Tropical cloud forest recovery: the role of seed banks in pastures dominated by an exotic grass

Author

• Guadalupe Williams-Linera
• , Martha Bonilla-Moheno 
• , Fabiola López-Barrera

Abstract

Soil seed banks may contribute to forest recovery, but the presence of exotic grasses may represent a constraint for the natural regeneration process. This study aims to evaluate the composition of seed banks in three successional stages of the lower montane peri-urban forest in Veracruz, Mexico, and experimentally determine the role of an exotic grass (Cynodon plectostachyus) in suppressing seed bank expression. For this, soil samples were collected from an abandoned pasture (P), a young secondary forest (SF), and an old secondary forest (F), and grass was experimentally removed in P. Seed density (seeds/m2) was higher in P (12,189 ± 2421), followed by SF (2825 ± 347) and F (3552 ± 865) with 76, 75 and 78 species, respectively. Tree seeds accounted for 1689 (P), 126 (SF) and 265 (F) emerged seedlings of 6, 8 and 6 tree species, respectively. The highest percentage of pioneer tree species was recorded in P seed banks (99 %). Similarity in tree species composition of the seed banks was higher between P and SF (Jaccard = 0.8) than between P and F (0.5). Similarity between soil seed bank tree species and tree standing vegetation was higher in P than in SF and F. Aboveground (1810 g/m2) and belowground (508 g/m2) biomass of C. plectostachyus is suppressing the emergence of individuals from the seed bank: when the grass was removed, nine woody species became established. Exotic grass removal in small nuclei may trigger early forest recovery through allowing the establishment of the tree species already present in the soil seed bank.

References

1. Aide M, Cavelier J (1994) Barriers to lowland tropical forest restoration in the Sierra Nevada de Santa Marta, Colombia. Restor Ecol 2:219–229CrossRef
2. Alvarez-Aquino C, Williams-Linera G, Newton AC (2005) Disturbance effects on the seed bank of mexican cloud forest fragments. Biotropica 37:337–342CrossRef
3. Chazdon RL (2003) Tropical forest recovery: legacies of human impact and natural disturbances. Perspect Plant Ecol Evol Syst 6:51–71CrossRef
4. Cole RJ, Holl KD, Zahawi RA (2010) Seed rain under tree islands planted to restore degraded lands in a tropical agricultural landscape. Ecol Appl 20:1255–1269CrossRefPubMed
5. Colwell RK (2013) EstamateS: statistical estimation of species richness and shared especies for samples. Version 9. http://​purl.​oclc.​org/​estimates
6. Corbin JD, Holl KD (2012) Applied nucleation as a forest restoration strategy. For Ecol Manag 265:37–46CrossRef
7. Craven D, Hall J, Verjans JM (2009) Impacts of herbicide application and mechanical cleanings on growth and mortality of two timber species in saccharum spontaneum grasslands of the Panama canal watershed. Restor Ecol 17:751–761CrossRef
8. Crawley MJ (2007) The R Book. Wiley, ChichesterCrossRef
9. Cubiña A, Aide TM (2001) The effect of distance from forest edge on seed rain and soil seed bank in a tropical pasture. Biotropica 33:260–267CrossRef
10. Dalling JW, Swaine MD, Garwood NC (1998) Dispersal patterns and seed bank dynamics of pioneer trees in moist tropical forest. Ecology 79:564–578CrossRef
11. de Souza Gomes Guarino E, Scariot A (2014) Direct seeding of dry forest tree species in abandoned pastures: effects of grass canopy and seed burial on germination. Ecol Res 29:473–482CrossRef
12. Dong M, de Kroon H (1994) Plasticity in morphology and biomass allocation in Cynodon dactylon, a grass species forming stolons and rhizomes. Oikos 70:99–106CrossRef
13. Esquivel MJ, Harvey CA, Finegan B, Casanoves F, Skarpe C (2008) Effects of pasture management on the natural regeneration of neotropical trees. J Appl Ecol 45:371–380CrossRef
14. García Córdova AA (2015) Relación de la conductividad hidráulica con otras propiedades del suelo en sitios en restauración y con bosque mesófilo de montaña conservado. Tesis de Licenciatura. Facultad de Ciencias Químicas. Universidad Veracruzana. Xalapa, Veracruz, p 68
15. Garcia-Orth X, Martínez-Ramos M (2007) Seed dynamics of early and late successional tree species in tropical abandoned pastures: seed burial as a way of evading predation. Restor Ecol 16:435–443CrossRef
16. Gardener CJ, McIvor JC, Jansen A (1993) Passage of legume and grass seeds through the digestive tract of cattle and their survival in faeces. J Appl Ecol 30(1):63–75CrossRef
17. Grau HR, Aide M (2008) Globalization and land-use transitions in Latin America. Ecol Soc 13:16
18. Griscom HP, Griscom BW, Ashton MS (2009) Forest regeneration from pasture in the dry tropics of Panama: effects of cattle, exotic grass, and forested riparia. Restor Ecol 17:117–126CrossRef
19. Gunaratne AMTA, Gunatilleke CVS, Gunatilleke IAUN, Weerasinghe HMSPM, Burslem DFRP (2010) Barriers to tree seedling emergence on human-induced grasslands in Sri Lanka. J Appl Ecol 47:157–165CrossRef
20. Gunaratne AMTA, Gunatilleke CVS, Gunatilleke IAUN, Madawala HMSP, Burslem DFRP (2014) Overcoming ecological barriers to tropical lower montane forest succession on anthropogenic grasslands: synthesis and future prospects. For Ecol Manag 329:340–350CrossRef
21. Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985CrossRef
22. Holl KD (1998) Effects of above- and below-ground competition of shrubs and grass on Calophyllum brasiliense(Camb.) seedling growth in abandoned tropical pasture. For Ecol Manag 109:187–195CrossRef
23. Holl KD (1999) Factors limiting tropical rain forest regeneration in abandoned pasture: seed rain, seed germination, microclimate, and soil. Biotropica 31:229–242CrossRef
24. Holl KD, Aide TM (2011) When and where to actively restore ecosystems? For Ecol Manag 261:1558–1563CrossRef
25. Holl KD, Loik ME, Lin EHV, Samuels IA (2000) Tropical montane forest restoration in Costa Rica: overcoming barriers to dispersal and establishment. Restor Ecol 8:339–349CrossRef
26. Hooper E, Condit R, Legendre P (2002) Responses of 20 native tree species to reforestation strategies for abandoned farmland in Panama. Ecol Appl 12:1626–1641CrossRef
27. Hooper E, Legendre P, Condit R (2005) Barriers to forest regeneration of deforested and abandoned land in Panama. J Appl Ecol 42:1165–1174CrossRef
28. Jacobs DF, Oliet JA, Aronson J, Bolte A, Bullock JM, Donoso PJ, Landhâusser SM, Madsen P, Peng S, Rey-Benayas JM, Weber JC (2015) Restoring forests: what constitutes success in the twenty-first century? New For 46:601–614CrossRef
29. Lemoine Rodríguez R (2012) Cambios en la cobertura vegetal de la ciudad de Xalapa-Enríquez, Veracruz y zonas circundantes entre 1950 y 2010. Tesis de Licenciatura. Facultad de Biología, Universidad Veracruzana. Xalapa, Veracruz, p 44
30. Lippok D, Walter F, Hensen I, Beck SG, Schleuning M (2013) Effects of disturbance and altitude on soil seed banks of tropical montane forests. J Trop Ecol 29:523–529CrossRef
31. Lopez-Toledo L, Martinez-Ramos M (2011) The soil seed bank in abandoned tropical pastures: source of regeneration or invasion? Rev Mex Biod 82:663–678
32. Maza-Villalobos S, Lemus-Herrera C, Martinez-Ramos M (2011) Successional trends in soil seed banks of abandoned pastures of a Neotropical dry region. J Trop Ecol 27:35–49CrossRef
33. Meli P, Rey-Benayas JM, Martinez-Ramos M, Carabias J (2015) Effects of grass clearing and soil tilling on establishment of planted tree seedlings in tropical riparian pastures. New For 46:9479CrossRef
34. Muñiz-Castro MA, Williams-Linera G, Benayas JMR (2006) Distance effect from cloud forest fragments on plant community structure in abandoned pastures in Veracruz, Mexico. J Trop Ecol 22:431–440CrossRef
35. Nepstad DC, Uhl C, Pereira CA, Cardoso da Silva JM (1996) A comparative study of tree establishment in abandoned pasture and mature forest of eastern Amazonia. OIKOS 76:25–39CrossRef
36. Ortega-Pieck A, López-Barrera F, Ramírez-Marcia N, García-Franco JG (2011) Early seedling establishment of two tropical montane cloud forest tree species: the role of native and exotic grasses. For Ecol Manag 261:1336–1343CrossRef
37. Pereira SR, Laura VA, Souza ALT (2013) Establishment of fabaceae tree species in a tropical pasture: influence of seed size and weeding methods. Restor Ecol 21:67–74CrossRef
38. Peterson CJ, Dosch JJ, Carson WP (2014) Pasture succession in the Neotropics: extending the nucleation hypothesis into a matrix discontinuity hypothesis. Oecologia 175:1325–1335CrossRefPubMed
39. Ramírez Marcial N, Gonzalez Espinosa M, Quintana Asencio PF (1992) Banco y lluvia de semillas en comunidades sucesionales de bosque de pino-emcino de Los Altos de Chiapas, Mexico. Acta Bot Mex 20:59–75
40. Rasiah V, Florentine SK, Williams BL, Westbrooke ME (2004) Soil properties dynamics under abandoned pasture in deforested tropical rainforest in Australia. Geoderma 120:35–45CrossRef
41. Reis A, Bechara FC, Tres DR (2010) Nucleation in tropical ecological restoration. Scientia Agricola 67:244–250CrossRef
42. Rey Benayas JM, Bullock JM, Newton AC (2008) Creating woodland islets: a new approach to reconcile ecological restoration, conservation, and agricultural land use. Front Ecol Environ 6:329–336CrossRef
43. Rey Benayas JM, Martínez-Baroja L, Pérez-Camacho L, Villar-Salvador P, Holl KD (2015) Predation and aridity slow down the spread of 21-year-old planted woodland islets in restored Mediterranean farmland. New For 46:841–853CrossRef
44. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Viena, Austria. http://​www.​R-project.​org/​
45. Rico-Gray V, García-Franco J (1992) Vegetation and soil seed bank of successional stages in tropical lowland deciduous forest. J Veg Sci 3:617–624CrossRef
46. Román-Dañobeytia FJ, Castellanos-Albores J, Levy-Tacher SI, Aronson J, Ramírez-Marcial N, Rodrigues RR (2012) Responses of 16 transplanted early-, mid-, and late-successional native tree species to invasive alien grass removals in an abandoned cattle pasture in the Lacandon region, Mexico. Trop Conserv Sci 5:192–207
47. Sobanski N, Marques MC (2014) Effects of soil characteristics and exotic grass cover on the forest restoration of the Atlantic Forest region. J Nat Conserv 22:217–222CrossRef
48. Standish RJ, Hobbs RJ, Miller JR (2013) Improving city life: options for ecological restoration in urban landscapes and how these might influence interactions between people and nature. Landsc Ecol 28:1213–1221CrossRef
49. Vinha D, Alves LF, Zaidan LBP, Grombone-Guaratini MT (2011) The potential of the soil seed bank for the regeneration of a tropical urban forest dominated by bamboo. Landsc Urban Plan 99:178–185CrossRef
50. Wijdeven SMJ, Kuzee ME (2000) Seed availability as a limiting factor in forest recovery processes in Costa Rica. Restor Ecol 8:414–424CrossRef
51. Williams-Linera G (1993) Soil seed banks in four lower montane forests of Mexico. J Trop Ecol 9:321–337CrossRef
52. Williams-Linera G (2002) Tree species richness complementarity, disturbance and fragmentation in a Mexican tropical montane cloud forest. Biodivers Conserv 11:1825–1843CrossRef
53. Williams-Linera G, Toledo-Garibaldi M, Gallardo-Hernández C (2013) How heterogeneous are the cloud forest communities in the mountains of central Veracruz, Mexico? Plant Ecol 214:685–701CrossRef
54. Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487CrossRef
55. Young KR, Ewel JJ, Brown BJ (1987) Seed dynamics during forest succession in Costa Rica. Vegetatio 71:157–173
56. Zimmerman J, Pascarella J, Aide M (2000) Barriers to forest regeneration in an abandoned pasture in Puerto Rico. Restor Ecol 8:350–360CrossRef

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