Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T12:55:17.643Z Has data issue: false hasContentIssue false
  • English
  • Français

Seed fate and seedling recruitment in monkey latrines in rustic cocoa plantations and rain forest in southern Mexico

Published online by Cambridge University Press:  21 December 2018

Diego A. Zárate ,
Ellen Andresen Open the ORCID record for Ellen Andresen [Opens in a new window]  and
Carolina Santos-Heredia
Diego A. Zárate
Affiliation:
Centro de Investigación La Suiza, Corporación Colombiana de Investigación Agropecuaria, Rionegro-Santander, Colombia Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, México Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Ciudad de México, México
Ellen Andresen*
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, México
Carolina Santos-Heredia
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, México Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Ciudad de México, México Escuela de Biología, Universidad Industrial de Santander, Bucaramanga, Colombia
*
*Email: andresen@iies.unam.mx
Get access Rights & Permissions [Opens in a new window]

Abstract

Primates are important seed dispersers in natural ecosystems and agro-ecosystems, but the latter scenario remains under-studied. The degree to which primates favour plant regeneration greatly depends on post-dispersal processes. The main objective of this study was to compare patterns of seed/seedling fate and seedling recruitment in two habitats of the black howler monkey (Alouatta pigra Lawrence 1933), rustic cocoa and rain forest, and two types of seed-deposition locations, monkey latrines and control locations. Field experiments were carried out within the non-overlapping home ranges of six monkey groups, three in cocoa and three in forest. Seed and seedling fates were assessed for one focal tree species, Brosimum lactescens. The probabilities of seed survival (0.52), germination (0.72), seedling establishment (0.73) and early seedling survival (0.38) were not affected by habitat or seed-deposition location. Late seedling survival was similar in the two habitats but was higher in control locations (0.22) than in latrines (0.09). In cocoa, 4641 seedlings of 59 species were recorded, in forest 3280 seedlings of 68 species. Seedling recruitment was similar in both habitats, but latrines had higher densities than control locations. The importance of agro-ecosystems with low management intensity for the maintenance of ecological processes in anthropogenic landscapes is discussed.

Keywords

Agro-ecosystemAlouatta pigraLacandonaplant regenerationshade cocoa
Type
Research Article
Information
Journal of Tropical Ecology , Volume 35 , Issue 1 , January 2019 , pp. 18 - 25
Copyright
© Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Almeida-Rocha, JM, Peres, CA and Oliveira, LC (2017) Primate responses to anthropogenic habitat disturbance: a pantropical meta-analysis. Biological Conservation 215, 30–38.CrossRefGoogle 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. Journal of Tropical Ecology 17, 61–78.CrossRefGoogle Scholar
Andresen, E, Arroyo-Rodríguez, V and Ramos-Robles, M (2018) Primate seed dispersal: old and new challenges. International Journal of Primatology 39, 443–465.CrossRefGoogle Scholar
Anzures-Dadda, A, Andresen, E, Martínez-Velázquez, ML and Manson, RH (2011) Howler monkey absence influences tree seedling densities in tropical rainforest fragments in southern Mexico. International Journal of Primatology 32, 634–665.CrossRefGoogle Scholar
Anzures-Dadda, A, Manson, RH, Andresen, E and Martínez-Velázquez, ML (2016) Possible implications of seed dispersal by the howler monkey for the early recruitment of a legume tree in small rain-forest fragments in Mexico. Journal of Tropical Ecology 32, 340–343.CrossRefGoogle Scholar
Balcomb, SR and Chapman, CA (2003) Bridging the gap: influence of seed deposition on seedling recruitment in a primate-tree interaction. Ecological Monographs 73, 625–642.CrossRefGoogle Scholar
Benítez-Malvido, J, González-Di Pierro, AM, 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
Braga, RF, Carvalho, R, Andresen, E, Anjos, DV, Alves-Silva, E and Louzada, J (2017) Quantification of four different post-dispersal seed deposition patterns after dung beetle activity. Journal of Tropical Ecology 33, 407–410.CrossRefGoogle 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.CrossRefGoogle Scholar
Bravo, SP (2012) The impact of seed dispersal by black and gold howler monkeys on forest regeneration. Ecological Research 27, 311–321.CrossRefGoogle Scholar
Cervantes López, MDJ (2017) Ensambles de anfibios y reptiles en cacaotales de sombra en la Selva Lacandona. Unpublished master’s dissertation, Universidad Nacional Autónoma de México.Google Scholar
Cuarón, AD (2000) Effects of land-cover changes on mammals in a neotropical region: a modeling approach. Conservation Biology 14, 1676–1692.CrossRefGoogle Scholar
Estrada, A and 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. Journal of Tropical Ecology 7, 459–474.CrossRefGoogle Scholar
Estrada, A, Garber, P, Rylands, AB, Roos, C, Fernandez-Duque, E, Di Fiore, A, Nekaris, KAI, Nijman, V, Heymann, E, Lambert, JE, Rovero, F, Barelli, C, Setchell, JM, Gillespie, TR, Mittermeier, RA, Arregoitia, LV, De Guinea, M, Gouveia, S, Dobrovolski, R, Shanee, S, Shanee, N, Boyle, SA, Fuentes, A, Mckinnon, K, Amato, KR, Meyer, ALS, Wich, S, Sussman, RW, Pan, R, Kone, I and LI, B (2017) Impending extinction crisis of the world’s primates: why primates matter. Science Advances 3, e1600946.CrossRefGoogle ScholarPubMed
Estrada, A, Raboy, BE and Oliveira, LC (2012) Agroecosystems and primate conservation in the tropics: a review. American Journal of Botany 74, 696–711.Google ScholarPubMed
Estrada, A, Van Belle, S and García Del Valle, Y (2004) A survey of black howler (Alouatta pigra) and spider (Ateles geoffroyi) monkeys along the río Lacantún, Chiapas, Mexico. Neotropical Primates 12, 70–75.Google Scholar
Feer, F and 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 and Chauvet, S (2001) Recruitment, a multi-stage process with unpredictable result: the case of a Sapotaceae in French Guianan forest. Revue d’ Ecologie-La Terre et la Vie 56, 119–145.Google Scholar
Feer, F, Ponge, J-F, Jouard, S and Gomez, D (2013) Monkey and dung beetle activities influence soil seed bank structure. Ecological Research 28, 93–102.CrossRefGoogle Scholar
Forget, P-M (1990) Seed-dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana. Journal of Tropical Ecology 6, 459–468.CrossRefGoogle Scholar
Forget, P-M, Milleron, T and 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 and Brown, ND (eds), Dynamics of Tropical Communities. Oxford: Blackwell, pp. 25–49.Google Scholar
Goulart, FF, Jacobson, TKB, Zimbres, BQC, Machado, RB, Aguiar, LMS and Fernandes, GW (2012) Agricultural systems and the conservation of biodiversity and ecosystems in the tropics. In Lameed, GA (eds), Biodiversity Conservation and Utilization in a Diverse World. Rijeka, In Tech, pp. 23–58.Google Scholar
Guzmán, A, Link, A, Castillo, JA and Botero, JE (2016) Agroecosystems and primate conservation: shade coffee as potential habitat for the conservation of Andean night monkeys in the Northern Andes. Agriculture, Ecosystems and Environment 215, 57–67.CrossRefGoogle Scholar
Hockings, KJ, Yamakoshi, G and Matsuzawa, T (2017) Dispersal of a human-cultivated crop by wild chimpanzees (Pan troglodytes verus) in a forest-farm matrix. International Journal of Primatology 38, 172–193.CrossRefGoogle Scholar
Iriarte, SBB and Chazdon, RL (2005) Light-dependent seedling survival and growth of four tree species in Costa Rican second-growth rain forests. Journal of Tropical Ecology 21, 383–395.Google Scholar
Julliot, C (1997) Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understory of tropical rain forest. Journal of Ecology 85, 431–440.CrossRefGoogle Scholar
Kurten, EL (2013) Cascading effects of contemporaneous defaunation on tropical forest communities. Biological Conservation 163, 22–32.CrossRefGoogle Scholar
Mayrinck, RC, Vaz, TAA and Davide, AC (2016) Classificação fisiológica de sementes florestais quanto à tolerância à dessecação e ao comportamento no armazenamento. Cerne 22, 85–92.CrossRefGoogle Scholar
Mcconkey, KR (2018) Seed dispersal by primates in Asian habitats: from species, to communities, to conservation. International Journal of Primatology 39, 466–492.CrossRefGoogle Scholar
Mcconkey, KR and O’Farrill, G (2016) Loss of seed dispersal before the loss of seed dispersers. Biological Conservation 201, 38–49.CrossRefGoogle Scholar
Mcconkey, KR, Prasad, S, Corlett, RT, Campos-Arceiz, A, Brodie, JF, Rogers, H and Santamaria, L (2012) Seed dispersal in changing landscapes. Biological Conservation 146, 1–13.CrossRefGoogle Scholar
Moguel, P and Toledo, VM (1999) Biodiversity conservation in traditional coffee systems of Mexico. Conservation Biology 13, 11–21.CrossRefGoogle Scholar
Peres, CA, Emilio, T, Schietti, J, Desmouliere, SJ and LEVI, T (2016) Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proceedings of the National Academy of Sciences USA 113, 892–897.CrossRefGoogle ScholarPubMed
Perfecto, I and Vandermeer, J (2008) Biodiversity conservation in tropical agroecosystems. Annals of the New York Academy of Sciences 1134, 173–200.CrossRefGoogle ScholarPubMed
Poorter, L &Hayashida-Oliver, Y (2000) Effects of seasonal drought on gap and understory seedlings in a Bolivian moist forest. Journal of Tropical Ecology 16, 481–498.CrossRefGoogle Scholar
Pouvelle, S, Feer, F and Ponge, J-F (2008) Topsoil effects of dung deposition under red howler monkey (Alouatta seniculus) resting places. Pedosphere 18, 691–698.CrossRefGoogle Scholar
Russo, SE (2005) Linking seed fate to natural dispersal patterns: factors affecting predation and scatter-hoarding of Virola calophylla seeds in Peru. Journal of Tropical Ecology 21, 243–253.CrossRefGoogle Scholar
Russo, SE and Augspurger, CK (2004) Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecology Letters 7, 1058–1067.CrossRefGoogle Scholar
Santos-Heredia, MC and Andresen, E (2014) Upward movement of buried seeds: another ecological role of dung beetles promoting seedling establishment. Journal of Tropical Ecology 30, 409–417.CrossRefGoogle Scholar
Santos-Heredia, MC, Andresen, E and Zárate, DA (2010) Secondary seed dispersal by dung beetles in a Colombian rain forest: effects of dung type and defecation pattern on seed fate. Journal of Tropical Ecology 26, 355–364.CrossRefGoogle Scholar
Santos-Heredia, C, Andresen, E, Zárate, DA and Escobar, F (2018) Dung beetles and their ecological functions in three agroforestry systems in the Lacandona rainforest of Mexico. Biodiversity and Conservation 27, 2379–2394.CrossRefGoogle Scholar
Schupp, EW (1995) Seed-seedling conflicts, habitat choice, and patterns of plant recruitment. American Journal of Botany 82, 399–409.CrossRefGoogle Scholar
Schupp, EW (2007) The suitability of a site for seed dispersal is context-dependent. In Dennis, AJ, Schupp, EW, Green, RJ and Westcott, DA (eds), Seed Dispersal Theory and its Application in a Changing World. Wallingford: CABI, pp. 445–462.CrossRefGoogle Scholar
Shepherd, VE and Chapman, CA (1998) Dung beetles as secondary seed dispersers: impact on seed predation and germination. Journal of Tropical Ecology 14, 199–215.CrossRefGoogle Scholar
Stevenson, PR (2011) The abundance of large ateline monkeys is positively associated with the diversity of plants regenerating in neotropical forests. Biotropica 43, 1744–7429.CrossRefGoogle Scholar
Vander Wall, SB and Beck, MJ (2012) A comparison of frugivory and scatter-hoarding seed-dispersal syndromes. Botanical Review 78, 10–31.CrossRefGoogle Scholar
Vander Wall, SB, Forget, P-M, Lambert, J and Hulme, P (2005) Seed fate pathways: filling the gap between parent and offspring. In Forget, P-M, Lambert, J, Hulme, P and Vander Wall, SB (eds), Seed Fate: Predation, Dispersal and Seedling Establishment. Wallingford: CABI, pp. 1–8.Google Scholar
Wang, BC and Smith, TB (2002) Closing the seed dispersal loop. Trends in Ecology and Evolution 17, 379–385.CrossRefGoogle Scholar
Williams-Guillén, K, McCann, C, Martínez Sánchez, JC and Foontz, 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? Animal Conservation 9, 331–338.CrossRefGoogle Scholar
Zárate, DA, Andresen, E, Estrada, A and Serio-Silva, JC (2014) Black howler monkey (Alouatta pigra) activity, foraging and seed dispersal patterns in shaded cocoa plantations versus rainforest in southern Mexico. American Journal of Primatology 76, 890–899.CrossRefGoogle ScholarPubMed