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A comparison of inter- and intraspecific variation in seed dispersal in three South American primates

Published online by Cambridge University Press:  08 November 2023

Ariek Barakat Norford Open the ORCID record for Ariek Barakat Norford [Opens in a new window] ,
Kelin Nathaly Echeverry ,
Juliana Ramos Obregón  and
Pablo R. Stevenson
Ariek Barakat Norford*
Affiliation:
Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY, USA
Kelin Nathaly Echeverry
Affiliation:
Departmento de Ciencias Biológicas, Universidad de Los Andes, Bogotá, Colombia
Juliana Ramos Obregón
Affiliation:
Departmento de Ciencias Biológicas, Universidad de Los Andes, Bogotá, Colombia
Pablo R. Stevenson
Affiliation:
Departmento de Ciencias Biológicas, Universidad de Los Andes, Bogotá, Colombia Centro de Investigaciones Ecológicas La Macarena, Universidad de Los Andes, Bogotá, Colombia
*
Corresponding author: Ariek Barakat Norford; Email: [email protected]
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Abstract

Primate communities vary in their level of redundancy, or overlap, in seed dispersal function, which could be due to body size, degree of frugivory or intraspecific variation, among other factors. In this study, we quantified redundancy in seed dispersal among three sympatric primate species: Lagothrix lagothricha, Alouatta seniculus and Sapajus apella in gallery forests in Meta, Colombia. We compared the median seed width dispersed and the number and species richness of large (≥5.9 mm wide) and very large (>7.5 mm wide) seeds per faecal sample. The medium-sized, highly folivorous A. seniculus mostly dispersed large seeds, the larger, highly frugivorous L. lagothricha dispersed very large and small seeds, and the smaller, partially frugivorous S. apella dispersed the smallest seeds. However, for L. lagothricha and S. apella, we did not find the expected results that adults disperse larger seeds than juveniles. Across species, there is complementarity in seed dispersal in relation to seed size, with L. lagothricha being unique in its contribution to the dispersal of very large seeds both in terms of quantity and richness.

Resumen [español]

Resumen [Español]

Los ensamblajes de primates varían en los papeles como dispersores de semillas, de acuerdo con la redundancia en la sobreposición en la dieta de las especies presentes, tamaño corporal, y grado de frugívoría, entre otros factores. Cuantificamos redundancia entre y dentro de tres primates simpátricos, Lagothrix lagothricha, Alouatta seniculus, y Sapajus apella en su función de dispersión en los bosques de galería de Meta, Colombia. Comparamos el tamaño medio de semillas dispersadas y el número y riqueza de especies de semillas grandes (ancho ≥5.9 mm) y muy grandes (>7.5 mm) dispersadas por muestra fecal. A. seniculus con tamaño intermedio y altamente folívoro dispersó principalmente semillas grandes; L. lagothricha, la especie más grande y altamente frugívora, dispersó principalmente semillas muy grandes y pequeñas; mientras que S. apella, el más pequeño y 50% frugívoro, dispersó muchas semillas pequeñas. Para dos especies, L. lagothricha y S. apella, no encontramos el patrón esperado de que los adultos dispersaron semillas de tamaño más grande de los juveniles. Encontramos complementariedad entre especies en su función de dispersión con relación al tamaño de las semillas, y L. lagothricha se caracterizó por su contribución dispersando semillas muy grandes, tanto en términos de cantidad, como en riqueza.

Keywords

Capuchin monkeysendozoochoryfunctional redundancyhowler monkeyswoolly monkeys
Type
Research Article
Information
Journal of Tropical Ecology , Volume 39 , 2024 , e38
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© The Author(s), 2023. Published by Cambridge University Press

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References

Andresen, E (1999) Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian forest. Biotropica 31, 145–158.Google Scholar
Andresen, E, Arroyo-Rodríguez, V and Ramos-Robles, M (2018) Primate seed dispersal: old and new challenges. International Journal of Primatology 39, 443–456.CrossRefGoogle Scholar
Ayres, JMC (1986) Uakaris and Amazonian flooded forest. PhD dissertation, Department of Vertebrate Anatomy, University of Cambridge.Google Scholar
Benchimol, M and Peres, CA (2014) Predicting primate local extinctions within “real-world” forest fragments: a pan-neotropical analysis. American Journal of Primatology 76, 289–302.CrossRefGoogle ScholarPubMed
Benítez-Malvido, J, Ma, A, Pierro, G-D, Lombera, R, Guillén, S and Estrada, A (2014) Seed source, seed traits, and frugivore habits: implications for dispersal quality of two sympatric primates. American Journal of Botany 101, 970–978.CrossRefGoogle ScholarPubMed
Bolker, B (2007) Likelihood and all that. In Bolker, B (ed.), Ecological Models and Data in R. Princeton: Princeton University Press, pp. 227–292.Google Scholar
Bossier, O, Feer, F, Henry, P-Y and Forget, P-M (2020) Modifications of the rain forest frugivore community are associated with reduced seed removal at the community level. Ecological Applications 30, e02086.CrossRefGoogle Scholar
Boubli, JP, Alves, SL, Buss, G, Calouro, AM, Carvalho, A, Ceballos-Mago, N, Heymann, EW, Lynch Alfaro, J, Martins, AB, Messias, M, Mittermeier, RA, Mollinedo, J, Moscoso, P, Palacios, E, Ravetta, A, Rumiz, DI, Rylands, AB, Shanee, S, Stevenson, PR, de la Torre, S and Urbani, B (2020) Sapajus apella. The IUCN Red List of Threatened Species 2020: e.T172351505A172353050. Available at https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T172351505A172353050.en (accessed 3 January 2021).CrossRefGoogle Scholar
Bueno, RS, Guevara, R, Ribeiro, MC, Culot, L, Bufalo, FS and Galetti, M (2013) Functional redundancy and complementarities of seed dispersal by the last neotropical megafrugivores. PLoS ONE 8, e56252.CrossRefGoogle ScholarPubMed
Bufalo, FS, Galetti, M and Culot, L (2016) Seed dispersal by primates and implications for the conservation of a biodiversity hotspot, the Atlantic Forest of South America. International Journal of Primatology 37, 333–349.CrossRefGoogle Scholar
Caro, OL and Ardila, I (2004) Diseño de un sendero ecológico interpretative e inventario general de la vegetación nativa del bosque de gallería ubicado en la hacienda Santa Rosa, municípos de San Martín, Meta, Orinoquía colombiana. Informe final, Bogotá.Google Scholar
Chacón-Moreno, EJ (2004) Mapping savanna ecosystems of the Llanos del Orinoco using multitemporal NOAA satellite imagery. International Journal of Applied Earth Observation and Geoinformation 5, 41–53.CrossRefGoogle Scholar
Chao, A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43, 783–791.CrossRefGoogle ScholarPubMed
Chao, A, Ma, KH, Hsieh, TC and Chiu, C-H (2016) SpadeR (Species-richness Prediction and Diversity Estimation in R): an R package in CRAN.Google Scholar
Chapman, CA and Russo, SE (2007) Primate seed dispersal: linking behavioral ecology with forest community structure. In Campbell, CJ (ed.), Primates in Perspective. Oxford: Oxford University Press, pp. 510–525.Google Scholar
Chen, S-C and Moles, AT (2015) A mammoth mouthful? A test of the idea that larger animals ingest larger seeds. Global Ecology and Biogeography 24, 1269–1280.CrossRefGoogle Scholar
Colwell, RK, Chao, A, Gotelli, NJ, Lin, S-Y, Mao, CX, Chazdon, RL and Longino, JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology 5, 3–21.CrossRefGoogle Scholar
Crockett, CM (1998) Conservation biology of the genus Alouatta. International Journal of Primatology 19, 549–578 CrossRefGoogle Scholar
Defler, TR and Defler, SB (1996) Diet of a group of Lagothrix lagothricha lagothricha in southeastern Colombia. International Journal of Primatology 17, 161–190.CrossRefGoogle Scholar
Dunn, OJ (1961) Multiple comparisons among means. Journal of the American Statistical Association 56, 52–64.CrossRefGoogle Scholar
Eadie, EC (2015) Ontogeny of foraging competence in capuchin monkeys (Cebus capucinus) for easy versus difficult to acquire fruits: a test of the needing to learn hypothesis. PLoS ONE 10, e0138001.CrossRefGoogle ScholarPubMed
Fligner, MA and Policello, GE (1981) Robust rank procedures for the Behrens-Fisher problem. Journal of the American Statistical Association 76, 484–507.CrossRefGoogle Scholar
Fuzessy, LF, Cornelissen, TG, Janson, C and Silveira, FAO (2016) How do primates affect seed germination? A meta-analysis of gut passage effects on Neotropical primates. Oikos 125, 1069–1080.CrossRefGoogle Scholar
Fuzessy, LF, Janson, C and Silveira, FAO (2018) Effects of seed size and frugivory degree on dispersal by Neotropical frugivores. Acta Oecologia 93, 41–47.CrossRefGoogle Scholar
Fuzessy, L, Sobrai, G and Culot, L (2021) Linking howler monkey ranging and defecation patterns to primary and secondary seed dispersal. American Journal of Primatology 82, e23354.Google Scholar
Galetti, M and Pedroni, F (1994) Seasonal diet of capuchin monkeys (Cebus apella) in a semideciduous forest in south-east Brazil. Journal of Tropical Ecology 10, 27–39.CrossRefGoogle Scholar
Ganzhorn, J, Fietz, J, Rakotovao, E, Schwab, D and Zinner, D (1999) Lemurs and the regeneration of dry deciduous forest in Madagascar. Conservation Biology 13, 794–804.CrossRefGoogle Scholar
Gardner, CJ, Bicknell, JE, Baldwin-Cantello, W, Struebig, MJ and Davies, ZG (2019) Quantifying the impacts of defaunation on natural forest regeneration in a global meta-analysis. Nature Communications 10, 4590.CrossRefGoogle Scholar
Google (2022) Available at https://earth.google.com/web/@3.49326733,73.53501244,334.22525041a,102843.84265026d,30.00001759y,-0h,0t,0r (accessed 26 May 2022).Google Scholar
Gonzalez, M, Clavijo, L, Betancur, J and Stevenson, PR (2016) Fruits eaten by woolly monkeys (Lagothrix lagothricha) at local and regional scales. Primates 57, 241–251.CrossRefGoogle ScholarPubMed
Hervé, M (2021) RVAideMemoire (Testing and plotting procedures for biostatistics): an R package in CRAN.Google Scholar
Howe, HF (2014) Diversity storage: implications for tropical conservation and restoration. Global Ecology and Conservation 2, 349–358.CrossRefGoogle Scholar
IDEAM (2019) Boletín predicción climática 2019. Instituto de Hidrología, Meteorología y Estudios Ambientales. Available at: http://www.ideam.gov.co/web/tiempo-y-clima/prediccion-climatica/-/document_library_display/ljPLJWRaQzCm/view/79336843 (accessed 23 January 2022).Google Scholar
Izawa, K (1979) Foods and feeding behavior of wild black-capped capuchin (Cebus apella). Primates 20, 57–76.CrossRefGoogle Scholar
Janson, D and Vegelius, J (1981) Measures of ecological association. Oecologia 49, 371–376.CrossRefGoogle ScholarPubMed
Julliot, C and Sabatier, D (1993) Diet of the red howler monkey (Alouatta seniculus) in French Guiana. International Journal of Primatology 14, 527–550.CrossRefGoogle Scholar
Julliot, C, Simmen, B and Zhang, S (2001) Frugivory and seed dispersal by three Neotropical primates: impact on plant regeneration. In Bongers, F, Charles-Dominique, P, Forget, PM and Théry, M (eds.), Nouragues. Monographiae Biologicae , vol 80. New York: Springer, pp. 197–205.Google Scholar
Koch, F, Ganzhorn, JU, Rothman, JM, Chapman, CA and Fichtel, C (2017) Sex and seasonal differences in diet and nutrient intake in Verreaux’s sifakas (Propithecus verreauxi). American Journal of Primatology 79, e22595.CrossRefGoogle ScholarPubMed
Koné, I, Lambert, JE, Refisch, J and Bakayoko, A (2008) Primate seed dispersal and its potential role in maintaining useful tree species in the Taï region, Côte-d’Ivoire: implications for the conservation of forest fragments. Tropical Conservation Science 1, 293–306.CrossRefGoogle Scholar
Lawton, JH and Brown, VK (1993) Redundancy in ecosystems. In Schulze, ED and Mooney, HA (eds.), Biodiversity and Ecosystem Function. Berlin: Springer, pp. 255–270.Google Scholar
Link, A, Palacios, E, Cortés-Ortiz, L, Stevenson, PR, Cornejo, FM, Mittermeier, RA, Shanee, S, de la Torre, S, Boubli, JP, Guzmán-Caro, DC, Moscoso, P, Urbani, B and Seyjagat, J (2021) Alouatta seniculus. The IUCN Red List of Threatened Species 2021: e.T198676562A198687134. Available at: https://doi.org/10.2305/IUCN.UK.2021-2.RLTS.T198676562A198687134.en (accessed 3 January 2021).CrossRefGoogle Scholar
Lopez, GO, Terborgh, J and Ceballos, N (2005) Food selection by a hyperdense population of red howler monkeys (Alouatta seniculus). Journal of Tropical Ecology 21, 445–450.CrossRefGoogle Scholar
Markl, JS, Schleuning, M, Forget, PM, Jordano, P, Lambert, JE, Traveset, A, Wright, SJ and Böhning-Gaese, K (2012) Meta-analysis of the effects of human disturbance on seed dispersal by animals. Conservation Biology 26, 1072–1081.CrossRefGoogle ScholarPubMed
Mazer, SJ and Wheelwright, NT (1993) Fruit size and shape: allometry at different taxonomic levels in bird-dispersed plants. Evolutionary Ecology 7, 556–575.CrossRefGoogle Scholar
Melin, AD, Chiou, KL, Walco, ER, Bergstrom, ML, Kawamura, S and Fedigan, LM (2017) Trichromacy increases fruit intake rates of wild capuchins (Cebus capucinus imitator). Proceedings of the National Academy of Sciences 114, 10402–10407.CrossRefGoogle ScholarPubMed
Michalski, F and Peres, CA (2005) Anthropogenic determinants of primate and carnivore local extinctions in a fragmented forest landscape of southern Amazonia. Biological Conservation 124, 383–396.CrossRefGoogle Scholar
Monasterio, M and Sarmiento, G (1976) Phenological strategies of plant species in the tropical savanna and the semi-deciduous forest of the Venezuelan Llanos. Journal of Biogeography 3, 325–355.CrossRefGoogle Scholar
Obregón, JR (2007) Comparación de la cantidad y el tipo de semillas dispersadas por Cebus apella y Alouatta seniculus en un bosque fragmentado, San Martín, Meta. Undergraduate thesis, Departmento de Ciencias Biológicas, Universidad de Los Andes.Google Scholar
Peres, CA (1993) Notes on the primates of the Juruá River, western Brazilian Amazonia. Folia Primatologica 61, 97–103.CrossRefGoogle ScholarPubMed
Peres, CA and Roosmalen, MV (2002) Primate frugivory in two species-rich neotropical forests: implications for the demography of large-seeded plants in overhunted areas. In Levey DJ, Silva WR and Galetti M (eds.), Third International Symposium-Workshop on Frugivores and Seed Dispersal. Oxon: CABI Publishing, pp. 407–421.CrossRefGoogle Scholar
Poulsen, JR, Clark, CJ, Connor, EF and Smith, TB (2002) Differential resource use by primates and hornbills: implications for seed dispersal. Ecology 83, 228–240.CrossRefGoogle Scholar
Ramírez, MA and Stevenson, PR (2020) Fruit production needed to maintain populations of woolly monkeys: recommendations for reintroduction projects. Global Ecology and Conservation 21, e00817.CrossRefGoogle Scholar
Rodríguez, GAC and Boher, S (1988) Notes on the biology of Cebus nigrivittatus and Alouatta seniculus in northern Venezuela. Primate Conservation 9, 61–66.Google Scholar
Rosin, C and Poulsen, JR (2016) Hunting-induced defaunation drives increased seed predation and decreased seedling establishment of commercially important tree species in an Afrotropical forest. Forest Ecology and Management 382, 206–213.CrossRefGoogle Scholar
RStudio Team (2020) RStudio: Integrated Development Environment for R v1.3.1093.Google Scholar
Sales, L, Culot, L and Pires, MM (2020) Climate niche mismatch and the collapse of primate seed dispersal services in the Amazon. Biological Conservation 247, 108628.CrossRefGoogle Scholar
Sandino, LI (2006) Flórula de leguminosas de San Martín, Meta. Undergraduate thesis, Departmento de Ciencias Biológicas, Universidad de Los Andes.Google Scholar
Smith, RJ and Jungers, WL (1997) Body mass in comparative primatology. Journal of Human Evolution 32, 523–559.CrossRefGoogle ScholarPubMed
Stevenson, PR (2000) Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia: dispersal distance, germination rates, and dispersal quantity. American Journal of Primatology 50, 275–289.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Stevenson, PR (2007) Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In Dennis, AJ, Schupp, EW, Green, RJ and Westcott, DA (eds.), Seed Dispersal: Theory and its Application in a Changing World. Oxfordshire: CABI Publishing, pp. 340–362.CrossRefGoogle Scholar
Stevenson, PR and Aldana, AM (2008) Potential effects of ateline extinction and forest fragmentation on plant diversity and composition in the western Orinoco Basin, Colombia. International Journal of Primatology 29, 365–377.CrossRefGoogle Scholar
Stevenson, PR, Cardona, L, Cárdenas, S and Link, A (2021a) Oilbirds disperse large seeds at longer distance than extinct megafauna. Scientific Reports 11, 1–8.CrossRefGoogle ScholarPubMed
Stevenson, PR, Castellanos, MC, Pizarro, JC and Garavito, M (2002) Effects of seed dispersal by three Ateline monkey species on seed germination at Tinigua National Park, Colombia. International Journal of Primatology 23, 1187–1204.CrossRefGoogle Scholar
Stevenson, PR, Defler, TR, de la Torre, S, Moscoso, P, Palacios, E, Ravetta, AL, Vermeer, J, Link, A, Urbani, B, Cornejo, FM, Guzmán-Caro, DC, Shanee, S, Mourthé, Í, Muniz, CC, Wallace, RB and Rylands, AB (2021b) Lagothrix lagothricha (amended version of 2020 assessment). The IUCN Red List of Threatened Species 2021:e.T160881218A192309103. Available at: https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T160881218A192309103.en (accessed on 23 January 2023).CrossRefGoogle Scholar
Stevenson, PR, Pineda, M and Samper, T (2005) Influence of seed size on dispersal patterns of woolly monkeys (Lagothrix lagothricha) at Tinigua Park, Colombia. Oikos 110, 435–440.CrossRefGoogle Scholar
Stevenson, PR, Quiñones, MJ and Ahumada, JA (1994) Ecological strategies of woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia. American Journal of Primatology 32, 123–140.CrossRefGoogle ScholarPubMed
Stevenson, PR, Quiñones, MJ and Ahumada, JA (2000) Influence of fruit availability on ecological overlap among four Neotropical primates at Tinigua National Park, Colombia. Biotropica 32, 533–544.CrossRefGoogle Scholar
Terborgh, J, Nuñez-Iturri, G, Pitman, NC, Valverde, FHC, Alvarez, P, Swamy, V, Pringle, EG and Paine, CE (2008) Tree recruitment in an empty forest. Ecology 89, 1757–1768.CrossRefGoogle Scholar
Wang, BC, Sork, VL, Leong, MT and Smith, TB (2007) Hunting of mammals reduces seed removal and dispersal of the Afrotropical tree Antrocaryon klaineanum (Anacardiaceae). Biotropica 39, 340–347.CrossRefGoogle Scholar
Wheeler, BC and Hammerschmidt, K (2013) Proximate factors underpinning receiver responses to deceptive false alarm calls in wild tufted capuchin monkeys: is it counter deception? American Journal of Primatology 75, 715–725.CrossRefGoogle Scholar
Williamson, RE, Webb, SE, Dubreuil, C, Lopez, R, Hernandez, SC, Fedigan, LM and Melin, AD (2021) Sharing spaces: niche differentiation in diet and substrate use among wild capuchins. Animal Behaviour 179, 317–338.CrossRefGoogle Scholar
Zambrano, VAB, Moncada, JZ and Stevenson, PR (2008) Diversity of regenerating plants and seed dispersal in two canopy trees from Colombian Amazon forests with different hunting pressure. International Journal of Tropical Biology 56, 1531–1542.Google Scholar
Zarate-Caicedo, DA and Stevenson, PR (2014) Ecological strategies of woolly monkeys (Lagothrix lagothricha) in a forest fragment (Guaviare, Colombia). In Defler, T and Stevenson, PR (eds.), The Woolly Monkey: Behavior, Ecology, Systematics, and Captive Research. New York: Springer, pp. 227–245.CrossRefGoogle Scholar
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