[en] Increasingly large proportions of tropical forests are anthropogenically disturbed. Where natural regeneration is possible at all, it requires the input of plant seeds through seed dispersal from the forest matrix. Zoochorous seed dispersal – the major seed dispersal mode for woody plants in tropical forests – is particularly important for natural regeneration. In this study, covering a period of more than 20 years, we show that small New World primates, the tamarins Saguinus mystax and Leontocebus nigrifrons, increase their use of an anthropogenically disturbed area over time and disperse seeds from primary forest tree species into this area. Through monitoring the fate of seeds and through parentage analyses of seedlings of the legume Parkia panurensis from the disturbed area and candidate parents from the primary forest matrix, we show that tamarin seed dispersal is effective and contributes to the natural regeneration of the disturbed area.
Research Center/Unit :
Chair of Statistics, University of Goettingen HEC Research - Asset and Risk Management
Disciplines :
Environmental sciences & ecology
Author, co-author :
Heymann, Eckhard W.
Culot, Laurence ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Knogge, Christoph
Smith, Andrew C.
Tirado Herrera, Emerita R.
Stojan-Dolar, Mojca
Ferrer, Yvan Lledo
Kubisch, Petra
Kupsch, Denis
Slana, Darja
Koopmann, Mareike Lena
Ziegenhagen, Brigit
Bialozyt, Ronald
Mengel, Christina
Hambuckers, Julien ; Université de Liège - ULiège > HEC Liège : UER > Finance de Marché
Mayaux, P. et al. Tropical forest cover change in the 1990s and options for future monitoring. Philosophical Transactions of the Royal Society of London B: Biological Sciences 360, 373–384, 10.1098/rstb.2004.1590 (2005).
Aide, T. M. et al. Deforestation and reforestation of Latin America and the Caribbean (2001–2010). Biotropica 45, 262–271, 10.1111/j.1744-7429.2012.00908.x (2013).
Chazdon, R. L. Secondary growth. The promise of tropical forest regeneration in an age of deforestation. (University of Chicago Press, 2014).
Arroyo-Rodríguez, V. et al. Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biological Reviews 92, 326–340, 10.1111/brv.12231 (2017).
Wunderle, J. M. Jr. The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. Forest Ecology and Management 99, 223–235 (1997).
Chazdon, R. L. & Guariguata, M. R. Natural regeneration as a tool for large-scale forest restoration in the tropics: prospects and challenges. Biotropica 48, 716–730, 10.1111/btp.12381 (2016).
del Castillo, R. F. & Ríos, M. A. P. Changes in seed rain during secondary succession in a tropical montane cloud forest region in Oaxaca, Mexico. Journal of Tropical Ecology 24, 433–444, 10.1017/S0266467408005142 (2008).
Tabarelli, M. & Peres, C. A. Abiotic and vertebrate seed dispersal in the Brazilian Atlantic forest: implications for forest regeneration. Biological Conservation 106, 165–176, 10.1016/S0006-3207(01)00243-9 (2002).
Gorchov, D. L., Cornejo, F., Ascorra, C. & Jaramillo, M. The role of seed dispersal in the natural regeneration of rain forest after strip-cutting in the Peruvian Amazon. Vegetatio 107, 339–349 (1993).
Duncan, R. S. & Chapman, C. A. Seed dispersal and potential forest succession in abandoned agriculture in tropical Africa. Ecological Applications 9, 998–1008 (1999).
Rylands, A. B. Habitat and the evolution of social and reproductive behavior in Callitrichidae. American Journal of Primatology 38, 5–18 (1996).
Buchanan-Smith, H. M., Hardie, S. M., Caceres, C. & Prescott, M. J. Distribution and forest utilization of Saguinus and other primates of the Pando Department, Northern Bolivia. International Journal of Primatology 21, 353–379 (2000).
Yoneda, M. Ecological study of the saddle backed tamarin (Saguinus fuscicollis) in Northern Bolivia. Primates 25, 1–12 (1984).
Egler, S. G. Feeding ecology of Saguinus bicolor bicolor (Callitrichidae: Primates) in a relict forest in Manaus, Brazilian Amazonia. Folia Primatologica 59, 61–76 (1992).
Knogge, C. & Heymann, E. W. Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis: diversity and characteristics of plant species. Folia Primatologica 74, 33–47 (2003).
Peres, C. A. Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in Amazonian terra firme forest. Journal of Zoology, London 230, 567–592 (1993).
Culot, L. Primary seed dispersal by two sympatric species of tamarins, Saguinus fuscicollis and Saguinus mystax, and post-dispersal seed fate, Université de Liege, (2009).
Oliveira, A. C. M. & Ferrari, S. F. Seed dispersal by black-handed tamarins, Saguinus midas niger (Callitrichinae, Primates): Implications for the regeneration of degraded forest habitats in eastern Amazonia. Journal of Tropical Ecology 16, 709–716 (2000).
Culot, L., Muñoz Lazo, F. J. J., Poncin, P., Huynen, M. C. & Heymann, E. W. Seasonal variation in seed dispersal by tamarins alters seed rain in a secondary rainforest. International Journal of Primatology 31, 553–569 (2010).
Kupsch, D., Waltert, M. & Heymann, E. W. Forest type affects prey foraging of saddleback tamarins, Saguinus nigrifrons. Primates 54, 403–413 (2014).
Rylands, A. B. et al. Taxonomic review of the New World tamarins (Primates: Callitrichidae). Zoological Journal of the Linnean Society 177, 1003–1028, 10.1111/zoj.12386 (2016).
Matauschek, C., Roos, C. & Heymann, E. W. Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group. American Journal of Physical Anthropology 144, 564–574 (2011).
Marengo, J. A. et al. The drought of Amazonia in 2005. Journal of Climate 21, 495–516, 10.1175/2007jcli1600.1 (2008).
Lewis, S. L., Brando, P. M., Philipps, O. L., van der Heijden, G. M. & Nepstad, D. The 2010 Amazon drought. Science 331, 554 (2011).
Condit, R., Hubbell, S. P. & Foster, R. B. Assessing the response of plant functional types to climatic change in tropical forests. Journal of Vegetation Science 7, 405–416 (1996).
Laurance, W. F. et al. Effects of a strong drought on Amazonian forest fragments and edges. Journal of Tropical Ecology 17, 771–785 (2001).
Engelbrecht, B. M. et al. Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447, 80–82 (2007).
Heymann, E. W. Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru. Journal of Zoology, London 237, 211–226 (1995).
Smith, A. C. et al. Long-term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): effects of foraging, thermoregulation, predation, and resource defense constraints. American Journal of Physical Anthropology 134, 340–353 (2007).
Heymann, E. W. et al. DNA fingerprinting validates seed dispersal curves from observational studies in the Neotropical legume Parkia. PLoS One 7, e35480 (2012).
Heymann, E. W. et al. Long-term consistency in spatial patterns of primate seed dispersal. Ecology and Evolution 7, 1435–1441 (2017).
Gelmi-Candusso, T. et al. Estimating seed dispersal distance: a comparison of methods using animal movement and plant genetic data on two primate-dispersed Neotropical plant species. Ecology and Evolution ece3.5422 https://doi.org/5410.1002/ece5423.5422 (2019).
Smith, A. C. Comparative ecology of saddleback (Saguinus fuscicollis) and moustached (Saguinus mystax) tamarins, University of Reading, (1997).
Lindell, C. The value of animal behavior in evaluations of restoration success Restoration Ecology 16 (2008).
Martin, P. & Bateson, P. Measuring behaviour: an introductory guide. 3 edn, (Cambridge University Press, 2007).
Culot, L., Huynen, M.-C. & Heymann, E. W. Primates and dung beetles: two dispersers are better than one in secondary forest. International Journal of Primatology 39, 397–414, 10.1007/s10764-018-0041-y (2018).
Hopkins, H. C. Parkia (Leguminosae, Mimosoideae). Flora Neotropica 43, 1–124 (1986).
Bialozyt, R. et al. Primate seed dispersal leaves spatial genetic imprint throughout subsequent life stages of the Neotropical tree Parkia panurensis. Trees 28, 1569–1575 (2014).
Koopman, S. J. Exact initial Kalman filtering and smoothing for nonstationary time series models. Journal of the American Statistical Association 92, 1630–1638, 10.1080/01621459.1997 (1997).
Kendall, M. & Stuart, A. The advanced theory of statistics, vol 3. 4 edn, (Griffin, 1983).
Brockwell, P. J. & Davis, R. A. Introduction to time series and forecasting. (Springer, 1996).
TIBCO Software Inc. Statistica (Software-System für Datenanalyse), Version 13, http://statistica.io. (2017).
Kupsch, D. Comparison in prey search and capture success of Saguinus fuscicollis between primary and secondary forest. (Master thesis, Georg-August University Göttingen, 2011).