Long-lasting effects of unplanned logging on the seed rain of mixed conifer-hardwood forests in southern South America

Abstract

Understanding the effects of disturbance on seed rain is critical to predict changes in forest species composition and diversity. Logging effects on seed rain in a mixed conifer-hardwood forest complex in southern Brazil were evaluated. One year of seed rain data were collected from a large-scale observational experiment in logged and protected forests and quantity and average seed size weighted by species abundance (CWM) were compared between old-growth and logged stands 55 years after logging activities. Using these data, variations in frequency of functional groups of species in the seed rain were examined to see if they could be attributed to logging. Results show that the number of seeds per trap was highly right-skewed, ranging from 13 to 12,788 seeds per trap in one year. Seed rain was affected by logging history, with seed traps in old-growth plots receiving significantly less seeds than traps in logged plots. All species included mean seed size weighted by species abundance were significantly smaller in logged than in old-growth forests. This difference persisted after the exclusion of Araucaria angustifolia, a large-seeded pioneer which was intensively logged, although the difference of seed size between the two forest classes was greatly reduced. Species abundance in the seed rain differed significantly from the established tree community, between logged and old-growth stands. The composition of the seed rain was much more variable than the composition of the established tree community and its points more scattered over the ordination space than the points corresponding to the protected forests. The number of collected seeds across different functional groups of species significantly differed between logged and old-growth plots. The seed rain of logged forests reflects their arrested succession as indicated by reduced abundance of functional groups such as pioneers, large seeded pioneers and Araucaria, as well as reduced functional diversity. Seed rain differences between logged and old- growth stands reflect the intensive logging of A. angustifolia.

Keywords

Arrested succession / Brazil / Logging / Long-lived pioneers / Seed rain

References

[1] Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift, 2013, 22: 711-728.

[2] Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol, 2001, 26: 32-46.

[3] Araujo M, Chami L, Longhi S, Avila AL, Brena DA. Análise de agrupamento em remanescente de Floresta Ombrófila Mista. Ciência Florest, 2010, 20: 1-18.

[4] Avila A, Araujo M, Gasparin E, Longhi S. Mecanismos de regeneração natural em remanescente de Floresta Ombrófila Mista, RS, Brasil. Cerne, 2013, 19: 621-628.

[5] Avila AL, Ruschel AR, Carvalho JOP, Mazzei L, Silva JNM, Lopes JC, Araujo MM, Dormann CF, Bauhus J. Medium-term dynamics of tree species composition in response to silvicultural intervention intensities in a tropical rain forest. Biol Conserv, 2015, 191: 577-586.

[6] Backes P, Irgang B. Árvores do sul: guia de identificação e reconhecimento, 2002 ecológico Porto Alegre: Pallotti.

[7] Bleher B, Böhning-Gaese K. Consequences of frugivore diversity for seed dispersal, seedling establishment and the spatial pattern of seedlings and trees. Oecologia, 2001, 129: 385-394.

[8] Both S, Riutta T, Paine CET, Elias DMO, Cruz RS, Jain A, Johnson D, Kritzler UH, Kuntz M, Majalap-Lee N, Mielke N, Pilco MXM, Ostle NJ, The YA, Malhi Y, Burslem DRFP. Logging and soil nutrients independently explain plant trait expression in tropical forests. New Phytol, 2019, 221: 1853-1865.

[9] Cabral DC, Cesco S. Notas para uma história da exploração madeireira na Mata Atlântica do sul-sudeste. Ambient Soc, 2008, XI: 33-48.

[10] Cademartori CV, Fabián ME, Menegheti JO. Variações na abundância de roedores (Rodentia, Sigmodontinae) em duas áreas de floresta ombrófila mista, Rio Grande do Sul, Brasil. Rev Bras Zoociências, 2004, 6: 147-167.

[11] Capellesso ES, Scrovonski KL, Zanin EM, Sausen TL. Relação entre chuva de sementes e estrutura florestal em remanescentes de Floresta Atlântica no Sul do Brasil. Iheringia-Ser Bot, 2018, 73: 176-181.

[12] Chami LB, Araujo MM, Longhi SJ, Kielse P, Lucio ADC. Mecanismos de regeneração natural em diferentes ambientes de remanescente de Floresta Ombrófila Mista, São Francisco de Paula, RS. Ciência Rural, 2011, 41: 251-259.

[13] Chazdon RL. Tropical forest recovery: legacies of human impact and natural disturbances. Perspect Plant Ecol Evol Syst, 2003, 6: 51-71.

[14] Coomes DA, Grubb PJ. Colonization, tolerance, competition and seed-size variation within functional groups. Trends Ecol Evol, 2003, 18: 283-291.

[15] De Avila AL, Araujo MM, Longhi SJ, Gasparin E. Agrupamentos florísticos na regeneração natural em remanescente de Floresta Ombrófila Mista, RS, Brasil. Sci For, 2011, 39: 331-342.

[16] De Cáceres M, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology, 2009, 90: 3566-3574.

[17] Dos Santos MFB, Cademartori CV. Composição e abundância da avifauna em quatro fitofisionomias de área rural pertencente ao domínio da Mata Atlântica no sul do Brasil. Ciência Florest, 2015, 25: 351-361.

[18] Edwards DP, Tobias JA, Sheil D, Meijaard E, Laurance WF. Maintaining ecosystem function and services in logged tropical forests. Trends Ecol Evol, 2014, 29: 511-520.

[19] Estrada A, Coates-Estrada R. Fruit eating and seed dispersal by howling monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxtlas, Veracruz, Mexico. Am J Primatol, 1984, 6: 77-91.

[20] Fialho M (2007) Riqueza e abundância da fauna de médio e grande porte em três modelos de áreas protegidas no sul do Brasil. Universidade Estadual de Campinas

[21] Fonseca CR, Ganade G, Baldissera R, Becker CG, Boelter CR, Brescovit AD, Campos LM, Fleck T, Fonseca VS, Hartz SM, Joner F, Kaffer MI, Leal-Zanchet AM, Marcelli MP, Mesquita AS, Mondin CA, Paz CP, Petry MV, Piovensan FN, Putzke J, Stranz A, Vergara M, Vieira EM. Towards an ecologically-sustainable forestry in the Atlantic Forest. Biol Conserv, 2009, 142: 1209-1219.

[22] Forgiarini C, Souza AF, Longhi SJ, Oliveira JM. In the lack of extreme pioneers: trait relationships and ecological strategies of 66 subtropical tree species. J Plant Ecol, 2015, 8: 359-367.

[23] Garreaud RD, Vuille M, Compagnucci R, Marengo J. Present-day South American climate. Palaeogeogr Palaeoclimatol Palaeoecol, 2009, 281: 180-195.

[24] Gasparin E, Faria JMR, José AC, Tonetti OAO, Melo RA, Hilhorst HWM. Viability of recalcitrant Araucaria angustifolia seeds in storage and in a soil seed bank. J For Res, 2019 in Press

[25] Gerwing J. Degradation of forests through logging and fire in the eastern Brazilian Amazon. For Ecol Manage, 2002, 157: 131-141.

[26] Gonçalves E, Souza A. Floristic variation in ecotonal areas: patterns, determinants and biogeographic origins of subtropical forests in South America. Austral Ecol, 2014, 39: 122-134.

[27] Gourlet-Fleury S, Mortier F, Fayolle A, Fayolle A, Baya F, Ouédraogo D, Bénédet F, Picard N. Tropical forest recovery from logging: a 24 year silvicultural experiment from Central Africa. Philos Trans R Soc B Biol Sci, 2013, 368: 20120302.

[28] Gutiérrez-Granados G. Effect of logging on rodent scatter-hoarding dynamics in tropical forests: implications for plant recruitment. Integr Zool, 2011, 6: 74-80.

[29] Hardesty BD, Parker VT. Community seed rain patterns and a comparison to adult community structure in a West African tropical forest. Plant Ecol, 2003, 164: 49-64.

[30] Harms KE, Wrght SJ, Calderón O, Hernández A, Herre EA. Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature, 2000, 404: 493-495.

[31] Heilbuth JC, Ilves KL, Otto SP. The consequences of dioecy for seed dispersal: modeling the seed-shadow handicap. Evolution, 2007, 55: 880-888.

[32] Iob G, Vieira EM. Seed predation of Araucaria angustifolia (Araucariaceae) in the Brazilian Araucaria Forest: influence of deposition site and comparative role of small and ‘large’ mammals. Plant Ecol, 2008, 198: 185-196.

[33] Jackson JF. Seed size as a correlate of temporal and spatial patterns of seed fall in a neotropical forest. Biotropica, 1981, 13: 121-130.

[34] Jansen PA, Hirsch BT, Emsens WJ, Zamora-Gutierrez V, Wikelski M, Kays R. Thieving rodents as substitute dispersers of megafaunal seeds. Proc Natl Acad Sci, 2012, 109: 12610-12615.

[35] Jones FA, Muller-Landau HC. Measuring long-distance seed dispersal in complex natural environments: an evaluation and integration of classical and genetic methods. J Ecol, 2008, 96: 642-652.

[36] Jordano P, Schupp EW. Seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecol Monogr, 2000, 70: 591-615.

[37] Klein RM. O aspecto dinâmico do pinheiro brasileiro. Sellowia, 1960, 12: 17-51.

[38] Laliberté E, Legendre P. A distance-based framework for measuring functional diversity from multiple traits. Ecology, 2010, 91: 299-305.

[39] Lavorel S, Grigulis K, McIntyre S, Williams NSG, Garden D, Dorrough J, Berman S, Quetier F, Thebault A, Bonis A. Assessing functional diversity in the field-methodology matters!. Funct Ecol, 2008, 22(1): 134-147.

[40] Lindenmayer DB, Laurance WF. The ecology, distribution, conservation and management of large old trees. Biol Rev, 2017, 92: 1434-1458.

[41] Lohbeck M, Poorter L, Martínez-Ramos M, Rodriguez-Velázquez J, van Breugel M, Bongers F. Changing drivers of species dominance during tropical forest succession. Funct Ecol, 2014, 28: 1052-1058.

[42] Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil, 1992, Nova Odessa: Plantarum.

[43] Mantovani A, Morellato LPC, Reis MS. Fenologia reprodutiva e produção de sementes em Araucaria angustifolia (Bert.) O. Kuntze Rev Bras Botânica, 2004, 27: 787-796.

[44] Marchiori JNC, Sobral M. Dendrologia das angiospermas, 1997 Myrtales Santa Maria: da UFSM.

[45] Marini MÂ, Barbet-Massin M, Martinez J, Prestes NP, Jiguet F. Applying ecological niche modelling to plan conservation actions for the Red-spectacled Amazon (Amazona pretrei). Biol Conserv, 2010, 143: 102-112.

[46] McConkey KR. Primary seed shadow generated by gibbons in the rain forests of Barito Ulu, central Borneo. Am J Primatol, 2000, 52: 13-29.

[47] McCune B, Grace JB. Analysis of ecological communities, 2002, Gleneden Beach: MJM Software.

[48] Medjibe VP, Putz FE, Romero C. Certified and uncertified logging concessions compared in gabon: changes in stand structure, tree species, and biomass. Environ Manage, 2013, 51: 524-540.

[49] Muller-Landau HC, Wright SJ, Calderón O, Condit R, Hubbell SP. Interspecific variation in primary seed dispersal in a tropical forest. J Ecol, 2008, 96: 653-667.

[50] Muscolo A, Bagnato S, Sidari M, Mercurio R. A review of the roles of forest canopy gaps. J For Res, 2014, 25: 725-736.

[51] Nathan R, Muller-Landau HC. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol, 2000, 15: 278-284.

[52] Nuñez CL, Clark JS, Clark CJ, Poulsen JR (2019) Low-intensity logging and hunting have long-term effects on seed dispersal but not fecundity in Afrotropical forests. AoB Plants 11(1). https://doi.org/10.1093/aobpla/ply074

[53] Osuri AM, Sankaran M. Seed size predicts community composition and carbon storage potential of tree communities in rain forest fragments in India’s Western Ghats. J Appl Ecol, 2016, 53: 837-845.

[54] Paise G, Vieira EM. Produção de frutos e distribuição espacial de angiospermas com frutos zoocóricos em uma Floresta Ombrófila Mista no Rio Grande do Sul, Brasil. Rev Bras Botânica, 2005, 28: 615-625.

[55] Peres CA, Thaise E, Schietti J, Desmoulieres SJM, Levi T. Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proc Natl Acad Sci USA, 2015, 113: 892-897.

[56] Poulsen JR, Clark CJ, Palmer TM. Ecological erosion of an Afrotropical forest and potential consequences for tree recruitment and forest biomass. Biol Conserv, 2013, 163: 122-130.

[57] Pyles MV, Prado-Junior JA, Magnago LFS, de Paula A, Meira-Neto JAA. Loss of biodiversity and shifts in aboveground biomass drivers in tropical rainforests with different disturbance histories. Biodivers Conserv, 2018, 27: 3215-3231.

[58] R-Core-Team. R: A language and environment for statistical computing. Version, 2017 3 4 3

[59] Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM. The Brazilian atlantic forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv, 2009, 142: 1141-1153.

[60] Schupp EW, Jordano P, Gómez JM. Seed dispersal effectiveness revisited: a conceptual review. New Phytol, 2010, 188: 333-353.

[61] Silva Matos DM, Watkinson AR. The fecundity, seed, and seedling ecology of the edible palm Euterpe edulis in southeastern Brazil. Biotropica, 1998, 30: 595-603.

[62] Sist P, Nguyen-Thé N. Logging damage and the subsequent dynamics of a dipterocarp forest in East Kalimantan (1990–1996). For Ecol Manage, 2002, 165: 85-103.

[63] Souza AF, Forgiarini C, Longhi SJ, Oliveira JM. Detecting ecological groups from traits: a classification of subtropical tree species based on ecological strategies. Brazilian J Bot, 2014, 37: 441-452.

[64] Souza AF. Ecological interpretation of multiple population size structures in trees: The case of Araucaria angustifolia in South America. Austral Ecol, 2007, 32: 524-533.

[65] Souza AF. Conifer demography in forest-grassland mosaics: a landscape-scale study over a 24-year period. Botany, 2017, 95: 717-729.

[66] Souza AF, Cortez LSR, Longhi SJ. Native forest management in subtropical South America: long-term effects of logging and multiple-use on forest structure and diversity. Biodivers Conserv, 2012, 21: 1953-1969.

[67] Souza AF, Forgiarini C, Longhi SJ, Brena DA. Regeneration patterns of a long-lived dominant conifer and the effects of logging in southern South America. Acta Oecologica, 2008, 34: 221-232.

[68] Souza AF, Longhi SJ (2019) Disturbance history mediates climate change effects on subtropical forest biomass and dynamics. Ecol Evol 00:ece3.5289-ece3.5289. https://doi.org/10.1002/ece3.5289

[69] Ter Steege H, Welch I, Zagt R. Long-term effect of timber harvesting in the Bartica Triangle, Central Guyana. For Ecol Manage, 2002, 170: 127-144.

[70] Terborgh J, Zhu K, Loayza PA, Valverde FC. Seed limitation in an Amazonian floodplain forest. Ecology, 2019, 100: e02642.

[71] Thomson FJ, Moles AT, Auld TD, Kingsford RT. Seed dispersal distance is more strongly correlated with plant height than with seed mass. J Ecol, 2011, 99: 1299-1307.

[72] Vieira EM, Iob G Fonseca CR, Souza AF, Leal-Zanchet AM Dispersão e predação de sementes de Araucaria angustifolia. Floresta com Araucária: Ecologia, Conservação e Desenvolvimento Sustentável, 2009, Ribeirão Preto: Holos 85 96

[73] Wright SJ, Calderón O, Hernandéz A, Detto M, Jansen PA. Interspecific associations in seed arrival and seedling recruitment in a Neotropical forest. Ecology, 2016, 97: 2780-2790.

[74] Yan J. geepack: yet another package for Generalized Estimating Equations. R News, 2002, 2(3): 12-14.

[75] Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R, 2009, New York: Springer