org/10.1017/s0266467402002596

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