Skip to main content
SpringerLink
Log in
Book cover

Howler Monkeys pp 111–139Cite as

Seed Dispersal by Howler Monkeys: Current Knowledge, Conservation Implications, and Future Directions

  • Chapter
  • First Online:

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR))

Abstract

Primate seed dispersal has been increasingly recognized as having a potentially profound impact on tropical forest regeneration and plant species composition. Confirming and quantifying this impact, however, has proven to be an important challenge. We review the literature on seed dispersal by howler monkeys (Alouatta spp.) throughout their geographical range and assess the impact for plant populations and communities. Howler monkeys spend ca. 50 % of their feeding time eating fruits from many plant species and different life forms. For some plant species they are probably the only or primary dispersal agent (e.g., fruits with large seeds and/or with hard indehiscent husks), especially in anthropogenically disturbed forests, where other large-bodied frugivores tend to be absent or are locally extinct. In this regard, howlers contribute to secondary succession, aiding in the restoration of degraded habitats. Alouatta spp. swallow most (>90 %) of the seeds they handle, defecating them undamaged. Studies indicate that passage through the howler gut has a positive effect on rates of seed germination. In addition, studies of secondary dispersal indicate that seeds voided in howler dung attract secondary seed dispersers such as rodents and dung beetles. Also, nutrients in the dung may enhance seedling establishment. Although certain components of howler seed dispersal such as seed shadows, post-dispersal seed fate, and seeds/seedlings survival need to be better studied, current information suggests that howler monkeys are effective seed dispersers for many plant species, with important consequences for plant communities and forest regeneration.

Resumen

La dispersión de semillas por primates puede tener un gran impacto potencial sobre la regeneración y composición de especies de plantas en bosques tropicales. Sin embargo, la confirmación y cuantificación de dicho impacto ha constituido un importante reto. Nosotros hacemos una revisión de la literatura sobre dispersión de semillas por monos aulladores (Alouatta spp.) en su rango de distribución geográfica y evaluamos su impacto sobre las poblaciones y comunidades de plantas. Encontramos que los aulladores dedican ca. 50 % de su tiempo a alimentarse de frutos de muchas especies de plantas y varias formas de vida. Ellos pueden ser los únicos o principales dispersores primarios para algunas especies (por ejemplo, frutos con semillas grandes y/o con exocarpo duro e indehiscente), especialmente en bosques perturbados, donde otros frugívoros de tamaño grande tienden a desaparecer. De hecho, estos primates pueden contribuir a la sucesión secundaria, ayudando a la restauración de hábitats degradados. Ellos tragan la mayoría de las semillas que manipulan, defecándolas sin dañarlas. Usualmente, el paso por el tracto digestivo tiene un efecto positivo en la germinación. Además, las semillas que se encuentran en las heces de monos aulladores pueden ser dispersadas por dispersores secundarios como roedores y escarabajos. Sus heces enriquecen el suelo y pueden favorecer el establecimiento de plántulas. Aunque algunos componentes de este mutualismo, como el destino final de las semillas dispersadas y la supervivencia de semillas/plántulas, necesitan ser mejor estudiados, la información actual sugiere que los monos aulladores son dispersores efectivos para muchas especies de plantas, con importantes consecuencias para las comunidades vegetales y la regeneración de bosques.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Amato KR, Estrada A (2010) Seed dispersal patterns in two closely related howler monkey species (Alouatta palliata and A. pigra): a preliminary report of differences in fruit consumption, traveling behavior, and associated dung beetle assemblages. Neotrop Primates 17:59–66

    Google Scholar 

  • Andresen E (1999) Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rainforest. Biotropica 31:145–158

    Google Scholar 

  • Andresen E (2000) Ecological roles of mammals: the case of seed dispersal. In: Entwistle A, Dunstone N (eds) Future priorities for the conservation of mammalian diversity: has the panda had its day? Cambridge University Press, Cambridge

    Google Scholar 

  • Andresen E (2001) Effects of dung presence, dung amount, and secondary dispersal by dung beetles on the fate of Micropholis guyanensis (Sapotaceae) seeds in Central Amazonia. J Trop Ecol 17:61–78

    Google Scholar 

  • Andresen E (2002a) Primary seed dispersal by red howler monkeys and the effect of defecation pattern on the fate of dispersed seeds. Biotropica 34:261–272

    Google Scholar 

  • Andresen E (2002b) Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecol Entomol 27:257–270

    Google Scholar 

  • Andresen E, Feer F (2005) The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests. In: Forget P-M, Lambert J, Hulme P, Vander Wall SB (eds) Seed fate: predation, dispersal and seedling establishment. CAB, Wallingford

    Google Scholar 

  • Andresen E, Levey DJ (2004) Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:145–154

    Google Scholar 

  • Anzures-Dadda A, Andresen E, Martinez ML, Manson RH (2011) Absence of howlers (Alouatta palliata) influences tree seedling densities in tropical rain forest fragments in southern Mexico. Int J Primatol 32:634–651

    Google Scholar 

  • Arroyo-Rodríguez V, Dias PAD (2010) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 71:1–16

    Google Scholar 

  • Beattie AJ, Hughes L (2002) Ant-plant interactions. In: Herrera CM, Pellmyr O (eds) Plant-animal interactions. An evolutionary approach. Blackwell, Oxford

    Google Scholar 

  • Bicca-Marques JC (2003) How do howler monkeys cope with habitat fragmentation. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer Academic, New York

    Google Scholar 

  • Bravo SP (2008) Seed dispersal and ingestion of insect-infested seeds by black howler monkeys in flooded forests of the Paraná river, Argentina. Biotropica 40:47–476

    Google Scholar 

  • Bravo SP (2009) Implications of behavior and gut passage for seed dispersal quality: the case of black and gold howler monkeys. Biotropica 41:751–758

    Google Scholar 

  • Bravo SP (2012a) From which Ocotea diospyrifolia trees does Alouatta caraya (Primates, Atelidae) eat fruits? J Trop Ecol 28:417–420

    Google Scholar 

  • Bravo SP (2012b) The impact of seed dispersal by black and gold howler monkeys on forest regeneration. Ecol Res 27:311–321

    Google Scholar 

  • Bravo SP, Zunino GE (1998) Effects of black howler monkey (Alouatta caraya) seed ingestion on insect larvae. Am J Primatol 45:411–415

    CAS  PubMed  Google Scholar 

  • Bravo SP, Zunino GE (2000) Germination of seeds from three species dispersed by black howler monkeys (Alouatta caraya). Folia Primatol 71:342–345

    CAS  PubMed  Google Scholar 

  • Bravo SP, Kowalewski MM, Zunino GE (1995) Dispersión y germinación de semillas de Ficus monckii por el mono aullador negro (Alouatta caraya). Bol Primatol Latin 5:25–27

    Google Scholar 

  • Chapman CA (1989) Primate seed dispersal: the fate of dispersed seeds. Biotropica 21:148–154

    Google Scholar 

  • Chapman CA (1995) Primate seed dispersal: coevolution and conservation implications. Evol Anthropol 4:74–82

    Google Scholar 

  • Chapman CA, Onderdonk DA (1998) Forests without primates: primate/plant codependency. Am J Primatol 45:127–141

    CAS  PubMed  Google Scholar 

  • 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 Primatol 32:177–192

    Google Scholar 

  • Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: den Boer PJ, Gradwell GR (eds) Dynamics of populations. Center for Agricultural Publication and Documentation, Wageningen

    Google Scholar 

  • Cortés-Ortiz L, Rylands AB, Mittermeier RA (2014) The taxonomy of howler monkeys: integrating old and new knowledge from morphological and genetic studies. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: adaptive radiation, systematics, and morphology. Springer, New York

    Google Scholar 

  • Cramer JM, Mesquita RCG, Williamson GB (2007) Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biol Conserv 137:415–423

    Google Scholar 

  • Cristóbal-Azkarate J, Arroyo-Rodríguez V (2007) Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation. Am J Primatol 69:1013–1029

    PubMed  Google Scholar 

  • Culot L, Huynen MC, Gérard P, Heymann EW (2009) Short-term post-dispersal fate of seeds defecated by two small primate species (Saguinus mystax and Saguinus fuscicollis) in the Amazonian forest of Peru. J Trop Ecol 25:229–238

    Google Scholar 

  • de Figueiredo RA (1993) Ingestion of Ficus enormis seeds by howler monkeys (Alouatta fusca) in Brazil: effects on seed germination. J Trop Ecol 9:541–543

    Google Scholar 

  • de Figueiredo RA, Longatti CA (1997) Ecological aspects of the dispersal of a melastomataceae by Marmosets and Howler monkeys (Primates: Platyrrhini) in a semideciduous forest of southeastern Brazil. Revue d’Ecologie (La Terre et la Vie) 52:3–8

    Google Scholar 

  • Dias PAD, Rangel-Negrin A (2014) Diets of howler monkeys. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation (pp. 21–56). Springer, New York

    Google Scholar 

  • Dunn JC, Asensio N, Arroyo-Rodríguez V, Schnitzer S, Cristóbal-Azkarate J (2012) The ranging costs of a fallback food: liana consumption supplements diet but increases foraging effort in howler monkeys. Biotropica 44(5):705–714. doi:10.1111/j.1744-7429.2012.00856.x

  • Estrada A (2014) Conservation of Alouatta: social and economic drivers of habitat loss, information vacuum and mitigating population declines. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation (pp. 383–409). Springer, New York

    Google Scholar 

  • Estrada A, Coates-Estrada R (1984) Fruit eating and seed dispersal by howlers (Alouatta palliata) in the tropical rain forest of Los Tuxtlas, Veracruz, Mexico. Am J Primatol 6:77–91

    Google Scholar 

  • Estrada A, Coates-Estrada R (1991) Howler monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed dispersal: ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. J Trop Ecol 7:459–474

    Google Scholar 

  • Feeley K (2005) The role of clumped defecation in the spatial distribution of soil nutrients and the availability of nutrients for plant uptake. J Trop Ecol 21:99–102

    Google Scholar 

  • Feer F (1999) Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guianan rain forest. J Trop Ecol 15:129–142

    Google Scholar 

  • Feer F, Forget P-M (2002) Spatio-temporal variations in post-dispersal seed fate. Biotropica 34:555–566

    Google Scholar 

  • Feer F, Julliot C, Simmen B, Forget P-M, Bayart F, Chauvet S (2001) Recruitment, a multi-stage process with unpredictable result: The case of a Sapotaceasae in French Guianan forest. Revue d’Ecologie (La Terre et la Vie) 56:119–145

    Google Scholar 

  • Fleming TH, Kress WJ (2011) A brief history of fruits and frugivores. Acta Oecol 37:521–530

    Google Scholar 

  • Forget P-M, Milleron T, Feer F (1998) Patterns in post-dispersal seed removal by Neotropical rodents and seed fate in relation to seed size. In: Newbery DM, Prins HHT, Brown ND (eds) Dynamics of tropical communities. Blackwell Science, Oxford

    Google Scholar 

  • Forget P-M, Lambert J, Hulme P, Vander Wall SB (2005) Seed fate. Predation, dispersal and seedling establishment. CABI, Wallingford

    Google Scholar 

  • Fragoso JMV, Silvus KM, Correa JA (2003) Long-distance seed dispersal by tapirs increases seed survival and aggregates tropical trees. Ecology 84:1998–2006

    Google Scholar 

  • Garber PA (1986) The ecology of seed dispersal in two species of Callitrichid primates (Saguinus mystax and Saguinus fuscicollis). Am J Primatol 10:155–170

    Google Scholar 

  • Garber PA, Estrada A, Pavelka MSM (2006) New perspectives in the study of Mesoamerican primates: concluding comments and conservation priorities. In: Estrada A, Garber PA, Pavelka M, Luecke L (eds) New perspectives in the study of Mesoamerican primates. Springer, New York

    Google Scholar 

  • Giraldo P, Gómez-Posada C, Martinez J, Kattan G (2007) Resource use and seed dispersal by red howler monkeys (Alouatta seniculus) in a Colombian Andean forest. Neotrop Primates 14:55–64

    Google Scholar 

  • González-Di Pierro AM (2011) Presencia de Alouatta pigra y regeneración en fragmentos forestales de la Selva Lacandona, Ph.D. Thesis, Universidad Nacional Autónoma de México, Morelia, Michoacán

    Google Scholar 

  • Gonzalez-Di Pierro AM, Benítez-Malvido J, Mendez-Toribio M, Zermeno I, Arroyo-Rodríguez V, Stoner KE, Estrada A (2011) Effects of the physical environment and primate gut passage on the early establishment of Ampelocera hottlei standley in rain forest fragments. Biotropica 43:459–466

    Google Scholar 

  • González-Zamora A, Arroyo-Rodríguez V, Chavez O, Sanchez-Lopez 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

    PubMed  Google Scholar 

  • González-Zamora A, Arroyo-Rodríguez V, Oyama AK, Sork V, Chapman CA, Stoner KE (2012) Sleeping sites and latrines of spider monkeys in continuous and fragmented rainforests: implications for seed dispersal and forest regeneration. PLoS One 7:e46852

    Google Scholar 

  • González-Zamora A, Arroyo-Rodríguez V, Escobar F, Rös M, Oyama K, Ibarra-Manríquez G, Stoner KE, Chapman CA (2014) Contagious deposition of seeds in spider monkeys’ sleeping trees limits effective seed dispersal in fragmented landscapes. PloS ONE 9:e89346

    Google Scholar 

  • Graeff VG, Bicca-Marques JC, Astarita LV (2007) Viability and germination of seeds of iguana hackberry, Celtis iguanaea (Jacq) Sargent, ingested by brown howler monkeys, Alouatta guariba clamitans Cabrera, 1940. A Primatologia no Brasil 10:363–374

    Google Scholar 

  • Hernández A (2011) Internal dispersal of seed-inhabiting insects by vertebrate frugivores: a review and prospects. Integr Zool 6:213–221

    PubMed  Google Scholar 

  • Herrera CM (2002) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant-animal interactions. An evolutionary approach. Blackwell, Oxford

    Google Scholar 

  • Howe HF (1980) Monkey dispersal and waste of a Neotropical fruit. Ecology 61:944–959

    Google Scholar 

  • Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228

    Google Scholar 

  • Hulme PE (2002) Seed-eaters: seed dispersal, destruction and demography. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford

    Google Scholar 

  • IUCN (2012) Alouatta. In: IUCN 2012. IUCN Red list of threatened species. Version 2012.2. www.iucnredlist.org. Downloaded on 06 November 2012

    Google Scholar 

  • Janson CH (1983) Adaptation of fruit morphology to dispersal agents in a Neotropical forest. Science 219:187–189

    CAS  PubMed  Google Scholar 

  • Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528

    Google Scholar 

  • Jones MB (1994) Secondary seed removal by ants, beetles, and rodents in a Neotropical moist forest, M.Sc. Thesis. University of Florida, Gainesville

    Google Scholar 

  • Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford

    Google Scholar 

  • Julliot C (1996a) Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. Int J Primatol 17:239–258

    Google Scholar 

  • Julliot C (1996b) Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. Am J Primatol 40:261–282

    Google Scholar 

  • Julliot C (1997) Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understorey of tropical rain forest. J Ecol 85:431–440

    Google Scholar 

  • Julliot C, Sabatier D (1993) Diet of the red howler monkey (Alouatta seniculus) in French Guiana. Int J Primatol 14:527–550

    Google Scholar 

  • Koné I, Lambert JE, Refisch J, 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. Trop Conserv Sci 1:293–306

    Google Scholar 

  • Lambert J (2002a) Red-Tailed Guenons (Cercopithecus ascanius) and Strychnos mitis: evidence for plant benefits beyond seed dispersal. Int J Primatol 22:189–201

    Google Scholar 

  • Lambert J (2002b) Exploring the link between animal frugivory and plant strategies: the case of primate fruit processing and post-dispersal seed fate. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford

    Google Scholar 

  • Lambert JE, Garber PA (1998) Evolutionary and ecological implications of primate seed dispersal. Am J Primatol 45:9–28

    CAS  PubMed  Google Scholar 

  • Marsh LK, Loiselle BA (2003) Recruitment of black howler fruit trees in fragmented forests of northern Belize. Int J Primatol 24:65–86

    Google Scholar 

  • Martínez-Mota R, Serio-Silva JC, Rico-Gray V (2004) The role of canopy ants in removing Ficus perforata seeds from howler monkey (Alouatta palliata mexicana) feces at Los Tuxtlas, Mexico. Biotropica 36:429–432

    Google Scholar 

  • Martins MM (2006) Comparative seed dispersal effectiveness of sympatric Alouatta guariba and Brachyteles arachnoides in southeastern Brazil. Biotropica 38:57–63

    Google Scholar 

  • Martins MM (2008) Fruit diet of Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil: comparison of fruit type, color, and seed size. Primates 49:1–8

    PubMed  Google Scholar 

  • Milton K (1980) The foraging strategy of howler monkeys. A study in primate economics. Columbia University Press, New York

    Google Scholar 

  • Moura ACDA, McConkey KR (2007) The capuchin, the howler, and the caatinga: seed dispersal by monkeys in a threatened Brazilian forest. Am J Primatol 69:220–226

    Google Scholar 

  • Neves N, Feer F, Salmon S, Chateil C, Ponge JF (2010) The impact of red howler monkey latrines on the distribution of main nutrients and topsoil components in tropical rain forests. Aus Ecol 35:545–559

    Google Scholar 

  • Palma AC, Vélez A, Gómez-Posada C, López H, Zárate-Caicedo DA, Stevenson PR (2011) Use of space, activity patterns, and foraging behavior of red howler monkeys (Alouatta seniculus) in an Andean forest fragment in Colombia. Am J Primatol 73:1062–1071

    PubMed  Google Scholar 

  • Pedroni F, Sanchez M (1997) Dispersao de sementes de Pereskia aculeata Muller (Cactaceae) num fragmento florestal no sudeste do Brasil. Rev Brasil Biol 57:479–486

    Google Scholar 

  • Peres CA (1997) Primate community structure at twenty western Amazonian flooded and unflooded forests. J Trop Ecol 13:381–405

    Google Scholar 

  • Peres CA, Palacios E (2007) Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: Implications for animal-mediated seed dispersal. Biotropica 39:304–315

    Google Scholar 

  • Ponce G (2004) Dispersión de semillas por mono araña (Ateles geoffroyi), saraguato negro (Alouatta pigra) y escarabajos coprófagos en el Parque Nacional Tikal, Guatemala, B.Sc. Thesis, Universidad del Valle de Guatemala, Guatemala

    Google Scholar 

  • Ponce G, Andresen E, Cano E, Cuaron AD (2006) Primary seed dispersal by primates and secondary seed dispersal by dung beetles in Tikal, Guatemala. Biotropica 38:390–397

    Google Scholar 

  • Pouvelle S, Feer F, Ponge J-F (2008) Topsoil as affected by dung deposition under resting places of red howler monkey (Alouatta seniculus). Pedosphere 18:691–698

    Google Scholar 

  • Pouvelle S, Jouard S, Feer F, Tully T, Ponge J-F (2009) The latrine effect: Impact of howler monkeys on the distribution of small seeds in a tropical rain-forest soil. J Trop Ecol 25:239–248

    Google Scholar 

  • Ramos-Obregon J (2007) Comparación de la cantidad y el tipo de semillas dispersadas por Cebus apella y Alouatta seniculus en un bosque fragmentado, San Martín; Meta, BSc. Thesis. Departamento de Ciencias Biológicas, Universidad de Los Andes, Bogota

    Google Scholar 

  • Ratiarison S, Forget P-M (2011) Fruit availability, frugivore satiation and seed removal in 2 primate-dispersed tree species. Integr Zool 6:178–194

    PubMed  Google Scholar 

  • Righini N (2004) Germinación de semillas de Ficus perforata ingeridas por monos aulladores (Alouatta palliata mexicana) y monos araña (Ateles geoffroyi vellerosus). Lab Prim Newslett 43:19–20

    Google Scholar 

  • Russo SE, Augspurger CK (2004) Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol Lett 7:1058–1067

    Google Scholar 

  • Russo SE, Chapman CA (2011) Primate seed dispersal: Linking behavioral ecology with forest community structure. In: Campbell CJ, Fuentes AF, MacKinnon KC, Panger M, Bearder S (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Russo SE, Portnoy S, Augspurger CK (2006) Incorporating animal behavior into seed dispersal models: implications for seed shadows and an example for a primate-dispersed tree. Ecology 87:3160–3174

    PubMed  Google Scholar 

  • Santamaría M (1999) Ecologia e comportamento de Alouatta seniculus em uma mata de terra firme na Amazonia Central, M.Sc. Thesis. Universidade Federal de Minas Gerais, Brazil

    Google Scholar 

  • Santos-Heredia C, Andresen E, Zarate DA (2010) Secondary seed dispersal by dung beetles in a Colombian rain forest: effects of dung type and defecation pattern on seed fate. J Trop Ecol 26:355–364

    Google Scholar 

  • Santos-Heredia C, Andresen E, Stevenson P (2011) Secondary seed dispersal by dung beetles in an Amazonian forest fragment of Colombia: influence of dung type and edge effect. Integr Zool 6:399–408

    PubMed  Google Scholar 

  • Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107:15–29

    Google Scholar 

  • Schupp EW, Milleron T, Russo SE (2002) Dissemination limitation and the origin and maintenance of species-rich tropical forests. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford

    Google Scholar 

  • Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353

    PubMed  Google Scholar 

  • Serio-Silva JC, Rico-Gray V (2002a) Influence of microclimate at different canopy heights on the germination of Ficus (Urostigma) seeds dispersed by Mexican howler monkeys (Alouatta palliata mexicana). Interciencia 27:186–190

    Google Scholar 

  • Serio-Silva JC, Rico-Gray V (2002b) Interacting effects of forest fragmentation and howler monkey foraging on germination and dispersal of fig seeds. Oryx 36:266–271

    Google Scholar 

  • Serio-Silva JC, Rico-Gray V (2003) Howler monkeys (Alouatta palliata mexicana) as seed dispersers of strangler figs in disturbed and preserved habitat in southern Veracruz, Mexico. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer Academic, New York

    Google Scholar 

  • Silver SC, Ostro LET, Yeager CP, Horwich R (1998) Feeding ecology of the black howler monkey (Alouatta pigra) in Northern Belize. Am J Primatol 45:263–279

    CAS  PubMed  Google Scholar 

  • 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, Westcott DW (eds) Seed dispersal: theory and its application in a changing world. CAB International, Wallingford

    Google Scholar 

  • Stevenson PR (2011) The abundance of large Ateline monkeys is positively associated with the diversity of plants regenerating in Neotropical forests. Biotropica 43:512–519

    Google Scholar 

  • Stevenson PR, Aldana AM (2008) Potential effects of Ateline extinction and forest fragmentation on plant diversity and composition in the western Orinoco Basin, Colombia. Int J Primatol 29:365–377

    Google Scholar 

  • Stevenson PR, Quiñones MJ, Ahumada JA (1998) Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species, at Tinigua National Park, Colombia. Int J Primatol 19:313–324

    Google Scholar 

  • Stevenson PR, Quiñones MJ, Ahumada JA (2000) The relationship between temporal variation in fruit abundance and ecological overlap among four Neotropical primates in Colombia. Biotropica 32:533–544

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Stoner KE, Riba-Hernandez P, Vulinec K, Lambert JE (2007) The role of mammals in creating and modifying seed shadows in tropical forests and some possible consequences of their elimination. Biotropica 39:316–327

    Google Scholar 

  • Terborgh J, Alvarez-Loayza P, Dexter K, Cornejo F, Carrasco C (2011) Decomposing dispersal limitation: limits on fecundity or seed distribution? J Ecol 99:935–944

    Google Scholar 

  • 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) See dispersal. Theory and its application in a changing world. CABI, Wallingford

    Google Scholar 

  • Vulinec K, Lambert JE (2009) Neutral and niche perspectives and the role of primates as seed dispersers: a case study from Rio Paratari, Brazil. 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, Developments in primatology: progress and prospects. Springer, New York

    Google Scholar 

  • Vulinec K, Lambert JE, Mellow DJ (2006) Primate and dung beetle communities in secondary growth rain forests: Implications for conservation of seed dispersal systems. Int J Primatol 27:855–879

    Google Scholar 

  • Wang B, Smith T (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379–385

    Google Scholar 

  • Wehncke EV, Valdez CN, Dominguez CA (2004) Seed dispersal and defecation patterns of Cebus capucinus and Alouatta palliata: consequences for seed dispersal effectiveness. J Trop Ecol 20:535–543

    Google Scholar 

  • Wilkie DS, Bennett EL, Peres CA, Cunningham SA (2011) The empty forest revisited. Ann New York Acad Sci 1223:120–128

    Google Scholar 

  • Williams-Guillén K, McCann C, Martínez-Sánchez JC, Koontz F (2006) Resource availability and habitat use by mantled howling monkeys in a Nicaraguan coffee plantation: can agroforests serve as core habitat for a forest mammal? Anim Conserv 9:331–338

    Google Scholar 

  • Yumoto T, Kimura K, Nishimura A (1999) Estimation of the retention times and distances of seed dispersed by two monkey species, Alouatta seniculus and Lagothrix lagotricha, in a Colombian forest. Ecol Res 14:179–191

    Google Scholar 

  • Zárate DA, Andresen E, Estrada A, Serio-Silva CJ (2014) Black howler monkey (Alouatta pigra) activity, foraging and seed dispersal patterns in shaded cocoa plantations versus rainforest in southern Mexico. Am J Primatol 76:890–899

    Google Scholar 

Download references

Acknowledgments

The Centro de Investigaciones en Ecosistemas (Universidad Nacional Autónoma de México) provided logistical support to V.A.R. and E.A., and CONICET (Consejo Nacional de Investigaciones Científicas y Tecnológicas, Argentina) and the Universidad de Buenos Aires provided financial support to S.P.B. Banco de la República (Colombia), Primate Conservation, Margot Marsh Fund, Colciencias, Ecopetrol, and Universidad de Los Andes have provided funds to P.R.S.

Author information

Authors and Affiliations

  1. Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico

    Víctor Arroyo-Rodríguez & Ellen Andresen

  2. IEGEBA—Instituto de Ecología, Genética y Evolución de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires—CONICET, Buenos Aires, Argentina

    Susana P. Bravo

  3. Laboratorio de Ecología de Bosques Tropicales y Primatología, Departamento de Ciencias Biológicas, Universidad de Los Andes, Bogotá, Colombia

    Pablo R. Stevenson

Authors
  1. Víctor Arroyo-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ellen Andresen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susana P. Bravo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pablo R. Stevenson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Víctor Arroyo-Rodríguez .

Editor information

Editors and Affiliations

  1. Estación Biológica Corrientes, Museo Argentino de Ciencias Naturales, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Martín M. Kowalewski

  2. Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

    Paul A. Garber

  3. Museum of Zoology, Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA

    Liliana Cortés-Ortiz

  4. Centro de Antropología, Instituto Venezolano de Investigaciones Científicas, Caracas, Venezuela

    Bernardo Urbani

  5. Department of Zoology, Aristotle University of Thessaloniki, GR-54124 Thessaloniki, Thessaloniki, Greece

    Dionisios Youlatos

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Arroyo-Rodríguez, V., Andresen, E., Bravo, S.P., Stevenson, P.R. (2015). Seed Dispersal by Howler Monkeys: Current Knowledge, Conservation Implications, and Future Directions. In: Kowalewski, M., Garber, P., Cortés-Ortiz, L., Urbani, B., Youlatos, D. (eds) Howler Monkeys. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1960-4_5

Download citation

Publish with us

Policies and ethics

Search

Navigation