Skip to main content

Advertisement

SpringerLink
Log in

Howlers Are Able to Survive in Eucalyptus Plantations Where Remnant and Regenerating Vegetation Is Available

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Reversing forest loss through reforestation has become a critical strategy to decrease global climate change, and such programs are more likely to be initiated if they can produce a subsequent monetary gain for the host country. As a result, the planting of monocultures of harvestable trees has become widespread and the practice is accelerating. However, little is known about the effect of such reforestation strategies on biodiversity. Here we quantify the demographic patterns of a population of black howlers (Alouatta pigra) living in a 200-ha eucalyptus plantation with connected remnant forests in southeastern Mexico. We compare our results to data from the literature from forest fragments, extensive forest tracts, and different agrosystems. The howler population inhabiting the plantation grew from 69 individuals in 2007 to 77 in 2008 (11.6% growth) and to 84 in 2009 (9.1% growth). During this time the howlers fed extensively on the native vegetation that was growing under the eucalyptus, vines that grew on the plantation trees, and adjacent areas of native secondary growth, but they almost never fed on eucalyptus. Howler density in the plantation was greater than in extensive forest tracts or forest fragments, whereas mean group size was similar to that in the forest tracts and greater than in the fragments and agrosystems. There was no apparent difference in the adult female-to-immature ratio among sites. Our results indicate that plantations that have associated native vegetation can play a positive role in the conservation of this species, but suggest that harvesting regimens must be carefully orchestrated to prevent associated food scarcity.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Araujo, M. B. (1995). The effect of Eucalyptus globulus Labill. plantations on biodiversity: a case study in Serre de Portel (South Portugal). University College London.

  • Arroyo-Rodríguez, V., Asensio, N., & Cristóbal-Azkarate, J. (2008). Demography, life history and migrations in a Mexican mantled howler group in a rainforest fragment. American Journal of Primatology, 70, 114–118.

    Article  PubMed  Google Scholar 

  • Asensio, N., Arroyo-Rodríguez, V., Dunn, J., & Cristóbal-Azkarate, J. (2009). Conservation value of landscape supplementation for howler monkeys living in forest patches. Biotropica, 41, 768–773.

    Article  Google Scholar 

  • Barrueta, R. T., Estrada, A., Pozo, C., & Calmé, S. (2003). Reconocimiento demográfico de Alouatta pigra y Ateles geoffroyi en la Reserva El Tormento, Campeche, México. Neotropical Primates, 11, 165–169.

    Google Scholar 

  • Boland, D. J., & Brophy, J. J. (1993). Essential oils of the eucalypts and related genera. In R. Teranishi, R. G. Buttery, & H. Sugisawa (Eds.), Bioactive volatile compounds from plants (pp. 72–87). Washington, DC: American Chemical Society.

    Chapter  Google Scholar 

  • Bonilla-Sánchez, Y. M., Serio-Silva, J. C., Pozo-Montuy, G., & Bynum, N. (2010). Population status and identification of potential habitats for the conservation of the black howler monkey in northern of Chiapas, Mexico. Oryx, 44, 293–299.

    Article  Google Scholar 

  • Boyd, E. (2010). Societal choice for climate change futures: Trees, biotechnology and clean development. Bioscience, 60, 742–750.

    Article  Google Scholar 

  • Carnus, J. P., Parrotta, J., Brockerhoff, E., Arbez, M., Hactel, H., Kremer, A., et al. (2006). Planted forests and biodiversity. Journal of Forestry, 104, 65–77.

    Google Scholar 

  • Chapman, C. A., & Chapman, L. J. (2002). Foraging challenges of red colobus monkeys: Influence of nutrients and secondary compounds. Comparative Biochemistry and Physiology. Part A, Physiology, 133, 861–875.

    Article  Google Scholar 

  • Close, C. C., Davidson, N. J., & Swanborough, P. W. (2011). Fire history and understorey vegetation: Water and nutrient relations of Eucalyptus bomphocephala and E. delegatensis overstory trees. Forest Ecology and Management, 262, 108–214.

    Article  Google Scholar 

  • CNA. (2010). Comisión Nacional del Agua. www.cna.gob.mx.

  • Cristinacce, A., Switzer, R. A., Cole, R. E., Jones, C. G., & Bell, D. J. (2009). Increasing use of exotic forestry tree species as refuges from nest predation by the critically endangered Mauritius fody Foudia rubra. Oryx, 97–103.

  • Díaz-López, H. M. (2010). Uso del espacio horizontal y vertical por Alouatta pigra en el dosel de plantaciones agroforestales de eucalipto (Eucalyptus grandis) en Balancán. Tabasco: Universidad Juárez Autónoma de Tabasco.

    Google Scholar 

  • Duncan, R. S., & Chapman, C. A. (2003). Consequences of plantation harvest during tropical forest restoration in Uganda. Forest Ecology and Management, 173, 235–250.

    Article  Google Scholar 

  • Dunning, J. B., Danielson, B. J., & Pulliam, R. (1992). Ecological processes that affect populations in complex landscapes. Oikos, 65, 196–175.

    Article  Google Scholar 

  • Engel, V., Jobbagy, E. G., Stieglitz, M., Williams, M., & Jackson, R. B. (2005). Hydrological consequences of Eucalyptus afforestation in the Argentine Pampas. Water Resources Research, 41, 1–14.

    Article  Google Scholar 

  • Estades, C. F., & Temple, S. A. (1999). Deciduous-forest bird communities in a fragmented landscape dominated by exotic pine plantations. Ecological Applications, 9, 573–585.

    Article  Google Scholar 

  • Estrada, A., Castellanos, L. Y. G., Franco, B., Muñoz, D., Ibarra, A., et al. (2002). Survey of the black howler monkey, Alouatta pigra, population at the Mayan site of Palenque, Chiapas, Mexico. Primates, 44, 51–58.

    Article  Google Scholar 

  • Estrada, A., Garber, P. A., Pavelka, M. S. M., & Luecke, L. (2006). Overview of the Mesoamerican primate fauna, primate studies, and conservation concerns. In A. Estrada, P. A. Garber, M. S. M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior and conservation (pp. 1–22). New York: Springer.

    Google Scholar 

  • Estrada, A., Luecke, L., Van Belle, S., Barrueta, E., & Rosales-Meda, M. (2004). Survey of black howler (Alouatta pigra) and spider (Ateles geoffroyi) monkeys in the Mayan sites of Calakmul and Yaxchilan, Mexico and Tikal, Guatemala. Primates, 45, 33–39.

    Article  PubMed  Google Scholar 

  • Estrada, A., Mendoza, A., Castellano, L., Pacheco, R., Van Belle, S., García, Y., et al. (2002). Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque, Chiapas, México. American Journal of Primatology, 58, 45–55.

    Article  PubMed  Google Scholar 

  • FAO. (2009). http:/www.fao.org.

  • Foggo, A., Ozanne, C. M. P., Speight, M. R., & Hambler, C. (2001). Edge effects and tropical forest canopy invertebrates. Plant Ecology, 153, 347–359.

    Article  Google Scholar 

  • Foley, W. J., & Moore, B. D. (2005). Plant secondary metabolites and vertebrate herbivores from physiological regulation to ecosystem function. Current Opinion in Plant Biology, 8, 430–435.

    Article  PubMed  CAS  Google Scholar 

  • Ganzhorn, J. (1987). A possible role of plantations for primate conservation in Madagascar. American Journal of Primatology, 12, 205–215.

    Article  Google Scholar 

  • Greenberg, R., Bichier, P., & Cruz, A. (2004). Bird conservation value of cacao plantations with diverse planted shade in Tabasco, Mexico. Animal Conservation, 22, 105–112.

    Google Scholar 

  • Hannah, L., Midgley, G. F., Lovejoy, T., Bond, W. J., Bush, M., Lovett, J. C., et al. (2002). Conservation of biodiversity in a changing climate. Conservation Biology, 16, 264–268.

    Article  Google Scholar 

  • Harris, T. R., & Chapman, C. A. (2007). Variation in the diet and ranging behavior of black-and-white colobus monkeys: Implications for theory and conservation. Primates, 28, 208–221.

    Article  Google Scholar 

  • Henzi, S. P., Brown, L. R., Barrett, L., & Marais, A. J. (2011). Troop size, habitat use, and diet of chacma baboons (Papio hamadryas ursinus) in commercial pine plantations: Implications for management. International Journal of Primatology, 32, 1020–1032.

    Article  Google Scholar 

  • Houghton, R. A. (2003). Revised estimates of the annual net flux of carbon to the atmosphere from changes in land use and land management 1850–2000. Tellus, 55, 378–390.

    Article  Google Scholar 

  • INEGI (2007). Instituto Nacional de Estadística, Geografía e Informática. Visualizador de ortofotos. http://mapserver.inegi.org.mx/map/visortoDx/visor.html?c=1379&s=geo

  • IPCC. (2007). Climate change 2007: Synthesis report. Geneva: Intergovernmental Panel on Climate Change.

    Google Scholar 

  • IPPC. (2001). Climate change 2001: The scientific basis. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Jackson, R. B., & Baker, J. S. (2010). Opportunities and constraints for forest climate mitigation. BioScience, 60, 698–707.

    Article  Google Scholar 

  • Jackson, R. B., Jobbagy, E. G., Avissar, R., Roy, S. B., Barrett, D. J., Cook, C. W., Farley, K. A., le Maitre, D. C., McCarl, B. A., & Murray, B. C. (2005). Trading water for carbon with biological sequestration. Science, 310, 1944–1947.

    Article  PubMed  CAS  Google Scholar 

  • Keith, H., Mackey, B. G., & Lindenmayer, D. B. (2009). Re-evaluation of forest biomass carbon stocks and lessons from the world’s most carbon-dense forests. Proceedings of the National Academy of Sciences of the USA, 106, 11635–11640.

    PubMed  CAS  Google Scholar 

  • Laurance, W. F., Ferreira, L. V., Rankin-de Merona, J. M., & Laurance, S. G. (1998). Rain forest fragmentation and the dynamics of Amazonian tree communities. Ecology, 79, 2032–2040.

    Article  Google Scholar 

  • Laurance, W. F., Vasconcelos, H. L., & Lovejoy, T. E. (2000). Forst loss and fragmentation in the Amazon: Implications for wildlife conservation. Oryx, 34, 39–45.

    Google Scholar 

  • Lindenmayer, D. B., Wood, J. T., Cunningham, R. B., Crane, M., MacGregor, C., Damian, M., et al. (2009). Experimental evidence of the effects of a changed matrix on conserving biodiversity within patches of native forest in an industrial plantation landscape. Landscape Ecology, 24, 1091–1103.

    Article  Google Scholar 

  • Mattjie-Prates, H., & Bicca-Marques, J. C. (2008). Age-sex analysis of activity budget, diet, and positional behavior in Alouatta caraya in an Orchard Forest. International Journal of Primatology, 29, 703–715.

    Article  Google Scholar 

  • McClean, C. J., Lovett, J. C., Kuper, W., Hannah, L., Sommer, J. H., Barthlott, W., et al. (2005). African plant diversity and climate change. Annals of the Missouri Botanical Gardens, 92, 139–152.

    Google Scholar 

  • Michon, G., & de Foresta, H. (1995). The Indonesian agro-forest model. In P. Halladay & D. A. Gimour (Eds.), Conserving biodiversity outside protected areas: The role of traditional agroecosystems. Gland, Switzerland: IUCN.

    Google Scholar 

  • Murphy, H. T., & Lovett-Doust, J. (2004). Context and connectivity in plant populations and landscape mosaics: Does the matrix matter? Oikos, 105, 3–14.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Nair, P. K. R., Nair, V. D., Kumar, B. M., & Haile, S. G. (2009). Soil carbon sequestration in tropical agroforestry systems: A feasibility appraisal. Environmental Science and Policy, 12, 1099–1111.

    Article  CAS  Google Scholar 

  • Omeja, P. A., Chapman, C. A., & Obua, J. (2009). Enrichment planting does not promote native tropical tree restoration in a former pine plantation. African Journal of Ecology, 47, 650–657.

    Article  Google Scholar 

  • Omeja, P. A., Chapman, C. A., Obua, J., Lwanga, J. S., Jacob, A. L., Wanyama, F., et al. (2011). Intensive tree planting facilitates tropical forest biodiversity and biomass accumulation. Forest Ecology and Management, 261, 703–709.

    Article  Google Scholar 

  • Ostro, L., Silver, S. C., Koontz, F. W., Horwich, R. H., & Brockett, R. (2001). Shifts in social structure of black howler (Alouatta pigra) groups associated with natural and experimental variation in population density. International Journal of Primatology, 22, 733–748.

    Article  Google Scholar 

  • Parmesan, C., & Yohe, G. A. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37–42.

    Article  PubMed  CAS  Google Scholar 

  • Pavelka, M. S. M. (2003). Group, range, and population size of Alouatta pigra at Monkey River, Belize. Neotropical Primates, 11, 187–191.

    Google Scholar 

  • Pérez-Vera, O. A., Yañez-Morales, M. J., Alvarado-Rosales, D., Cibrian-Tovar, D., & García-Díaz, S. E. (2005). Hongos asociados a Eucalipto, Eucalyptus grandis Hill: Maid Fungi. Agrociencia, 39, 311–318.

    Google Scholar 

  • Pounds, J. A., Fogden, M. P. L., & Campbell, J. H. (1999). Biological response to climate change on a tropical mountain. Nature, 398, 611–615.

    Article  CAS  Google Scholar 

  • Pozo-Montuy, G., Bonilla-Sánchez, Y. M., Díaz-López, H. M., & Serio-Silva, J. C. (2009). Estudio poblacional de monos aulladores negros Alouatta pigra habitando dentro de plantaciones de Eucalipto en Balancán, Tabasco. Paper presented at the IV Congreso Mexicano de Primatología, Villahermosa, Tabasco, México.

  • Pozo-Montuy, G., & Serio-Silva, J. C. (2006). Comportamiento alimentario de monos aulladores negros (Alouatta pigra Lawrence Cebidae) en hábitat fragmentado en Balancán Tabasco México. Acta Zoologica Mexicana ns, 22, 53–66.

    Google Scholar 

  • Pozo-Montuy, G., Serio-Silva, J. C., & Bonilla-Sanchez, Y. M. (2011). The influence of the matrix on the survival of arboreal primates in fragmented landscapes. Primates, 52, 139–147.

    Article  PubMed  Google Scholar 

  • Pozo-Montuy, G., Serio-Silva, J. C., Bonilla-Sánchez, Y. M., Bynum, N., & Landgrave, R. (2008). Current status of the habitat and population of the black howler monkey (Alouatta pigra) in Balancán, Tabasco, Mexico. American Journal of Primatology, 70, 1–8.

    Article  Google Scholar 

  • Rode, K. D., Chapman, C. A., Chapman, L. J., & McDowell, L. R. (2003). Mineral resource availability and consumption by colobus in Kibale National Park, Uganda. International Journal of Primatology, 24, 541–573.

    Article  Google Scholar 

  • Rosales-Meda, M., Estrada, A., & López, J. E. (2007). Demographic survey of black howler monkey (Alouatta pigra) in the Lachuá Eco-region in Alta Verapaz, Guatemala. American Journal of Primatology, 70, 231–237.

    Article  Google Scholar 

  • Sauther, M. L., & Cuozzo, F. P. (2009). The impact of fallback foods on wild ring-tailed lemurs biology: A comparison of intact and anthropogenically disturbed habitats. American Journal of Physical Anthropology, 140, 671–686.

    Article  PubMed  Google Scholar 

  • Seppänen, P. (2003). Costo de la captura de carbono en plantaciones de eucalipto en el trópico. Foresta Veracruzana, 5, 1–6.

    Google Scholar 

  • Serio-Silva, J. C., Pozo-Montuy, G., & Bonilla-Sánchez, Y. M. (2006). Black howler monkeys (Alouatta pigra) inhabiting eucalyptus (Eucalyptus grandis) plantations in Tabasco, Mexico: Habitat use and questions to answer. American Journal of Primatology, 68, 35.

    Article  Google Scholar 

  • Trevelin, L. C., Port-Carvalho, M., Silveira, M., & Morell, E. (2007). Abundance, habitat use and diet of Callicebus nigrifrons Spix (Primates, Pitheciidae) in Cantareira State Park, São Paulo, Brazil. Revista Brasileira de Zoologia, 24, 1071–1077.

    Article  Google Scholar 

  • van Belle, S., & Estrada, A. (2006). Demographic features of Alouatta pigra populations in extensive and fragmented forest. In A. Estrada, P. Garber, M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates: Distribution, ecology, behavior and conservation (pp. 121–142). New York: Kluwer Academic/Plenum Press.

    Google Scholar 

  • van Vliet, A., & Schwartz, M. D. (2002). Phenology and climate: The timing of life cycle events as indicators of climate variability and change. International Journal of Climatology, 22, 1713–1714.

    Article  Google Scholar 

  • Walther, G. R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J. C., et al. (2002). Ecological responses to recent climate change. Nature, 416, 389–395.

    Article  PubMed  CAS  Google Scholar 

  • Zanne, A. E., & Chapman, C. A. (2001). Expediting reforestation in tropical grasslands: Distance and isolation from seed sources in plantations. Ecological Applications, 11, 1610–1621.

    Article  Google Scholar 

Download references

Acknowledgments

We thank CONACYT for the graduate studies scholarships awarded to Y. M. Bonilla-Sánchez (no. 165883) and G. Pozo-Montuy (no. 165885), NSERC, and CRC. Hilda M. Díaz, Wilbert Arcos Pozo, and Luis A. Pozo provided help in the field, and we also thank Laura T. Hernández Salazar and Jorge Morales Mávil for their advice throughout this study. Bianca Delfosse translated this article from the original Spanish and made helpful suggestions. We thank the reviewers and Joanna Setchell for their constructive comments that improved the quality of this manuscript.

Author information

Authors and Affiliations

  1. Programa de Doctorado, Instituto de Neuroetología-Universidad Veracruzana, C.P. 91190, Xalapa, Veracruz, Mexico

    Yadira Magali Bonilla-Sánchez & Gilberto Pozo-Montuy

  2. Red de Biología y Conservación de Vertebrados, Instituto de Ecología AC, Xalapa, Veracruz, Mexico

    Juan Carlos Serio-Silva

  3. Department of Anthropology and McGill School of Environment, McGill University, Montreal, QC, H3A 2T7, Canada

    Colin A. Chapman

  4. Department of Anthropology and McGill School of Environment, Wildlife Conservation Society, Bronx, NY, 10460, USA

    Colin A. Chapman

Authors
  1. Yadira Magali Bonilla-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Carlos Serio-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gilberto Pozo-Montuy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Colin A. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Colin A. Chapman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bonilla-Sánchez, Y.M., Serio-Silva, J.C., Pozo-Montuy, G. et al. Howlers Are Able to Survive in Eucalyptus Plantations Where Remnant and Regenerating Vegetation Is Available. Int J Primatol 33, 233–245 (2012). https://doi.org/10.1007/s10764-011-9569-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-011-9569-9

Keywords

Search

Navigation