Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T06:57:31.114Z Has data issue: false hasContentIssue false

Extensive clonal propagation and resprouting drive the regeneration of a Brazilian dry forest

Published online by Cambridge University Press:  10 May 2021

Renato Soares Vanderlei*
Affiliation:
Botany Department, Federal University of Pernambuco. Rua Professor Moraes Rego, Cidade Universitária. 50.670-901. Recife, Pernambuco, Brazil
Maria Fabíola Barros
Affiliation:
Botany Department, Federal University of Pernambuco. Rua Professor Moraes Rego, Cidade Universitária. 50.670-901. Recife, Pernambuco, Brazil Programa de Capacitação Institucional (PCI), Museu Paraense Emílio Goeldi, Av. Magalhães Barata, 66040-170, Belém, Pará, Brazil
Arthur Domingos-Melo
Affiliation:
Botany Department, Federal University of Pernambuco. Rua Professor Moraes Rego, Cidade Universitária. 50.670-901. Recife, Pernambuco, Brazil
Gilberto Dias Alves
Affiliation:
Botany Department, Federal University of Pernambuco. Rua Professor Moraes Rego, Cidade Universitária. 50.670-901. Recife, Pernambuco, Brazil
Ana Beatriz Silva
Affiliation:
Botany Department, State University of Santa Cruz, Rodovia Ilhéus – Itabuna, Salobrinho, km 16. 46.662-900. Ilheus, Bahia, Brazil
Marcelo Tabarelli
Affiliation:
Botany Department, Federal University of Pernambuco. Rua Professor Moraes Rego, Cidade Universitária. 50.670-901. Recife, Pernambuco, Brazil
*
Author for correspondence: *Renato Soares Vanderlei, Email: renato.vanderlei@gmail.com

Abstract

Woody plant resprouting has received considerable attention in the last two decades as human disturbances continue to encroach on terrestrial ecosystems globally. We examined the regeneration mechanisms of a Caatinga dry forest in the context of slash-and-burn agriculture and resprouting ability of the local flora. We excavated two old fields (from 32) experiencing early forest regeneration dominated by the tree Pityrocarpa moniliformis (Fabaceae) to map clonal propagation and, in parallel, submitted 260 seedlings from 13 woody plant species to experimental clipping. What seemed to be ‘seedlings’ popping up around P. moniliformis stumps and remaining adults actually were condensed sets of root suckers connected via complex networks of long, ramified shallow horizontal roots without taproots. We mapped respectively 39 and 783 connected root suckers, which summed 96 m and 910 m in root length. Regarding the seedlings, 33% resprouted across nine species with resprouting rates varying between 5–100%. Seedling height before clipping positively influenced resprouting vigour. Our preliminary results suggest that the Caatinga dry forest supports a relatively high proportion of resprouting species, some of them able to clonally propagate and playing an ecosystem-level role by responding to early forest regeneration and high abundance/biomass across both regenerating and old-growth forests.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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

Arnan, X, Leal, IR, Tabarelli, M, Andrade, JF, Barros, MF, Câmara, T, Jamelli, D, Knoechelman, CM, Meneses, T, Menezes, AGS, Oliveira, FMP, Paula, ASDe, Pereira, SC, Rito, KF, Sfair, JC, Silva, FSDa, Souza, DG, Specht, MJ, Vieira, LA and Andersen, AN (2018) A framework for deriving measures of chronic anthropogenic disturbance: surrogate, direct, single and multi-metric indices in Brazilian Caatinga. Ecological Indicators 94, 274282.CrossRefGoogle Scholar
Arroyo-Rodríguez, V, Melo, FPL, Martínez-Ramos, M, Bongers, F, Chazdon, RL, Meave, JA, Norden, N, Santos, BA, Leal, IR and Tabarelli, M (2017) Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biological Reviews 92, 326340.CrossRefGoogle ScholarPubMed
Barros, MF, Ribeiro, EM, Vanderlei, R, de Paula, AS, Silva, AB, Wirth, R, Cianciaruso, M and Tabarelli, M (2021) Resprouting drives successional pathways and the resilience of Caatinga dry forest in human-modified landscapes. Forest Ecology and Management 482, 112.CrossRefGoogle Scholar
Bellingham, PJ and Sparrow, AD (2000) Resprouting as a life history strategy in woody plant communities. Oikos 89, 409416.CrossRefGoogle Scholar
Bond, WJ and Midgley, JJ (2001) Ecology of sprouting in woody plants: the persistence niche. Trends in Ecology and Evolution 16, 4551.CrossRefGoogle ScholarPubMed
Buisson, E, Le Stradic, S, Silveira, FAO, Durigan, G, Overbeck, GE, Fidelis, A, Fernandes, GW, Bond, WJ, Hermann, JM, Mahy, G, Alvarado, ST, Zaloumis, NP and Veldman, JW (2018) Resilience and restoration of tropical and subtropical grasslands, savannas, and grassy woodlands. Biological Reviews 94, 590609.CrossRefGoogle ScholarPubMed
Chidumayo, EN and Gumbo, DJ (2013) The environmental impacts of charcoal production in tropical ecosystems of the world: a synthesis. Energy for Sustainable Development 17, 8694.CrossRefGoogle Scholar
Clarke, P, Lawes, MJ and Midgley, JJ (2010) Resprouting as a key functional trait in woody plants – challenges to developing new organizing principles. New Phytologist 188, 651654.CrossRefGoogle ScholarPubMed
Derroire, G, Balvanera, P, Castellanos-Castro, C, Decocq, G, Kennard, DK, Lebrija-Trejos, E, Leiva, JA, Odén, PC, Powers, JS, Rico-Gray, V, Tigabu, M and Healey, JR (2016) Resilience of tropical dry forests – a meta-analysis of changes in species diversity and composition during secondary succession. Oikos 125, 13861397.CrossRefGoogle Scholar
Dons, K, Smith-Hall, C, Meilby, H and Fensholt, R (2015) Operationalizing measurement of forest degradation: identification and quantification of charcoal production in tropical dry forests using very high resolution satellite imagery. International Journal of Applied Earth Observation and Geoinformation 39, 1827.CrossRefGoogle Scholar
Espelta, JM, Retana, J and Habrouk, A (2003) Resprouting patterns after fire and response to stool cleaning of two coexisting Mediterranean oaks with contrasting leaf habits on two different sites. Forest Ecology and Management 179, 401414.CrossRefGoogle Scholar
Figueirôa, JM, Pareyn, FGC, Araújo, EL, Silva, CE, Santos, VF, Cutler, DF, Baracat, A and Gasson, P (2006) Effects of cutting regimes in the dry and wet season on survival and sprouting of woody species from the semi-arid caatinga of northeast Brazil. Forest Ecology and Management 229, 294303.CrossRefGoogle Scholar
Hasnat, GNT and Hossain, MK (2019) Global overview of tropical dry forests. In Bhadouria, R (ed.), Handbook of Research on the Conservation and Restoration of Tropical Dry Forests. Hershey, PA: IGI Global, pp. 123.Google Scholar
Hayashi, AH and Appezzato-da-glória, B (2009) Resprouting from roots in four Brazilian tree species. International Journal of Tropical Biology 57, 789800.Google ScholarPubMed
Heinimann, A, Mertz, O, Frolking, S, Egelund Christensen, A, Hurni, K, Sedano, F, Chini, LP, Sahajpal, R, Hansen, M and Hurtt, G (2017) A global view of shifting cultivation: recent, current, and future extent. PLoS ONE 12, 121.CrossRefGoogle ScholarPubMed
Houghton, RA, Byers, B and Nassikas, AA (2015) A role for tropical forests in stabilizing atmospheric CO2 . Nature Climate Change 5, 10221023.CrossRefGoogle Scholar
Jaureguiberry, P, Cuchietti, A, Gorné, LD, Bertone, GA and Díaz, S (2020) Post-fire resprouting capacity of seasonally dry forest species – two quantitative indices. Forest Ecology and Management 473, 112.CrossRefGoogle Scholar
Jenik, J (1994) Clonal growth in woody plants: a review. Folia Geobotanica et Phytotaxonomica 29, 291306.CrossRefGoogle Scholar
Kammesheidt, L (1999) Forest recovery by root suckers and above-ground sprouts after slash-and-burn agriculture, fire and logging in Paraguay and Venezuela. Journal of Tropical Ecology 15, 143157.CrossRefGoogle Scholar
Kennard, DK, Gould, K, Putz, FE, Fredericksen, TS and Morales, F (2002) Effect of disturbance intensity on regeneration mechanisms in a tropical dry forest. Forest Ecology and Management 162, 197208.CrossRefGoogle Scholar
Knoechelmann, CM, Oliveira, FMP, Siqueira, FFS, Wirth, R, Tabarelli, M and Leal, IR (2020) Leaf-cutting ants negatively impact the regeneration of the Caatinga dry forest across abandoned pastures. Biotropica 52, 686696.CrossRefGoogle Scholar
Maass, JM, Balvanera, P, Castillo, A, Daily, GC, Mooney, HA, Ehrlich, P, Quesada, M, Miranda, A, Jaramillo, VJ, García-Oliva, F, Martínez-Yrizar, A, Cotler, H, López-Blanco, J, Pérez-Jiménez, A, Búrquez, A, Tinoco, C, Ceballos, G, Barraza, L and Ayala, R (2005) Ecosystem services of tropical dry forests: insights from long-term ecological and social research on the Pacific coast of Mexico. Ecology and Society 10, 542564.CrossRefGoogle Scholar
McDonald, MA (2010) What are the mechanisms of regeneration post-disturbance in tropical dry forest? Environmental Evidence 37, 224.Google Scholar
Melo, FPL, Arroyo-Rodríguez, V, Fahrig, L, Martínez-Ramos, M and Tabarelli, M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends in Ecology and Evolution 28, 462468.CrossRefGoogle ScholarPubMed
O’Brien, MJ, Leuzinger, S, Philipson, CD, Tay, J and Hector, A (2014) Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nature Climate Change 4, 710714.CrossRefGoogle Scholar
Pausas, JG and Keeley, JE (2014) Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. New Phytologist 204, 5565.CrossRefGoogle ScholarPubMed
Pausas, JG, Pratt, RB, Keeley, JE, Jacobsen, AL, Ramirez, AR, Vilagrosa, A, Paula, S, Kaneakua-Pia, IN and Davis, SD (2016) Towards understanding resprouting at the global scale. New Phytologist 209, 945954.CrossRefGoogle Scholar
Pennington, RT, Lavin, M and Oliveira-Filho, A (2009) Woody plant diversity, evolution, and ecology in the tropics: perspectives from seasonally dry tropical forests. Annual Review of Ecology, Evolution, and Systematics 40, 437457.CrossRefGoogle Scholar
Poorter, L, Bongers, F, Aide, TM and Zambrano, AMA (2016) Biomass resilience of Neotropical secondary forests. Nature 530, 211214.CrossRefGoogle ScholarPubMed
Portillo-Quintero, C, Sanchez-Azofeifa, A, Calvo-Alvarado, J, Quesada, M and do Espirito Santo, MM (2015) The role of tropical dry forests for biodiversity, carbon and water conservation in the neotropics: lessons learned and opportunities for its sustainable management. Regional Environmental Change 15, 10391049.CrossRefGoogle Scholar
Pulla, S, Ramaswami, G, Mondal, N, Chitra-Tarak, R, Suresh, HS, Dattaraja, HS, Vivek, P, Parthasarathy, N, Ramesh, BR and Sukumar, R (2015) Assessing the resilience of global seasonally dry tropical forests. International Forestry Review 17, 91113.CrossRefGoogle Scholar
Rito, KF, Arroyo-Rodríguez, V, Queiroz, RT, Leal, IR and Tabarelli, M (2017 a) Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation. Journal of Ecology 105, 828838.CrossRefGoogle Scholar
Rito, KF, Tabarelli, M and Leal, IR (2017 b) Euphorbiaceae responses to chronic anthropogenic disturbances in Caatinga vegetation: from species proliferation to biotic homogenization. Plant Ecology 218, 749759.CrossRefGoogle Scholar
Rizzini, CT and Heringer, EP (1962) Studies on the underground organs of trees and shrubs from some southern Brazilian savannas. Anais da Academia Brasileira de Ciências 34, 235247.Google Scholar
Sampaio, EVSB, Salcedo, IH and Kauffman, JB (1993) Effect of different fire severities on coppicing of caatinga vegetation in Serra Talhada, PE, Brazil. Biotropica 25, 452460.CrossRefGoogle Scholar
Schacht, WH, Mesquita, RCM, Malechek, JC and Kirmse, RD (1989) Response of caatinga vegetation to decreasing levels of canopy cover. Pesquisa Agropecuaria Brasileira 24, 14211426.Google Scholar
Schwilk, DW and Ackerly, D (2005) Is there a cost to resprouting? Seedling growth rate and drought tolerance in sprouting and nonsprouting Ceanothus (Rhamnaceae). American Journal of Botany 92, 404410.CrossRefGoogle Scholar
Silva, JMC, Leal, IR and Tabarelli, M (2017) Caatinga: The Largest Tropical Dry Forest Region in South America. Cham: Springer International Publishing.CrossRefGoogle Scholar
Singh, SP (1998) Chronic disturbance, a principal cause of environmental degradation in developing countries. Environmental Conservation 25, 12.CrossRefGoogle Scholar
Sobrinho, MS, Tabarelli, M, Machado, IC, Sfair, JC, Bruna, EM and Lopes, AV (2016) Land use, fallow period and the recovery of a Caatinga forest. Biotropica 48, 586597.CrossRefGoogle Scholar
Souza, DG, Sfair, JC, De Paula, AS, Barros, MF, Rito, KF and Tabarelli, M (2019) Multiple drivers of aboveground biomass in a human-modified landscape of the Caatinga dry forest. Forest Ecology and Management 435, 5765.CrossRefGoogle Scholar
Specht, MJ, Santos, BA, Marshall, N, Melo, FPL, Leal, IR, Tabareli, M and Baldauf, C (2019) Socioeconomic differences among resident, users and neighbour populations of a protected area in the Brazilian dry forest. Journal of Environmental Management 232, 607614.CrossRefGoogle ScholarPubMed
Sunderland, T, Apgaua, D, Baldauf, C, Blackie, R, Colfer, C, Cunningham, AB, Dexter, K, Djoudi, H, Gautier, D, Gumbo, D, Ickowitz, A, Kassa, H, Parthasarathy, N, Pennington, RT, Paumgarten, F, Pulla, S, Sola, P, TNG, D, Waeber, P and Wilmé, L (2015) Global dry forests: a prologue. International Forestry Review 17, 19.CrossRefGoogle Scholar
Tabarelli, M, Siqueira, FF, Backé, J, Wirth, R and Leal, IR (2017) Ecology of leaf-cutting ants in human-modified landscapes. In Oliveira, PS and Koptur, S (eds), Ant-Plant Interactions: Impacts of Humans on Terrestrial Ecosystems. Cambridge: Cambridge University Press, pp. 7390.CrossRefGoogle Scholar
Trejo, I and Dirzo, R (2000) Deforestation of seasonally dry tropical forest: a national and local analysis in Mexico. Biological Conservation 94, 133142.CrossRefGoogle Scholar
Trindade, DPF, Sfair, JC, de Paula, AS, Barros, MF and Tabarelli, M (2020) Water availability mediates functional shifts across ontogenetic stages in a regenerating seasonally dry tropical forest. Journal of Vegetation Science 31, 10881099.CrossRefGoogle Scholar
Vesk, PA and Yen, JDL (2019) Plant resprouting: how many sprouts and how deep? Flexible modelling of multi-species experimental disturbances. Perspectives in Plant Ecology, Evolution and Systematics 41, 19.CrossRefGoogle Scholar
Vieira, DLM and Scariot, A (2006) Principles of natural regeneration of tropical dry forests for regeneration. Restoration Ecology 14, 1120.CrossRefGoogle Scholar
Vieira, DLM, Scariot, A, Sampaio, AB and Holl, KD (2006) Tropical dry-forest regeneration from root suckers in Central Brazil. Journal of Tropical Ecology 22, 353357.CrossRefGoogle Scholar
Werden, LK, Calderón-Morales, E, Alvarado, JP, Gutiérrez, LM, Nedveck, DA and Powers, JS (2020) Using large-scale tropical dry forest restoration to test successional theory. Ecological Applications 30, 117.CrossRefGoogle ScholarPubMed