Abstract
Seed predation and dispersal play key roles in the regeneration of tropical trees. Pre-dispersal predation may cause high mortality in seed crops. Seeds may escape pre-dispersal predation when ingested with the fruit pulp and moved away from the parent trees by frugivores. In southern Mexico, we investigated if seed traits (i.e., length, width, and mass) and seed damage by insects on Dialium guianense differed according to seed source: from the tree crowns, the ground, and from howler (Alouatta pigra) and spider monkey (Ateles geoffroyi) feces. We counted the number of seeds with circular entrance and/or exit holes in their tegument. Ingested seeds were larger, heavier, and wider than non-ingested seeds. Seeds ingested by the howler were, however, significantly larger than those ingested by the spider monkey. Damaged seeds showed the lowest values for all seed traits. The proportion of damage declined significantly from seeds on the ground (37 %), to seeds in spider monkey feces (29 %), to seeds from tree crowns (11 %), and finally to seeds in howler monkey feces (7 %). Fruit selection by primates influences dispersal quality differently, even when feeding on the same plant species. The howler monkey may increase the reproductive success of D. guianense by selecting larger and predation-free seeds/fruits.
Similar content being viewed by others
References
Amato KR, Garber PA (2014) Nutrition and foraging strategies of the black howler monkey (Alouatta pigra) in Palenque National Park, Mexico. Am J Primatol 76:774–787. doi:10.1002/ajp.22268
Baraloto C, Forget PM (2007) Seed size, seedling morphology, and response to deep shade and damage in Neotropical rain forest trees. Am J Bot 94:901–911
Beckman NG, Muller-Landau HC (2011) Linking fruit traits to variation in predispersal vertebrate seed predation, insect seed predation, and pathogen attack. Ecology 92:2131–2140
Benítez-Malvido J, González-Di Pierro AM, Lombera R, Guillén S, Estrada A (2014) Seed source, seed traits, and frugivore habits: implications for dispersal quality in two sympatric primates. Am J Bot 101:970–978
Boege K, Dirzo R (2004) Intraspecific variation in growth, defense and herbivory in Dialium guianense (Caesalpiniaceae) mediated by edaphic heterogeneity. Plant Ecol 175:59–69
Bravo SP (2008) Seed dispersal and ingestion of insect-infested seeds by black howler monkeys in flooded forests of the Parana River, Argentina. Biotropica 40:471–476
Burgos A, Grezb AA, Bustamante RO (2008) Seed production, pre-dispersal seed predation and germination of Nothofagus glauca (Nothofagaceae) in a temperate fragmented forest in Chile. For Ecol Manag 255:1226–1233
Chaves OM, Stoner KE, Arroyo-Rodríguez V, Estrada A (2011) Effectiveness of spider monkeys (Ateles geoffroyi vellerosus) as seed dispersers in continuous and fragmented rain forests in Southern Mexico. Int J Prim 1:177–192
Cipollini ML, Stiles EW (1991) Seed predation by the bean weevil Acanthoscelides obtectus on Phaseolus species: consequences for seed size, early growth and reproduction. Oikos 60:205–214
Crawley MJ (1992) Seed predators and plant population dynamics. In: Fenner M (ed) The ecology of regeneration in plant communities. Commonwealth Agricultural Bureau International, Wallingford, pp 157–191
Crawley M (1993) GLIM for ecologists. Blackwell, Cambridge
Cullen J, Julien M, Mcfadyen R (2012) Biological control of weeds in Australia. CSIRO Publishing, Melbourne
Dew JL (2008) Spider monkeys as seed dispersers. In: Campbell CJ (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 155–182
Di Fiore A, Campbell CJ (2007) The Atelines: variation in ecology, behavior, and social organization. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger M, Bearder S (eds) Primates in perspective. Oxford University Press, Oxford, pp 155–185
Di Fiore A, Link A, Dew JL (2008) Diets of wild spider monkeys. In: Campbell CJ (ed) Spider monkeys: behaviour, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 81–137
Estrada A, Van belle S, García Del Valle Y (2004) Survey of black howler (Alouatta pigra) and spider (Ateles geoffroyi) monkeys along the Río Lacantún, Chiapas, Mexico. Neotrop Primates 12:70–75
Felton AM, Felton A, Raubenheimer D, Simpson SJ, Foley WJ, Wood JT, Lindenmayer DB (2009a) Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav Ecol 20:685–690. doi:10.1093/beheco/arp021
Felton AM, Felton A, Lindenmayer DB, Foley WJ (2009b) Nutritional goals of wild primates. Funct Ecol 23:70–78
Fox CW, Wallin WG, Bush ML, Czesak ME, Messina FJ (2012) Effects of seed beetles on the performance of desert legumes depend on host species, plant stage, and beetle density. J Arid Environ 80:10–16
Fricke E, Tewksbury JJ, Rogers HS (2014) Multiple natural enemies cause distance-dependent mortality at the seed-to-seedling transition. Ecol Lett 17:593–598
Gómez-Pompa A, Dirzo R (1995) Atlas de las áreas naturales protegidas de México. CONABIO-INE, Mexico City
González-Di Pierro AM, Benítez-Malvido J, Méndez-Toribio M, Zermeño I, Arroyo-Rodríguez V, Stoner KE, Estrada A (2011) Effects of the physical environment and primate gut passage on the early establishment of an old-growth forest tree species (Ampelocera hottlei Standley) in tropical rain forest fragments. Biotropica 43:459–466
González-Zamora A, Arroyo-Rodríguez V, Chaves OM, Sánchez-López S, Stoner KE, Riba-Hernández P (2009) Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions. Am J Primatol 71:8–20
Howe HF, Smallwood J (1986) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228
Jansen PA, Hirscha BT, Emsensb W-J, Zamora-Gutiérrez V, Wikelskia M, Kayset R (2012) Thieving rodents as substitute dispersers of megafaunal seeds. PNAS 109:12610–12615
Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528
Janzen DH (1980) Specificity of seed-attacking beetles in a Costa Rican deciduous forest. J Ecol 68:929–952
Johnson CD (1981) Interactions between bruchid (Coleoptera) feeding guilds and behavioral patterns of pods of the Leguminosae. Environ Entomol 10:249–253
Jordano P (2014) Fruits and frugivory. In: Ghallager RS (ed) Seeds: the ecology of regeneration in plant communities, 3rd edn. CABI Publishing, Wallingford, pp 18–61
Julliot C (1996) Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. Am J Primatol 40:261–282
Kalko EKV, Herre EA, Handley CO (1996) Relation of fig fruit characteristics to fruit-eating bats in the new and old world tropics. J Biogeo 23:565–576
Lambert JE (1998) Primate digestion: interaction among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20
Link A, Di Fiore A (2006) Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. J Trop Ecol 22:235–246
Mariaca-Méndez R (2002) Marqués de Comillas, Chiapas: procesos de inmigración en el trópico húmedo de México. Ph.D. Dissertation, Universidad Iberoamericana, Mexico
Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Pro Roy Soc B-Biol Sci 273:2575–2584
Martins MM (2006) Comparative seed dispersal effectiveness of sympatric Alouatta guariba and Brachyteles arachnoides in southeastern Brazil. Biotropica 38:57–63
Milton K (1981) Food choice and digestive strategies by two sympatric primate species. Am Nat 117:496–505
Milton K (1998) Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobinae. Int J Primatol 19:513–548
Moles AT, Warton DI, Westoby M (2003) Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 84:3148–3162
Nakagawa M et al (2005) Predispersal seed predation by insects vs. vertebrates in six Dipterocarp species in Sarawak, Malaysia. Biotropica 37:389–396
Naranjo E (2009) Ecology and conservation of Baird’s tapir in Mexico. Trop Conserv Sci 2:140–158
Norconk MA, Wright BW, Conklin-Brittain NL, Vinyard CJ (2008) Mechanical and nutritional properties of foods as factors in Plattirrhyne dietary adaptations. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates: comparative perspectives in the study of behavior, ecology and conservation. Springer, New York, pp 279–319
Paz H, Martínez-Ramos M (2003) Seed mass and seedling performance within eight species of Psychotria (Rubiaceae). Ecology 84:439–450
Pennington TD, Sarukhán J (1998) Árboles tropicales de México. UNAM-FCE, Mexico
Peres CA (1991) Seed predation of Cariniana micrantha (Lecythidaceae) by brown capuchin monkeys in Central Amazonia. Biotropica 23:262–270
Port-Carvalho M, Ferrari SF (2004) Occurrence and diet of the black bearded saki (Chiropotes satanas satanas) in the fragmented landscape of western Maranhão, Brazil. Neotrop Primates 12:17–21
R-Core-Team-R (2015) R: a language and environment for statistical computing. Foundation for statistical computing, Vienna, Austria. In: computing, R.F.F.S. (ed). URL http://www.r-project.org/.
Rey PJ, Gutierrez LE, Alcantara J, Valera F (1997) Fruit size in wild olives: implications for avian seed dispersal. Funct Ecol 11:611–618
Robertson AW, Trass A, Ladley JJ, Kelly D (2006) Assessing the benefits of frugivory for seed germination: the importance of the deinhibition effect. Funct Ecol 20:58–66
Russo SE, Chapman CA (2011) Primate seed dispersal: linking behavioural ecology with forest community structure. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspective 523-534. Oxford University Press, Oxford
Sallabanks R, Courtney SP (1992) Frugivory, seed predation, and insect–vertebrate interactions. Ann Rev Entomol 37:377–400
Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revised: a conceptual review. New Phytol 188:333–353
Shiels AB, Drake DR (2011) Are introduced rats (Rattus rattus) both seed predators and dispersers in Hawaii? Biol Inv 13:883–894
Silvius KM, Fragoso JMV (2002) Pulp handling by vertebrate seed dispersers increases palm seed predation by bruchid beetles in the northern Amazon. J Ecol 90:1024–1032
Simão I, Maës Dos Santos FA, Pizzo MA (1997) Vertical stratification and diet of psittacids in a tropical lowland forest of Brazil. Ararajuba 5:169–174
Sokal RS, Rohlf FJ (1995) Biometry. Freeman and Company, New York
Stevenson PR, Castellanos MC, Pizarro JC, Garavito M (2002) Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. Int J Primatol 23:1187–1204
Stevenson PR, Pineda M, Samper T (2005) Influence of seed size on dispersal patterns of woolly monkeys (Lagothrix lagothricha) at Tinigua Park, Colombia. Oikos 110:435–440
Traveset A, Robertson AW, Rodríguez-Pérez J (2007) A review on the role of endozoochory in seed germination. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CABI Publishing, Wallingford, pp 78–103
Vallejo-Marín M, Domínguez CA, Dirzo R (2006) Simulated predation reveals a variety of germination responses of Neotropical rainforest species. Am J Bot 93:360–376
Van Der Pijl L (1982) Principles of dispersal in higher plants. Springer-Verlag, Berlin 82 pp
Vieira ICG, Gavão N, Rosa NA (1996) Caracterização morfológica de frutos e germinação de sementes de espécies arbóreas nativas da Amazônia. Boletim Paraense Emílio Goeldi, Série Botânica 12:271–288
Wheelwright NT (1985) Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818
Acknowledgments
This research was supported by grants from the Consejo Nacional de Ciencia y Tecnología, Mexico (CONACyT-79121) and Universidad Nacional Autónoma de México (PAPIIT IN206111 and DGAPA sabbatical grant) to J. Benítez-Malvido. We thank the Comisión Nacional de Áreas Naturales Protegidas (CONANP, permission number SGPA/DGVS/07830)) for granting permits to work in the MABR and the Instituto de Investigaciones en Ecosistemas y Sustentabilidad, UNAM, for providing logistical support. We are grateful to G. Lombera for his valuable assistance in the field and to F. Noguera and J. Romero-Nápoles for identifying the insect taxa. We are grateful for the technical support provided by J. M. Lobato-García, J. Rodríguez-Velázquez, H. Ferreira, and A. Valencia-García. We want to thank L. Culot and an anonymous reviewer whose comments and suggestions improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R.A. Montgomery.
Rights and permissions
About this article
Cite this article
Benítez-Malvido, J., Zermeño-Hernández, I., González-DiPierro, A.M. et al. Frugivore choice and escape from pre-dispersal seed predators: the case of Dialium guianense and two sympatric primate species in southern Mexico. Plant Ecol 217, 923–933 (2016). https://doi.org/10.1007/s11258-016-0617-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-016-0617-6