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Successional, spatial, and seasonal changes in seed rain in the Atlantic forest of southern Bahia, Brazil


Autoři: Daniel Piotto aff001;  Dylan Craven aff002;  Florencia Montagnini aff003;  Mark Ashton aff003;  Chadwick Oliver aff003;  William Wayt Thomas aff004
Působiště autorů: Centro de Formação em Ciências Agroflorestais, Universidade Federal do Sul da Bahia, Ilhéus, Bahia, Brazil aff001;  Biodiversity, Macroecology & Biogeography, University of Goettingen, Göttingen, Germany aff002;  School of Forestry and Environmental Studies, Yale University, New Haven, Connecticut, United States of America aff003;  The New York Botanical Garden, Bronx, New York, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226474

Souhrn

Seed arrival is a limiting factor for the regeneration of diverse tropical forests and may be an important mechanism that drives patterns of tree species’ distribution. Here we quantify spatial and seasonal variation in seed rain of secondary forests in southern Bahia, Brazil. We also examine whether secondary forest age enhances seed dispersal and whether seed rain density and diversity in secondary forests decay with distance from mature forest. Across a chronosequence of 15 pairs of mature and secondary forests, 105 seed traps were installed and monitored for one year. We tested the effects of secondary forest age, distance from mature forest, and seasonality on monthly seed rain density, diversity, seed dispersal mode, and diaspore size. We found that secondary forest age had strong, positive effects on the diversity of seed rain, which was generally higher during the wet season. Moreover, contrasting patterns among diversity indices revealed that seeds of rare species occurred more often in 40 yr old secondary forests and mature forests. While the proportion of biotically and abiotically dispersed seeds did not change significantly with distance from mature forest across all forest age classes, we found that biotically dispersed seeds contributed disproportionately more to seed rain diversity. Our results emphasize the importance of biotic dispersal to enhance diversity during secondary succession and suggest that changes in secondary forest structure have the potential to enhance the diversity of tropical secondary forests, principally by increasing dispersal of rare species.

Klíčová slova:

Forest ecology – Forests – Seasons – Seeds – Simpson index – Species diversity – Trees – Ecological succession


Zdroje

1. FAO. 2015. Global forest resources assessment 2015. Food and Agriculture Organization of the United Nations. Rome, Italy. 2015

2. Chazdon RL, Peres CA, Dent D, Sheil D, Lugo AE, Lamb D, et al. The potential for species conservation in tropical secondary forests. Conservation Biology. 2009; 23 (6): 1406–17. doi: 10.1111/j.1523-1739.2009.01338.x 20078641

3. Lugo AE. The emerging era of novel tropical forests. Biotropica. 2009; 41 (5): 589–91.

4. Lamb D. Restoration of degraded tropical forest landscapes. Science. 2005; 310 (5754): 1628–32. doi: 10.1126/science.1111773 16339437

5. Poorter L, Bongers F, et al. Biomass resilience of Neotropical secondary forests. Nature. 2016; 530 (7589): 211–14. doi: 10.1038/nature16512 26840632

6. Chazdon RL. Beyond deforestation: restoring forests and ecosystem services on degraded lands. Science. 2008; 320 (5882): 1458–60. doi: 10.1126/science.1155365 18556551

7. Reid JL, Holl KD. Arrival ≠ Survival. Restor Ecol. 2013; 21: 153–155.

8. Silva JMC, Tabarelli M. Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature. 2000; 404 (6773): 72–74. doi: 10.1038/35003563 10716443

9. Benitez-Malvido J, Kossmann-Ferraz ID. Litter cover variability affects seedling performance and herbivory. Biotropica. 1999; 31 (4), 598–606.

10. Wijdeven SMJ, Kuzee ME. Seed availability as a limiting factor in forest recovery processes in Costa Rica. Restoration Ecology. 2000; 8 (4): 414–24.

11. Ingle NR. Seed dispersal by wind, birds, and bats between Philippine montane rainforest and successional vegetation. Oecologia. 2003; 134 (2): 251–61. doi: 10.1007/s00442-002-1081-7 12647166

12. Martínez-Garza C, González-Montagut R. Seed rain from forest fragments into tropical pastures in Los Tuxtlas, Mexico. Plant Ecology. 1999; 145 (2): 255–65.

13. Uhl C, Clark K, Clark H, Murphy P. Early plant succession after cutting and burning in the upper Rio Negro region of the Amazon Basin. The Journal of Ecology. 1981; 69 (2): 631.

14. Reid JL, Holl KD, Zahawi R. Seed dispersal limitations shift over time in tropical forest restoration. Ecological Applications. 2015; 25 (4): 1072–82. doi: 10.1890/14-1399.1 26465043

15. Leps J, Rejmánek M. Convergence or divergence: what should we expect from vegetation succession?. Oikos. 1991; 62 (2):261.

16. Endress B, Chinea JD. Landscape Patterns of Tropical Forest Recovery in the Republic of Palau1. Biotropica. 2001; 33 (4): 555–65.

17. Thomlinson JR, Serrano SI, Lopez TM, Aide TM, Zimmerman JK. Land-use dynamics in a post-agricultural Puerto Rican landscape (1936–1988). Biotropica. 1996; 28 (4): 525.

18. Gunter S, Weber M, Erreis R, Aguirre N. Influence of distance to forest edges on natural regeneration of abandoned pastures: a case study in the tropical mountain rain forest of southern Ecuador. European Journal of Forest Research. 2006; 126 (1): 67–75.

19. Hooper ER, Legendre P, Condit R. Factors affecting community composition of forest regeneration in deforested abandoned land in Panama. Ecology. 2004; 85 (12): 3313–26.

20. Barnes AD, Chapman HM. Dispersal traits determine passive restoration trajectory of a Nigerian montane forest. Acta Oecologia. 2014; 56: 32–40.

21. Blackham GV, Andri T, Webb EL, Corlett RT. Seed rain into a degraded tropical peatland in Central Kalimantan, Indonesia. Biol. Conserv. 2013; 167, 215–223.

22. Teegalapalli K, Hiremath AJ, Jathanna D. Patterns of seed rain and seedling regeneration in abandoned agricultural clearings in a seasonally dry tropical forest in India. Journal of Tropical Ecology. 2010; 26:25–33.

23. Nepstad DC, Uhl C, Pereira CA, Silva JMC, Silva JMC. A comparative study of tree establishment in abandoned pasture and mature forest of Eastern Amazonia. Oikos. 1996; 76 (1): 25.

24. Janzen DH. Management of habitat fragments in a tropical dry forest: growth. Annals of the Missouri Botanical Garden. 1988; 75 (1): 105.

25. McClanahan TR. The Effect of a seed source on primary succession in a forest ecosystem. Vegetatio. 1986; 65 (3): 175–78.

26. Guevara S, Purata SE, Van der Maarl. The role of remnant forest trees in tropical secondary succession. Vegetatio. 1986; 66, 77–84.

27. Holl KD. Factors limiting tropical rain forest regeneration in abandoned pasture: seed rain, seed germination, microclimate, and soil. Biotropica. 1999; 31 (2): 229–42.

28. Willson MF, Crome HJ. Patterns of seed rain at the edge of a tropical Queensland rain forest. Journal of Tropical Ecology. 1989; 5 (03): 301–8.

29. van Breugel, Hall JS, Craven D, Bailon M, Hernandez A, Abbene M, Van Breugel P. Succession of ephemeral secondary forests and their limited role for the conservation of floristic diversity in a human-modified tropical landscape. PLoS ONE. 2013; 8(12), e82433. doi: 10.1371/journal.pone.0082433 24349283

30. Lohbeck ML, Poorter L, Lebrija-Trejos E, Martínez-Ramos M, et al. Successional changes in functional composition contrast for dry and wet tropical forest. Ecology. 2013; 94(6), 1211–6. doi: 10.1890/12-1850.1 23923479

31. Bazzaz FA. The physiological ecology of plant succession. Annual Review of Ecology and Systematics. 1979; 10, 351–371.

32. Ewel J. Tropical succession: manifold routes to maturity. Biotropica. 1980; 12(2), 2–7.

33. Pearse IS, Lamontagne JM, Koenig WD. Inter-annual variation in seed production has increased over time (1900–2014). Proc. R. Soc. B. 2017; 284: 1666.

34. Foster RB. 1985. The seasonal rhythm of fruitfall on Barro Colorado Island. in Leigh E. G., Rand A. S. & Windsor D. M. (eds). The ecology of a tropical forest. Smithsonian Institution Press, Washington, DC. 1985; pp. 151–172.

35. Marques MCM, Oliveira PEAM. Seasonal rhythms of seed rain and seedling emergence in two tropical rain forests in southern Brazil. Plant Biology. 2008; 10 (5): 596–603. doi: 10.1111/j.1438-8677.2008.00061.x 18761498

36. Melo FPL, Dirzo R, Tabarelli M. Biased seed rain in forest edges: evidence from the Brazilian Atlantic Forest. Biological Conservation. 2006; 132 (1): 50–60.

37. Grombone-Guaratini MT, Rodrigues RR. Seed bank and seed rain in a seasonal semi-deciduous forest in South-Eastern Brazil. Journal of Tropical Ecology. 2002; 18 (05): 759–74.

38. Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparro VB. Phenology of Atlantic Rain Forest trees: a comparative study. Biotropica. 2000; 32 (4b): 811–23.

39. Thomas WW, Carvalho AMV, Amorim AM, Hanks JG, Santos TS. Diversity of woody plants in the Atlantic coastal forest of southern Bahia. Mem N Y Bot Gard. 2008; 100, 21–66

40. Whitmore TC, Prance GT. Biogeography and quaternary history in tropical America. Oxford Monographs on Biogeography, 8. 1987.

41. De la Peña-Domene M, Howe HF, Cruz-Leon E, Jiménez-Rolland R, Lozano-Huerta C, Martínez-Garça C. Seed to seedling transitions in successional habitats across a tropical landscape. Oikos. 2016, 126 (3): 410–19.

42. O’Brien MJ, Perez-Aviles D, Powers JS. Resilience of seed production to a severe El Niño‐induced drought across functional groups and dispersal types. Glob. Chang. Biol. 2018; 24(11):5270–5280 doi: 10.1111/gcb.14416 30080318

43. Landau EC. Normais de precipitação no sudeste da Bahia, Brasil. In: Prado PI, Landau EC, Moura RT, Pinto LPS, Fonseca GAB, Alger K (eds) Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia. Publicação em CD-ROM, Ilhéus, IESB/CI/CABS/UFMG/UNICAMP, Ilhéus. 2003.

44. Thomas WW, Barbosa MRV. Natural vegetation types in the Brazilian Atlantic coastal forest north of the Rio Doce. Mem N Y Bot Gard. 2008; 100, 6–20

45. Santana SO, Santos RD, Lopes IA, Jesus RM, et al. Solos da região sudeste da Bahia: atualização da legenda de acordo com o sistema brasileiro de classificação de solos. CEPLAC/EMBRAPA, Rio de Janeiro. 2002.

46. Cornejo F, Janove J. Seeds of Amazonian plants. Walter de Gruyter GmbH. 2010.

47. Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. vols. 1 and 2. Editora Plantarum, Nova Odessa. 1998.

48. Tabarelli M, Peres CA. Abiotic and vertebrate seed dispersal in the Brazilian Atlantic Forest: implications for forest regeneration. Biological Conservation. 2002; 106 (2): 165–76.

49. Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs. 2014; 84(1), 45–67.

50. Jost L. Entropy and diversity. Oikos. 2006; 113 (2): 363–75.

51. Chao A, Jost L. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology. 2012; 93 (12): 2533–47. 23431585

52. Chao A, Chiu CH, Jost L. Statistical challenges of evaluating diversity patterns across environmental gradients in mega-diverse communities. Journal of Vegetation Science. 2016; 27 (3): 437–38.

53. Hsieh TC, Ma KH, Chao A. INEXT: an R package for rarefaction and extrapolation of species diversity (Hill Numbers). Methods in Ecology and Evolution. 2016; 7 (12): 1451–56.

54. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2018.

55. Harrison XA. Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ. 2014; doi: 10.7717/peerj.616 25320683

56. Bates D, Maechler DM, Bolker B, Walker S, et al. lme4: linear mixed-effects models using Eigen and S4. 2014; R Package Version 1 (7).

57. Piotto D, Montagnini F, Thomas W, Ashton M, Oliver C. Forest recovery after swidden cultivation across a 40-year chronosequence in the Atlantic forest of southern Bahia, Brazil. Plant Ecol. 2009; 205: 261.

58. Martini AMZ, Santos FAM. Effects of distinct types of disturbance on seed rain in the Atlantic Forest of NE Brazil. Plant Ecology. 2006; 190 (1): 81–95.

59. Ganade G. Forest restoration in abandoned pastures of Central Amazonia. In: Bierregaard RO, Gascon C, Lovejoy TE, Mesquita RCG (eds). Lessons from Amazonia. The ecology and conservation of a fragmented forest. Yale University Press, New Haven. 2001; pp 313–324.

60. Young KR, Ewel JJ, Brown BJ. Seed dynamics during forest succession in Costa Rica. Vegetatio. 1987; 71, 157–173.

61. Opler PA, Baker HG, Frankie GW. Plant reproductive characteristics during secondary succession in Neotropical lowland forest ecosystems. Biotropica. 1980; 12 (2): 40.

62. Silva FRD, Montoya D, Furtado R, Memmott MA, Pizzo MA, Rodrigues RR. The restoration of tropical seed dispersal networks. Restoration Ecology. 2015; 23(6), 852–860.

63. Pascarella JB, Aide TM, Serrano MI, Zimmerman JK. Land-use history and forest regeneration in the Cayey Mountains Puerto Rico. Ecosystems. 2000; 3 (3): 217–28.

64. Wunderle JM. The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. Forest Ecology and Management. 1997; 99 (1–2): 223–35.

65. Dent DH, Dewalt SJ, Denslow JS, Cáceres M. Secondary forests of central Panama increase in similarity to old-growth forest over time in shade tolerance but not species composition. Journal of Vegetation Science. 2013; 24(3), 530–542.

66. Purata SE. Floristic and structural changes during old-field succession in the Mexican tropics in relation to site history and species availability. Journal of Tropical Ecology. 1986; 2 (03): 257–76.

67. Guevara S, Laborde J. Monitoring seed dispersal at isolated standing trees in tropical pastures: consequences for local species availability. Vegetatio. 1993; 107/108, 319–338.

68. Hooper ER, Legendre P, Condit R. Barriers to forest regeneration of deforested and abandoned land in Panama. Journal of Applied Ecology. 2005; 42(6), 1165–1174.

69. Gorchov DL, 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. 1993; 107/108, 339–349.

70. Powell L, Stouffer LP, Johnson E. Recovery of understory bird movement across the interface of primary and secondary Amazon rainforest. The Auk. 2013; 130(3), 459–468.

71. Lowe WH, McPeek MA. Is dispersal neutral? Trends in Ecology and Evolution. 2014; 29, 444–450. doi: 10.1016/j.tree.2014.05.009 24962790

72. Kelly D, Sork DL. Mast seeding in perennial plants: why, how, where? Annual Review of Ecology and Systematics. 2002; 33(1):427–447.

73. Garwood NC. 1983. Seed germination in a seasonal tropical forest in Panama: a community study. Ecological Monographs 53 (2): 159–81.


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