Instituto de Geociências
FRANCISCO HERNAN SANTIAGO RIOS
ESTUDOS TAFONÔMICOS DE FOLHAS DE ANGIOSPERMAS NO
ESTADO DE SÃO PAULO, BRASIL, E A ANÁLISE DA MARGEM FOLIAR
PARA AMÉRICA DO SUL. IMPLICAÇÕES PALEOBOTÂNICAS.
CAMPINAS 2017
FRANCISCO HERNAN SANTIAGO RIOS
ESTUDOS TAFONÔMICOS DE FOLHAS DE ANGIOSPERMAS NO
ESTADO DE SÃO PAULO, BRASIL, E A ANÁLISE DA MARGEM FOLIAR
PARA AMÉRICA DO SUL. IMPLICAÇÕES PALEOBOTÂNICAS.
TESE APRESENTADA AO INSTITUTO DE
GEOCIÊNCIAS DA UNIVERSIDADE ESTADUAL DE CAMPINAS PARA OBTENÇÃO DO TÍTULO DE DOUTOR EM CIÊNCIAS NA ÁREA DE GEOLOGIA E RECURSOS NATURAIS
ORIENTADORA: PROF.(a) FRÉSIA SOLEDAD RICARDI TORRES BRANCO
ESTE EXEMPLAR CORRESPONDE À VERSÃO FINAL DA TESE DEFENDIDA PELO ALUNO FRANCISCO HERNAN SANTIAGO RIOS E ORIENTADA PELA PROFA. DRA. FRESIA SOLEDAD RICARDI TORRES BRANCO
CAMPINAS 2017
Ficha catalográfica
Universidade Estadual de Campinas Biblioteca do Instituto de Geociências Cássia Raquel da Silva - CRB 8/5752
Santiago Rios, Francisco Hernan,
Sa59e SanEstudos tafonômicos de folhas de angiospermas no estado de São Paulo,
Brasil, e a análise da margem foliar para América do Sul. Implicaçôes paleobotânicas. / Francisco Hernan Santiago Rios. – Campinas, SP : [s.n.], 2017.
SanOrientador: Fresia Soledad Ricardi Torres Branco.
SanTese (doutorado) – Universidade Estadual de Campinas, Instituto de
Geociências.
San1. Paleobotânica. 2. Serapilheira. 3. Macro-restos de vegetais. 4.
Angiosperma. 5. Análise foliar. I. Ricardi-Branco, Fresia,1963-. II. Universidade Estadual de Campinas. Instituto de Geociências. III. Título.
Informações para Biblioteca Digital
Título em outro idioma: Tafonomic studies of angiosperms leaves in São Paulo State,
Brazil, and the leaf margin analysis for South America. Paleobotanical implications.
Palavras-chave em inglês: Paleobotany Plant litter Plant macroremains Angiosperm Leaf analysis
Área de concentração: Geologia e Recursos Naturais Titulação: Doutor em Ciências
Banca examinadora:
Fresia Soledad Ricardi Torres Branco [Orientador] Luiz Carlos Ruiz Pessenda
Fernando Roberto Martins Alessandro Batezelli Rafael Souza de Faria
Data de defesa: 22-08-2017
Programa de Pós-Graduação: Geociências
UNIVERSIDADE ESTADUAL DE CAMPINAS INSTITUTO DE GEOCIÊNCIAS
AUTOR: Francisco Hernan Santiago Rios
Estudos Tafonômicos de Folhas de Angiospermas no Estado de São Paulo, Brasil, e a Análise da Margem Foliar para América do Sul.
ORIENTADORA: Profa. Dra. Fresia Soledad Ricardi Torres Branco
Aprovado em: 22 / 08 / 2017
EXAMINADORES:
Profa. Dra. Fresia Soledad Ricardi Torres Branco - Presidente
Prof. Dr. Luiz Carlos Ruiz Pessenda
Prof. Dr. Fernando Roberto Martins
Prof. Dr. Alessandro Batezelli
Prof. Dr. Rafael Souza de Faria
A Ata de Defesa assinada pelos membros da Comissão Examinadora, consta no processo de vida acadêmica do aluno.
À memória de minhas tias,
Marilyn del Valle e Maria de la Trinidad, as quais partiram ao longo desde doutorado.
AGRADECIMENTOS
Durante o doutorado muitas pessoas contribuíram de uma forma ou de outra, para o desenvolvimento deste trabalho e minha formação, para todas elas meus sinceros agradecimentos. Em especial agradeço:
A minha orientadora, profa. Dra. Fresia Ricardi-Branco, por ter me recebido em seu laboratório, pelo apoio, incentivo e por ter sempre confiado em meu potencial. Sua conduta como orientadora, professional e amiga serão eternos exemplos para mim.
A família de minha orientadora, seu esposo, Geólogo Fabio Branco, e seu filho, Rafael, pela amizade, seu incentivo e apoio em algumas etapas deste trabalho.
À profa. Dra. Sueli Yoshinaga Pereira e seu esposo o Dr. Paulo Ricado Brum Pereira, pela amizade, seu incentivo e pelo grande apoio logístico.
Ao Instituto Florestal, Secretária do Meio ambiente, Governo do Estado de São Paulo, e a Fundação José Pedro de Oliveira-A.R.I.E. Mata de Santa Genebra e, pelas autorizações e apoio concedidos para a realização deste trabalho.
Ao pessoal das Unidades de Conservação do estado de São Paulo visitadas durante a realização deste trabalho, em especial ao da Estação Ecológica de Mogi Guaçu, pela ajuda prestada na coleta de amostras.
A Gustavo e Ana pela ajuda prestada durante o processamento do material botânico.
Ao Prof. Me. Jorge Tamashiro, Instituto de Biologia, Universidade Estadual de Campinas, pela ajuda prestada na identificação do material botânico.
Ao prof. Dr. Luiz C. Pessenda, Laboratório de 14C, Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, pela ajuda prestada no processamentodas amostras coletadas para datação por carbono-14.
Ao prof. Dr. Giorgio Basilicipela amizade e incentivo.
Aos funcionários do Instituto de Geociências (IG), em especial aos do Laboratório de Paleohidrogeologia, Cristiano, Seção de Infraestrutura Operacional e Manutenção, Elcio e Edinalva, Biblioteca "Conrado Paschoale", Claudineia, e Tecnologia de Informação e Comunicação, Moacir, por toda sua ajuda e disponibilidade.
A meus colegas de laboratório Melina, Isabel, Daniele, Adriana e Isadora pelos bons momentos de companheirismo e amizade.
A Isabela, Amanda, Flavia, Rafael, Ariel e Bia por toda a ajuda, amizade e conselhos.
A Aurora, Tabata e Emanuel por todo o apoio, pelos grandes momentos de amizade e mais variados possíveis que compartilhamos.
A meus amigos de longe Gloria, Renny, Gwendolyn, Maryelli, Auris, Yulia, Maria Auxiliadora e Isabelle pelo apoio, incentivo e torcida.
A minha mãe, Marilú, meus avós, Hernan e Florencia, minhas tias, Marilyn (†), Mariela, e Marisela, e meus primos, José Francisco e Sigifredo José, pelo suporte e compreensão apesar da distância.
A minha namorada, Andrea, pelo amor e companheirismo essenciais em todas as etapas do meu trabalho e da minha vida.
À Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) pela bolsa concedida, á Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; processos 2010/20379-6 e 2013/22729-2) e ao Fundo de Apoio ao Ensino, à Pesquisa e Extensão (FAEPEX) pelo apoio financeiro que possibilitou o desenvolvimento deste trabalho e minha participação em congressos.
“The most erroneous stories are those we think we know best - and therefore never scrutinize or question” (Stephen Jay Gould)
Neotropical (2009–2013) pela Universidad de Los Andes, Venezuela. Desenvolve atividades na área de paleontologia, com ênfase em paleobotânica, na área de reconstruções paleoclimáticas e paleoecológicas, e análise tafonômica.
RESUMO
ESTUDOS TAFONÔMICOS DE FOLHAS DE ANGIOSPERMAS NO ESTADO DE SÃO PAULO, BRASIL, E A ANÁLISE DA MARGEM FOLIAR PARA AMÉRICA DO SUL. IMPLICAÇÕES PALEOBOTÂNICAS.
Neste estudo se analisou a composição taxonômica e as características fisionômicas do material foliar de sete amostras de serapilheira da floresta ripária da Estação Ecológica de Mogi Guaçu, Nordeste do estado de São Paulo, assim como de cinco acumulações de macro-restos vegetais que se encontram ao longo de rios meandrantes do Nordeste, Leste e litoral Sul do estado de São Paulo, com a finalidade de se obter novas pautas para a análise e interpretação das associações fósseis de angiospermas. Também se analisou a relação entre a proporção de espécies sem dentes de uma flora e a temperatura média anual (TMA) de um conjunto de 121 localidades da América do Sul, com o objetivo de se obter uma nova equação baseada na Análise da Margem Foliar para a região. Ao analisar o material foliar das amostras de serapilheira observamos que a relação entre o número de espécies e de folhas/folíolos, assim como a composição florística, depende da localidade, do habitat e da dispersão produzida pelo vento. Deste material foliar 60–95% pertence a 2–3 espécies arbóreas. A maior parte das espécies identificadas pertence às famílias Bignoniaceae, Euphorbiaceae, Fabaceae, Myrtaceae e Sapindaceae. Das espécies identificadas 55–70% são arbóreas e o 20–40% restante são trepadeiras, as quais representam 8–35% da riqueza total de espécies arbóreas e 5–32% da riqueza total de espécies de trepadeiras da área. As principais características fisionômicas do material foliar nos permitiram estimar a TMA e a precipitação média anual (PMA). Os valores da TMA obtidos subestimaram o valor real em 0.8–1.8 °C e o superestimaram em 1.5–4.8 °C, e os valores da PMA obtidos subestimaram o valor real em 11–188 mm e o superestimaram em 44–83 mm. As acumulações de macro-restos vegetais estudadas podem ser consideradas um registro de alta resolução de El Niño. O material foliar que está presente nestas acumulações depende da localidade, do habitat, e do transporte produzido pelo vento e pela água. Deste material foliar 70–85% pertence a 2–3 espécies arbóreas. A maior parte das espécies identificadas pertence às famílias Bignoniaceae, Fabaceae e Sapindaceae. Das espécies identificadas 70% são arbóreas e o 30% restante são trepadeiras, as quais representam 25– 35% da riqueza total de espécies arbóreas e 23–32% da riqueza total de espécies de trepadeiras da área. As principais características fisionômicas deste material foliar permitiram estimar a TMA e a PMA para o momento de sua deposição. Os valores da TMA obtidos subestimaram o valor real em 0.5–1.3 °C e o superestimaram em 2.2 °C, e os valores da PMA obtidos subestimaram o valor real em 332–1070 mm. A análise da relação entre a proporção de espécies sem dentes e a TMA de um conjunto de 121 localidades da América do Sul nos permitiu gerar uma nova equação de regressão linear, baseada na Análise da Margem Foliar, mais apta para a reconstrução da TMA de floras fósseis cenozoicas da região.
Palavras-chave: Material foliar, serapilheira, acumulações de macro-restos vegetais, angiospermas, Análise da Margem Foliar
PAULO, BRAZIL, AND THE LEAF MARGIN ANALYSIS FOR SOUTH AMERICA. PALEOBOTANICAL IMPLICATIONS.
In this study, we analyzed the taxonomic composition and physiognomic features of the leaf material of seven samples of leaf litter of the riparian forest of Mogi Guaçu Ecological Station, Northeastern of the Sao Paulo State, Brazil, as well as five accumulations of plant macroremains that are found along meandering rivers of the Northeastern, Eastern and the South coastline of Sao Paulo State, with the purpose of obtaining new guidelines for the analysis and interpretation of the fossil associations angiosperms. We also analyzed the relationship in between the proportion of the untoothed species of a flora and the mean annual temperature (MAT) of a dataset of 121 localities the South America, in attempt to establishing a new equation based on the Leaf Margin Analysis for the whole region. When analyzing the foliar material from the leaf litter, we observed that the relationship in between the number of species and the number of leaves/leaflets, as well as the floristic composition, depends on the locality, habitat and wind-induced dispersion. The 60–95% of these leaf material belongs to 2–3 tree species. Most of the identified species belongs to the Bignoniaceae, Euphorbiaceae, Fabaceae, Myrtaceae and Sapindaceae families. The 55–70% of the identified species are from trees and the remaining 20-40% are climbing species. These species represent a 8–35% of all tree species richness and a 5–32% of all climbing species richness of the área. The main physiognomic features of the leaf material allowed us to estimate the MAT and the mean annual precipitation (MAP). The obtained MAT values underestimated the real value in 0.8–1.8 °C and overestimated in 1.5–4.8 °C, and the obtained MAP values underestimated the real value in 11–188 mm and overestimated in 44–83 mm. The accumulations of plant macroremains studied can be considered a high-resolution record of the El Niño. The leaf material that is present in these accumulations depends on the locality, habitat and transport produced by wind and water. The 70–85% of this leaf material belongs to 2–3 tree species. Most of them are identified as part of the Bignoniaceae, Fabaceae and Sapindaceae families. The 70% of the identified species are from tree and the remaining 30% are climbing species. These species represent a 25–35% of all tree species richness and a 23–32% of all climbing species richness of the área. The main physiognomic features of the leaf material allowed estimation of the MAT and MAP at the moment of deposition. The obtained AMT values underestimated the real value in 0.5–1.3 °C and overestimated the real value in 2.2 °C, and the obtained values of MAP underestimated the real value in 332–1070mm. The relationship analysis in between the proportion of the untoothed species and the MAT of a dataset of 121 localities the South America allowed us to create a new linear regression equation based on the Leaf Margin Analysis, more robust to reconstruct the MAT of Cenozoic fossil flora of the region.
Keywords: Leaf material, leaf litter, accumulations of plant macroremains, angiosperms, Leaf
SUMÁRIO
INTRODUÇÃO 14
OBJETIVOS E APRESENTAÇÃO DOS RESULTADOS 17
CAPÍTULO 1. Characterization of the leaf litter of a riparian forest associated
with the Cerrado biome, Southeastern Brazil. 19
1. Introduction 20
2. Materials and methods 22
3. Results 25
4. Discussion 28
5. Conclusions 33
References 35
CAPÍTULO 2. Caracterização taxonômica e fisionômica do material foliar de duas acumulações de macro-restos vegetais do curso médio superior da bacia do
Rio Mogi Guaçu, São Paulo, Brasil. 64
1. Introdução 65 2. Materiais e métodos 68 3. Resultados 71 4. Discussão 73 5. Conclusões 78 Referências bibliográficas 80
CAPÍTULO 3. Reconstrução da temperatura média anual e a precipitação média anual a partir do material foliar preservado nas acumulações de
macro-restos vegetais da bacia do Rio Itanhaém, São Paulo, Brasil. 102
1. Introdução 103 2. Materiais e métodos 105 3. Resultados 106 4. Discussão 107 5. Conclusões 108 Referências bibliográficas 108
1. Introdução 122 2. Materiais e métodos 124 3. Resultados 126 4. Discussão 126 5. Conclusões 129 Referências bibliográficas 130
CAPÍTULO 5. Uma nova equação para a estimação da temperatura média
anual na América do Sul com base na Análise da Margem Foliar. 142
1. Introdução 143 2. Materiais e métodos 144 3. Resultados 146 4. Discussão 147 5. Conclusão 149 Referências bibliográficas 149 CONCLUSÕES FINAIS 162 REFERÊNCIAS BIBLIOGRÁFICAS 163 ANEXO 167
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INTRODUÇÃO
A paleobotânica objetiva através do uso do registro fóssil reconstruir a vegetação, interpretar as mudanças ambientais e climáticas dos diferentes biomas ao longo do tempo, com a finalidade de compreender os padrões evolutivos e migratórios da biota vegetal (Burnham, 1989). O registro fóssil só nos permite ter acesso a uma parte desta informação, já que ele não preserva toda a diversidade de espécies, devido ao transporte, soterramento e diagênese que ocorre durante o processo de fossilização (Martín-Closas e Gomez, 2004; Ricardi-Branco et al., 2009). O ramo da paleontologia que auxilia no entendimento dos processos de fossilização é denominado tafonomia, a qual os agrupa em três fases sucessivas, conhecidas como necrologia, bioestratinomia e fóssildiagêneses (Efremov, 1940). A necrologia estuda as causas da produção de um determinado resto vegetal, a bioestratinomia o processo de transporte e sedimentação, e a fóssildiagêneses os procesos litosféricos que ocorrem durante o enterramento (Martín-Closas e Gomez, 2004).
Com a finalidade de compreender cada uma dessas três fases, sobretudo a de necrologia e da bioestratinomia, foram realizados estudos experimentais de laboratório e de campo (Martín-Closas e Gomez, 2004). Os estudos de campo se baseiam em observações em uma ampla variedade de ambientes (Martín-Closas e Gomez, 2004), especialmente nos fluviais, os quais apresentam um grande potencial para a conservação de folhas (Burnham, 1989; Ricardi-Branco et al., 2009, 2011; Ellis e Johnson, 2013). Na região tropical estes estudos são muito importantes, já que as fases tafonômicas apresentam características únicas devido à falta de estações bem definidas, o que leva a uma acumulação contínua do material foliar (Ricardi-Branco et al., 2009). Estes estudos se focaram em analisar as folhas da serapilheira de diferentes ambientes de sedimentação nas florestas modernas, para compreender a acumulação primária do material foliar e a influência do processo de transporte e de deposição (Burnham, 1989, 1994, 1997; Burnham e Spicer, 1986; Ricardi-Branco et al., 2009; Ellis e Johnson, 2013).
Os resultados obtidos nestes estudos nem sempre são diretamente aplicáveis ao registro fóssil, mas eles nos permitem ter uma ideia de como influenciam o transporte e a dispersão na composição taxonômica (Burnham, 1989, 1994, 1997; Ellis e Johnson, 2013), conhecer o hábito das espécies que estão presentes (Burnham, 1989, 1994, 1997), e a riqueza relativa de espécies que representa (Burnham, 1993). Isto nos permite realizar reconstruções
paleoecológicas mais precisas, e compreender melhor os padrões e processos evolutivos (Burnham e Johnson, 2004).
As folhas de angiospermas, que estão presentes nas associações fósseis a partir do Cretáceo não só nos permitem fazer a reconstrução da vegetação, suas principais características fisionômicas, tipo de margem e tamanho, têm sido amplamente utilizadas pelos paleobotânicos para a reconstrução da temperatura e a precipitação (Little et al., 2010; Peppe et al., 2011; Royer, 2012; Ellis e Johnson, 2013). Diferentes metodologias foram desenvolvidas com base em observações realizadas em florestas modernas, onde é possível notar que há uma covariância entre as margens com dentes e a temperatura média anual (TMA), e entre o tamanho da folha e a precipitação média anual (PMA) (Royer, 2012).
A Análise da Margem Foliar tem sido a metodologia mais amplamente utilizada para a determinação da TMA (Little et al., 2010). Esta se baseia na relação linear entre a percentagem de espécies de dicotiledôneas lenhosas sem dente de uma flora com a TMA (Wilf, 1997; Little et al., 2010; Hinojosa et al., 2011). Esta correlação tem sido calibrada na maioria das regiões do mundo, e geralmente é estatisticamente significativa e convergente entre as regiões (Royer, 2012). Na América do Sul esta correlação tem sido estudada em regiões muito específicas (Gregory-Wodzicki, 2000; Aizen e Ezcurra, 2008; Hinojosa et al., 2011; Fanton, 2013), assim como em toda a região tropical (Kowalski, 2002; Hinojosa et al., 2011) e tropical/temperada (Hinojosa et al., 2011; Kennedy et al., 2014). Como o tipo de margem das folhas de uma flora está submetido a restrições filogenéticas e históricas recomenda-se aplicar uma correlação no contexto de uma história fitogeográfica compartilhada, com a finalidade de que as estimações da TMA sejam significativas (Aizen e Ezcurra, 2008; Little et al., 2010; Hinojosa et al., 2011). Na atualidade assume-se que a Análise da Margem Foliar subestima a TMA (Peppe et al., 2011), apresentando um erro mínimo de ±5 °C (Peppe et al., 2011; Royer, 2012), e no caso em que é utilizada uma calibração regional apropriada o erro é aproximadamente de ±2 °C (Royer, 2012).
Há diversos estudos realizados que demonstram a aplicabilidade da Análise da Margem Foliar na região tropical (Wilf, 1997; Kowalski, 2002). Também para conhecer o viés que introduz a tafonomia têm sido realizados diferentes estudos com base nas folhas do dossel (Burnham et al., 2001, 2005) e da serapilheira (Burnham, 1989, 1997; Ellis e Johnson, 2013; Ricardi-Branco et al., 2015). Estes estudos permitiram concluir que as estimações da TMA não são afetadas pela alta diversidade (Burnham et al., 2005). Estas são afetadas principalmente pela
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frequência de espécies com margem sem dentes (Burnham et al., 2001), a qual pode variar drasticamente entre os diferentes habitats de uma mesma floresta (Burnham et al., 2001). As estimativas podem ser muito precisas independentemente do tipo de habitat (Ellis e Johnson, 2013), mas geralmente as florestas que crescem associadas a lagos ou rios subestimam a TMA, devido à alta proporção de espécies com margem sem dentes (Burnham, 1989; Burnham et al., 2001), apresentando um erro entre ±2.5 a ±5 °C (Burnham et al., 2001).
A reconstrução da PMA geralmente é realizada por meio da Análise da Área Foliar, a qual relaciona a área foliar média de uma flora com a PMA (Wilf et al., 1998). Ao contrário da Análise da Margem Foliar, a história evolutiva afeta em menor grau o tamanho da folha que o tipo de margem (Little et al., 2010). As estimativas não são muito precisas, apresentando, em geral, um erro de ±500 mm (Wilf et al., 1998) a ±1000 mm ou ainda superior (Peppe et al., 2011). Isto se deve principalmente a que em muitas localidades as folhas podem refletir um déficit hídrico, devido as características da temperatura, do solo e/ou das águas subterrâneas (Royer, 2012). Portanto, recomenda-se ser extremamente cauteloso no momento de fazer as interpretações (Wilf et al., 1998; Jacobs, 1999, 2002; Burnham et al., 2005; Peppe et al., 2011).
A aplicabilidade da Análise da Área Foliar na região tropical foi comprovada através de diversos estudos (Jacobs, 1999, 2002; Burnham et al., 2005), assim como o viés que introduz a tafonomia nas estimações da PMA (Burnham et al., 2005; Ellis e Johnson, 2013; Ricardi-Branco et al., 2015). Estes estudos concluíram que as estimações da PMA podem ser muito imprecisas (Jacobs, 2002; Burnham et al., 2005) ou muito precisas (Ricardi-Branco et al., 2015), e que podem variar em uma grande proporção entre os diferentes habitats de uma mesma floresta (Ellis e Johnson, 2013). Geralmente se subestima a PMA (Burnham et al., 2005; Ellis e Johnson, 2013; Ricardi-Branco et al., 2015), apresentando um erro maior aos ±400 mm (Burnham et al., 2005), e quando se sobrestima o erro é de aproximadamente ±1000 mm (Jacobs, 2002).
No Sudeste do Brasil, nos últimos anos se têm levado a cabo diversos estudos que analisam o material foliar que se acumula na serapilheira das florestas modernas e ao longo de rios meandrantes com a finalidade de conhecer a dimensão do viés introduzido pelos processos tafonômicos, principalmente pela necrologia e a bioestratinomia, ao registro fóssil e como estes afetam a reconstrução da vegetação e o clima (Ricardi-Branco et al., 2009, 2011, 2015). Também foi estudada com base na Análise da Margem Foliar a relação entre a proporção de
espécies sem dentes e a TMA com a finalidade de gerar uma equação de regressão, que pudesse ser utilizada para reconstruir a TMA das floras fósseis cenozoicas da região (Fanton, 2013). Estes estudos são de grande importância, já que a maioria das associações de folhas fósseis que se encontram ao redor do mundo foram derivadas de florestas tropicais, com uma grande riqueza de espécies, ou apresentaram as condições favoráveis para concentrar um grande número de espécies derivadas de diferentes unidades ecológicas (Burnham et al., 2005).
OBJETIVOS E APRESENTAÇÃO DOS RESULTADOS
O objetivo principal deste trabalho foi analisar o material foliar que se acumula na serapilheira de uma floresta ripária e ao longo da margem de vários rios meandrantes do estado de São Paulo, com a finalidade de conhecer e discutir como afetam os principais processos tafonômicos a reconstrução da vegetação e o clima. Também se analisou a relação entre a proporção de espécies sem dentes e a TMA na América do Sul a partir de um novo conjunto de dados. Os objetivos específicos incluíram:
Caracterização taxonômica e fisionômica do material foliar da serapilheira da floresta ripária da Estação Ecológica de Mogi Guaçu;
Caracterização taxonômica e fisionômica do material foliar de diferentes acumulações de macro-restos vegetais do estado de São Paulo;
Analisar a relação entre a proporção de espécies sem dentes e a TMA na América do Sul a partir de um conjunto de dados de 121 localidades.
Os resultados obtidos nesta pesquisa são apresentados na forma de artigos em língua inglesa e portuguesa. Assim, a tese apresentada contempla os seguintes capítulos e textos anexos:
Capítulo 1: apresenta o artigo intitulado “Characterization of the leaf litter of a riparian forest associated with the Cerrado biome, Southeastern Brazil”;
Capítulo 2: apresenta o artigo intitulado “Caracterização taxonômica e fisionômica do material foliar de duas acumulações de macro-restos vegetais do curso médio superior da bacia do Rio Mogi Guaçu, São Paulo, Brasil”;
Capítulo 3: apresenta o artigo intitulado “Reconstrução da temperatura média anual e a precipitação média anual a partir do material foliar preservado nas acumulações de macro-restos vegetais da bacia do Rio Itanhaém, São Paulo, Brasil”;
18
Capítulo 4: apresenta o artigo intitulado “Caracterização taxonômica e fisionômica do material foliar de uma acumulação de macro-restos vegetais do Rio Capivari, São Paulo, Brasil”;
Capítulo 5: apresenta o artigo intitulado “Uma nova equação para a estimação da temperatura média anual na América do Sul com base na Análise da Margem Foliar”;
Anexo: apresenta o capítulo de livro intitulado “Relationships among subaquatic environment and Leaf/Palinomorph Assemblages of the Quaternary Mogi-Guaçú River alluvial plain, SP, Brazil”, onde se podem observar resultados parciais desta pesquisa.
CAPÍTULO 1. Characterization of the leaf litter of a riparian forest associated with the Cerrado biome, Southeastern Brazil.
1
Francisco Santiago, 1Fresia Ricardi-Branco, 1Sueli Y. Pereira, 2Paulo R. B. Pereira 1
Universidade Estadual de Campinas, Instituto de Geociências, Departamento de Geologia e Recursos Naturais, Campinas 13083-970, SP, Brazil. email: franciscorios@ige.unicamp.br
2
Instituto Florestal, Estação Experimental de Mogi Mirim, Mogi Mirim 13801-350, SP, Brazil.
Abstract
The leaf litter of a riparian forest in Southeastern Brazil was characterized through seven samples, four collected under the canopy and three near the river bank, in order to provide modern analogs for a better understanding of fossil angiosperms associations. When analyzing the individual samples, as well as grouped for each microhabitat, we can see that the relation between the number of species and leaves/leaflets, the floristic composition and the number of leaves/leaflets by species present depend on the site, the microhabitat and the lateral dispersion of the leaves/leaflets produced by the wind. We also have that 60–96% of the leaf material belongs to 2–5 tree species, which are characterized by being the most important of the canopy, and the remaining 4–40% to a variable number of tree and climbing species. Most of the species identified belong to the families Bignoniaceae, Euphorbiaceae, Fabaceae, Myrtaceae and Sapindaceae which group the greatest richness of arboreal and climbing species of the area. Of all the species identified we have to 56–73% are arboreal and 21–38% are climbing, that represented in 8–35% and in 5–32% the total richness of tree and climbing species of the area. The physiognomic characteristics of the leaves/leaflets that are present in the leaf litter samples allowed to reconstruct the mean annual temperature, which generally overestimates the real value, and mean annual precipitation of the area, which generally underestimates the real value.
Keywords: Leaf litter, riparian forest, physiognomic characteristics, mean annual
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1. Introduction
The analysis of the primary accumulation of leaf litter in modern forests is essential to have a better understanding of the taphonomy of fossil angiosperm associations, to have a better idea about the original community structure and see how the leaf physiognomic characteristics reflect the climate (e.g., Burnham, 1989, 1994, 1997; Greenwood, 1991, 1992, 2005; Ellis and Johnson, 2013). All this in order to improve the reconstruction of the evolutionary history of vegetation and climate during the Cenozoic.
Several studies have been conducted in tropical forests which focus on understanding the way the permanent vegetation and the climate are reflected by the leaf litter (Burnham, 1989, 1997; Greenwood, 1991, 1992, 2005; Ellis and Johnson, 2013). These have allowed to conclude, that in the leaf litter, one can recognize the dominant/subdominant canopy species, a large proportion of the climbing species, the most important families in the area, and that the total tree species richness is poorly reflected (Burnham, 1989, 1993, 1994, 1997; Greenwood, 1991, 1992, 2005; Steart et al., 2005; Ellis and Johnson, 2013). The studies also concluded that the leaf physiognomic characteristics allow to determine the climate of a restricted area (Burnham, 1989; Ellis and Johnson, 2013; Ricardi-Branco et al., 2015). The applicability and accuracy of the different predictive models developed to determine the climate have been corroborated in tropical forests based on canopy leaves (Wilf, 1997; Burnham et al., 2001, 2005; Kowalski, 2002), and of leaf litter (Burnham, 1989, 1997; Burnham et al., 2001; Ellis and Johnson, 2013; Ricardi-Branco et al., 2015), allowing to know the influence of habit and habitat in the estimates.
To help better understand the angiosperm fossilization process and as the vegetation and climate of a restricted area can be reflected in the fossil record, a new study of the primary accumulation of leaf litter was carried out in a riparian forest associated with the Cerrado biome. The forest is found in a fluvial plain in which meanders develop that present great potential for the conservation of fossil leaves (Burnham, 1989; Ricardi-Branco et al., 2009, 2011, 2015). The Cerrado is one of the most important biomes of Brazil, which is characterized for being a wide tropical savannah region that presents various physiognomies, among which the riparian forest stands out (Ribeiro and Walter, 2001). The riparian forests are of great importance in the plant diversity of the Cerrado biome because in these are concentrated near 33% of all known species of the biome, despite occupying a small area, approximately 5% in relation to the other physiognomies (Felfili et al., 2001). These forests
are related to the natural drainage system, which allow them to interact with other large biomes, such as the Amazonian forest and the Atlantic forest which have penetrated the Cerrado domains meanwhile the valleys have expanded (Ribeiro and Walter, 2001). Because riparian forests contain floristic elements of other biomes, they become large repositories of diversity, as they act as a refuge for plant species threatened by the destruction of continuous forest formations (Felfili et al., 2001).
Therefore, this project has the objective of analyzing the accumulated leaf litter in a riparian forest is located in a tropical region, in order to obtain new guidelines for sampling, analysis, and interpretation of fossil angiosperms associations of high diversity that developed along meandering rivers during the Cenozoic.
1.1. Characterization of the study area
The riparian forest, where the study was conducted, is located in SE Brazil, in the NE region of the state of São Paulo, in a fluvial plain of the middle course of the hydrographic basin of Mogi Guaçu river. The area lies within the limits of Mogi Guaçu Ecological Station (22°10′– 22°18′ S, 47°08′–47°11′ W) (Fig. 1), which is under the administration of the Forestry Institute, Secretary for the Environment of the State of São Paulo.
The fluvial dynamics of the middle course of Mogi Guaçú river are conditioned by the different lithologies and geological structures that are present, allowing the development of fluvial plains with meandering currents (Zancope and Filho., 2006), that can wander around the plain or be restricted to the meandering strip (Zancope et al., 2009). These fluvial plains sustain the riparian forest, which it is the plant formation most important of the area, for its wide distribution, that is found associated with different physiognomies of the Cerrado biome (Leitao-Filho, 1982).
The riparian forest of Mogi Guaçu Ecological Station (Fig. 2) follows the main course of Mogi Guaçu river along 19 km and is directly influenced by it, through the hydric regime and temporary floods (Gibbs and Leitão-Filho, 1978; Passos, 1998; Ricardi-Branco et al., 2015). This originates an environmental selectivity process, which defines the species that must occupy the different habitats, resulting in the forest having a structure and floristic composition quite variable (Gibbs and Leitão-Filho, 1978; Mantovani et al., 1989; Passos, 1998). This forest is characterized by presenting a low and open canopy, with a dense understory (Passos, 1998). For this forest have been reported between 43 and 59 tree species
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(Gibbs and Leitão-Filho, 1978; Gibbs et al., 1980; Mantovani et al., 1989; Passos, 1998), and 89 climbing species, between herbaceous and woody, which are abundant in the canopy and make up a significant proportion of the vegetation (Neto et al., 2012).
According to Köppen climate classification, the area presents a Cwa climate, humid temperate climate with dry winters and hot summers (Sparovek et al., 2007). According to the data collected by the weather station of Mogi Guaçu Ecological Station, for the period of 1971– 2010, the area presents a mean annual temperature (MAT) of 20.6 °C and a mean annual precipitation (MAP) of 1348 mm.
2. Materials and methods 2.1. Sampling sites
Throughout the study area, four sites were selected (Fig. 1), which represent different habitats within the forest, to collect four samples of leaf litter accumulated under the canopy and three samples near the river bank (Table 1). These locations are described below:
1. Site I (Points 1.1, 1.2): known as Catingueiro, is subject to frequent flooding during periods of river overflow.
2. Site II (Point 2.1): known as Ilha 1, located in a steep ravine without the direct influence of the river.
3. Site III (Points 3.1, 3.2): known as Ilha 2, located in an old abandoned river bed, which is activated during periods of river overflow, where water accumulates to form semi-permanent ponds.
4. Site IV (Points 4.1, 4.2): known as Fundão, presents similar characteristics to Site III.
2.2. Sample collection
Individual samples of leaf litter were collected in an area of 1.5 × 1.5 m, which it is the recommended to carry out paleobotanical studies (Burnham, 1994), in each of the selected points for each site. The leaf litter collected were pressed in the field, and subsequently classified and identified in the laboratory. The samples were collected between September and November 2013, and they represent the accumulated leaf litter of the last 18 months, where the leaves/leaflets of the months of July and August predominate, this is considered the period of greatest production (Delitti, 1984).
Samples of the most representative vegetation in each of the selected sites were also collected, which were pressed and dried by traditional methods of herbarium, the purpose of making a reference collection that would allow the identification of the leaves/leaflets present in the leaf litter collected.
2.3. Classification and identification of leaf material
The leaves found in each sample of leaf litter collected were initially classified as morphotypes, based on its leaf architecture, following the DMNS (2011) classification scheme, and subsequently identified with the support of the reference collection, lists of vegetation of the area (Gibbs and Leitão-Filho, 1978; Gibbs et al., 1980; Mantovani et al.,
1989; Passos, 1998; Neto et al., 2012), and virtual herbarium
(http://fm1.fieldmuseum.org/vrrc/, http://www.herbariovirtualreflora.jbrj.gov.br/, http://www.tropicos.org/). For each identified species the number of leaves/leaflets and the fragments of leaves/leaflets that preserved its integrity by more than 50% was counted.
2.4. Statistical analysis
To determine the influence of the species distribution in the area and the microhabitat on the floristic composition of the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2), a Correspondence Analysis (CA) was carried out, which is a multivariate technique that allows summarizing large amounts of information in a reduced number of dimensions (Benzecri, 1992).
Initially, a CA was performed from the presence-absence data of species in each of the samples, and subsequently, another analysis was performed from the number of specimens per species data in each of the samples. For both analyzes, the statistical package XLSTAT 2016 was used.
2.5. Determination of relative species richness
The relative tree species richness found in the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2), as individual or grouped samples for each microhabitat, was determined based on the lists of tree species for the area made by Gibbs and Leitão-Filho (1978), Gibbs et al. (1980), Mantovani et al. (1989) and Passos (1998). The species reported by the different authors were grouped into families (Supplementary Data 1), according to the classification proposed by the APG III (2009). Their
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names and the existence of botanical synonyms were revised in the database of Missouri Botanical Garden (http://www.tropicos.org/).
To determine the relative climbing species richness found in the leaf litter collected, as individual or grouped samples for each microhabitat, it was used as reference the list of woody climbing species made for the area by Neto et al. (2012).
2.6. Reconstruction of mean annual temperature (MAT) and mean annual precipitation (MAP)
The reconstruction of MAT from the leaf samples litter collected it was performed based on the Leaf Margin Analysis (LMA), which relates the percentage of woody dicot leaf species with untoothed leaves of a flora with the MAT (Wilf, 1997; Greenwood, 2005; Hinojosa et al., 2011). You can also include some species of a genus of monocots, Smilax, by its similarity foliar with the dicotyledonous leaves (Wilf, 1997). The selected equation can be seen in Table 2. This equation was developed from a database that contains only locations of South America, therefore the values obtained are significant (Hinojosa et al., 2011). This presents a standard error of ±3.5 °C (Hinojosa et al., 2011), the which is very broad, for this reason it was assumed the minimum error of ±2 °C recommended by Wilf (1997).
For the reconstruction of MAP from the leaf litter samples collected, a Leaf Area Analysis (LAA) was performed, which relates the leaf area of the species of flora with MAP (Wilf et al., 1998). The selected equation can be seen in Table 2. This equation was generated from a database that contains some localities of South America (Jacobs and Herendeen, 2004). The estimates of MAP are very inaccurate, usually presenting an error of ±500 mm (Wilf et al., 1998), which is very large, for this reason it was assumed the minimum error of ±20%, which is the recommended for tropical forests with precipitation less than 1500 mm (Burnham et al., 2005).
3. Results
3.1. Characteristics of leaf litter
The leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) present between 293 and 771 leaves/leaflets, which correspond to between 11 and 29 species (Fig. 3, Supplementary Data 2). The relation between the number of species and of leaf/leaflets present in each of the samples seems to be conditioned first by the site and second by the sampling microhabitat (Fig. 3).
The influence of the microhabitat on the relation between the number of species and of leaves/leaflets is maintained at the moment of grouping the samples collected for each one of them. This is clearly seen, given that in the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) we have a total of 2003 leaf/leaflets, which correspond to 59 species, and in the leaf litter collected near the river bank (Points 1.2, 3.2 and 4.2) we have a total of 1576 leaves/leaflets, which correspond to 42 species (Supplementary Data 2).
The sampling site not only influence the relation between the number of species and of leaves/leaflets, but also the floristic composition of each of the leaf litter samples collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) (Fig. 4, Supplementary Data 3). Although the sampling site is the main influencing factor, we also have that the microhabitat plays a very important role. We can see this very well when the identified species are correlated in both microhabitats for each site (eg, Site I, Points 1.1 and 1.2), with the exception of Site II. The correlations indicate that 20–44% of the species present in the leaf litter collected under the canopy were also found in the leaf litter collected near the river bank, whereas a 24-50% of the species present in the leaf litter collected near the river bank were also found in the leaf litter collected under the canopy (Fig. 5). A similar behavior can also be observed at the moment of grouped correlation of the species identified in the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) with the species identified in the leaf litter collected near the river bank (Points 1.2, 3.2 and 4.1) (Fig. 5).
Besides influencing the relation between the number of species and of leaves/leaflets and the floristic composition of each of the samples, the site and microhabitat of sampling also affect the relation between the number of leaves/leaflets per species in each of the samples (Fig. 6). It is because of this that in the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and
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4.1) we have 2–5 species, mainly trees, representing a 66–96% of all leaves/leaflets (Table 3, Supplementary Data 2). A similar behavior was also found in the leaf litter collected near the river bank (Points 1.2, 3.2 and 4.2), where we have that 2-3 tree species represent a 60-77% of all leaves/leaflets (Table 3, Supplementary Data 2). This behavior is maintained when grouping the samples for each of the microhabitat, where we can observe that 4–5 tree species are approximately equivalent to 62–63% of all leaves/leaflets (Table 3, Supplementary Data 2).
In the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2), despite having a small set of species which groups a large proportion of all leaves/leaflets (Table 3), we have a large variety of species within the remaining 5–40% of leaves/leaflets (Supplementary Data 2). This behavior is maintained when grouping the samples for each of the microhabitat, where we have that the 37–38% of all leaves/leaflets represent a large variety of species (Supplementary Data 2).
The large majority of species that are present in the leaf litter collected are associated with the families Bignoniaceae, Euphorbiaceae, Fabaceae, Myrtaceae, and Sapindaceae (Table 4, Supplementary Data 3). Generally, the tree species are related to the families Euphorbiaceae, Fabaceae, and Myrtaceae, and the climbing species to the families Bignoniaceae and Sapindaceae (Supplementary Data 3).
By analyzing the habit of all identified species in the leaf litter samples collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2), we have that 56–73% are trees and 21–38% are climbing species (Table 5). It was also possible to appreciate some shrub species, these were only found in the samples collected in the Site III (Points 3.1 and 3.2) (Supplementary Data 3). When grouping the samples for each microhabitat, we have that a 63% of the species are trees and a 32–33% are climbing species (Table 5).
The percentage of tree species present in the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.1) represent in an 8–15% the total tree species richness reported for the area, and when grouping the samples for each microhabitat this value increases to 25–35% (Table 5). In the individual samples of leaf litter we also have a significant percentage of climbing species, which represent in an 5–16% the total climbing species richness reported for the area, and when grouping the samples for each microhabitat this value increases to 23–32% (Table 5).
3.2. Reconstruction of mean annual temperature (MAT) and mean annual precipitation (MAP)
The results of the MAT estimates based on leaf litter collected under the canopy(Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2), as individual and grouped samples for each microhabitat can be appreciated in Table 6 and the Fig. 7. The estimates generally overestimated the real value when the percentage of species untoothed was 87–93% (Table 6). We can also appreciate an underestimation of the real value when the percentage of species untoothed was 65–69% (Table 6).
The TMA values obtained from the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) will depend on the percentage of species untoothed, which it’s closely related with the site and microhabitat of sampling (Table 6, Fig. 7). The microhabitat of sampling is the main factor of influence, which we can appreciate clearly when compare to one another the MAT estimates obtained from the leaf litter collected under the canopy and near the river bank for each of the sites (eg, Site I, Points 1.1 and 1.2). In the Site I (Points 1.1 and 1.2) and Site IV (Points 4.1 and 4.2) the values obtained from the leaf litter collected under the canopy are lower than those obtained from the leaf litter collected near the river bank in 3.3–4.2 °C, because the percentage of species untoothed varies by 14-18% (Table 6). On the other hand, we have that in the Site III (Points 3.1 and 3.2) the value obtained from the leaf litter collected under the canopy is superior to that obtained from the leaf litter collected near the river bank in 3.1 °C, because the percentage of species untoothed varies by 13% (Table 6).
The MAT estimates obtained from the leaf litter samples collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) are very inconsistent, they underestimated the real value in 0.8–1.8 °C and overestimated in 4.3–4.8 °C (Table 6, Fig. 7). On the other hand, the estimates obtained from the leaf litter samples collected near the river bank (Points 1.2, 3.2 and 4.2) are more consistent, they overestimated the real value in 1.5–3.4 °C (Table 6, Fig. 7). When grouping the samples for each microhabitat we have that the TMA estimates are similar, and overestimate the real value in 1.7 °C (Table 6, Fig. 7).
From the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) the MAP was also assessed. The results obtained for the individual and grouped samples for each microhabitat can be appreciated in the Table 7 and the Fig. 8. The estimates generally underestimated the real value in 11–188 mm and
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overestimated in 44–83 mm (Table 7), due to the variability in the proportion of leaves with larger leaf area present in the samples (Supplementary Data 4).
The microhabitat of sampling also affects MAP estimates, which we can appreciate clearly when compare to one another the MAP estimates obtained from the leaf litter collected under the canopy and near the river bank for each of the sites (eg, Site I, Points 1.1 and 1.2). In the Site I (Points 1.1 and 1.2) and Site III (Points 3.1 and 3.2) the values obtained from the leaf litter collected under the canopy are lower than those obtained from the leaf litter collected near the river bank in 8–271 mm (Table 7). On the other hand, we have that in the Site IV (Points 4.1 and 4.2) the value obtained from the leaf litter collected under the canopy is superior to that obtained from the leaf litter collected near the river bank in 20 mm (Table 7).
The MAP estimates obtained from the leaf litter samples collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) are very inconsistent, they underestimated the real value in 11–188 mm and overestimated in 44 mm (Table 7, Fig. 8). On the other hand, the estimates obtained from the leaf litter samples collected near the river bank (Points 1.2, 3.2 and 4.2) are more consistent, they underestimated the real value in 31–87 mm and the overestimated in 83 mm (Table 7, Fig. 8). When grouping the samples for each microhabitat we have that the PMA tend to underestimate the real value in 19–87 mm, being the leaf litter collected near the river bank which better reflects the PMA (Table 7, Fig. 8).
4. Discussion
4.1. Characteristics of leaf litter
The floristic composition of the riparian forest of Mogi Guaçu Ecological Station is very variable. This is mainly due to the influence of Mogi Guaçu river, as well as by the water table and the topography of the area, which has generated a process of environmental selectivity, that defines the species that occupy the different sites and their microhabitats (Gibbs and Leitão-Filho, 1978; Mantovani et al., 1989; Passos, 1998). It is because of this that we have the variability in the relation between the number of species and of leaves/leaflets, the floristic composition, and in the relation between the number of leaves/leaflets per species observed in each of the leaf litter samples collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) (Supplementary Data 2). This characteristic has also been observed in other similar studies carried out in tropical forests (Burnham, 1989; Greenwood, 1991, 1992).
The sampling microhabitat plays a fundamental role in the floristic composition of leaf litter collected. This is because in a same site of the forest exist different girdles, which can present a floristic relation of between 52% and 67% (Mantovani et al., 1989), due to the structural pattern and floristic composition of the area (Gibbs and Leitão-Filho, 1978; Mantovani et al., 1989; Passos, 1998). The floristic composition of leaf litter is also influenced by the dispersion of the leaves, which is generally produced by the wind (Burnham, 1989; Greenwood, 1991). The leaves can be transported between 15 and 20 m (Burnham, 1994, 1997), and in open sites the transport may be greater than under the canopy, since the wind encounters no obstacles (Greenwood, 1991; Martín-Closas and Gomez, 2004).
In the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) exist a small set of species which groups a large proportion of all leaves/leaflets (Table 3). This is because the forest has girdles that can be dominated by few species (Mantovani et al., 1989; Passos, 1998), which may have a high density (Gibbs and Leitão-Filho, 1978; Gibbs et al., 1980; Mantovani et al., 1989; Passos, 1998). These species are emerging, and they are the most important of the canopy (Gibbs and Leitão-Filho, 1978; Gibbs et al., 1980; Mantovani et al., 1989; Passos, 1998).
They are also characterized by presenting small leaves/leaflets (Greenwood, 1992; Martín-Closas and Gomez, 2004; Steart et al., 2005), and to provide the largest amount of leaf material of the forest (Delitti, 1984; Burnham, 1989; Greenwood, 1991, 1992), because they are exposed directly to the action of the wind (Martín-Closas and Gomez, 2004). But it should not be assumed that only the most important canopy species are the only ones that are well represented in the leaf litter, since other species of minor importance are also well represented (Supplementary Data 2). This characteristic has also been observed in other similar studies carried out in tropical forests (Burnham, 1989, 1994, 1997). Therefore, in the leaf litter can generally be observed the most important species of the canopy, despite that all of them are not synchronous in their leaf abscission, due to climatic periodicity (Deletti, 1984). Unfortunately, it is difficult to establish the hierarchy of these species in the forest based on the proportion of leaves/leaflets present in the leaf litter (Burnham, 1994; Ellis and Johnson, 2013), since the species of small leaves/leaflets can produce more leaf material than the species of bigger leaves/leaflets (Greenwood, 1992; Steart et al., 2005).
In the leaf litter collected, we also have that many species are represented by a small proportion of all leaves/leaflets (Supplementary Data 2), which is not visible to the naked eye,
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since they are masked by the large proportion of leaves/leaflets from the most important canopy species (Steart et al., 2005). The species that are represented by this small proportion of all leaves/leaflets usually produce little leaf material, as they occur with a low density in the area (Gibbs and Leitão-Filho, 1978; Mantovani et al., 1989; Passos, 1998; Neto et al., 2012). This behavior is very common of the 70% of the tree species of the area, which may become widely distributed or may be restricted by environmental conditions (Gibbs and Leitão-Filho, 1978; Mantovani et al., 1989; Passos, 1998), and all climbing species, which generally grow in the upper strata of the canopy and are widely distributed (Neto et al., 2012).
In the leaf litter collected, although a small set of species groups a large proportion of all leaf/leaflets (Table 5), we can observe that it reflects very well the families that concentrate the greater tree species richness of the area, which are Euphorbiaceae, Fabaceae and Myrtaceae (Mantovani et al., 1989; Passos, 1998), and families that concentrate the greater climbing species richness, which are Bignoniaceae and Sapindaceae (Neto et al., 2012).
In the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) the proportion of tree species is 56–73% and climbing species is 21–38% (Table 5). This great variability is mainly due to the high heterogeneity of the forest. However, when samples are grouped for each of microhabitats we have that a 63% of the species are trees and 32–33% are climbing species (Table 5). Since the grouped samples are more representative of the area, it attenuates the variability due to the heterogeneity of the forest, and it achieved values very similar to those found in other tropical forests (Burnham, 1994, 1997). It should be noted that the high percentage of climbing species present in each of the individual and grouped samples for each microhabitat allow to observe a significant component of the vegetation, which is of great importance in the canopy structure, and increases the accuracy in the estimation of all climbing species richness of the area (Burnham, 1994, 1997).
The proportion of tree and climbing species present in the leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) represent only 8–15% of all tree species richness and 5–16% of all climbing species richness of the area (Table 5). This characteristic that leaf litter samples poorly reflect the total richness of tree and climbing species of the area seems to be common in tropical forests (Burnham, 1993, 1994). This is due to the structural and floristics high heterogeneity of the forest, and habitat disturbances (Burnham, 1993). Unfortunately this behavior does not change much when the
samples are grouped for each microhabitat, since we only have 25–35% of all tree species richness and 23–32% of all climbing species richness of the area (Table 5), as well as in other tropical forests where similar studies have been carried out (Burnham, 1993). Therefore, the results obtained here further support the hypothesis that not the all species richness in the tropical forests is directly available in the leaf litter (Burnham, 1993).
4.2. Reconstruction of mean annual temperature (MAT) and mean annual precipitation (MAP)
Generally, MAT estimates based on the LMA tend to underestimate the real value by 2.5–5 °C when the leaf material is associated with rivers and lakes, due to the large proportion of species with toothed margin which are present in these areas (Burnham et al., 2001; Greenwood, 2005). This behavior is different from that observed in the MAT estimates obtained in the riparian forest of Mogi Guaçu Ecological Station based on the leaf litter collected under the canopy and near the river bank (Points 1.2, 3.2 and 4.2), which tend to overestimate the real value by 1.5–4.8 °C, due to the large proportion of species with untoothed margin that is present (Table 6). We may also observe an underestimation of the real value, which is not very common, but when it happens is 0.8–1.8 °C, due to a decrease in the proportion of species with untoothed margin (Table 6).
Estimates of the MAT in a determined area based on leaves/leaflets present in the leaf litter is mainly influenced by floristic composition (Greenwood, 1992), the habitat and habit of provenance of the leaves/leaflets (Burnham et al., 2001; Greenwood, 2005), and by its lateral distribution (Greenwood, 1991, 1992), as well as by environmental stresses (Greenwood et al., 2004). This can be clearly seen when comparing the values obtained from the leaf litter collected under the canopy and near the river bank for each one of the sites (eg, Site I, Points 1.1 and 1.2), where exists a difference of 3.1–4.2 °C, because the proportion of species with untoothed margin can vary in a 13–18% (Table 6).
The values obtained from the leaf litter samples collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) are very inconsistent (Table 6, Fig. 7), due to the presence of a discontinuous and complex canopy, with small clearings, which allow the incidence of solar rays at different angles, generating microclimates (Gibbs and Leitão-Filho, 1978; Mantovani et al., 1989; Passos, 1998). On the other hand, the values obtained from the leaf litter samples collected near the river bank (Points 1.2, 3.2 and 4.2) tend to be more consistent and accurate (Table 6, Fig. 7), although the vegetation adapted to this area is discontinuous and presents a large
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number of individuals in the understory, because the penetration of the solar radiation and the humidity are constant due to the river bed (Mantovani et al., 1989). Therefore, the microhabitat of provenance of the samples, defined by its location and the forest structure, is the most influential factor in the MAT estimates in the riparian forest of Mogi Guaçu Ecological Station, since it conditions the floristic composition, the incidence of the sun's rays, and the variations in the air and the soil moisture levels (Gibbs and Leitão-Filho, 1978; Mantovani et al., 1989; Passos, 1998).
The influence of the microhabitat on the estimates is attenuated when we group the samples for each of the microhabitats, as the values obtained are very accurate, better reflecting the MAT of the area (Table 6, Fig. 7). This is primarily because the number of species identified in the grouped samples is larger than the recommended minimum of 25–30 (Wilf, 1997; Burnham et al., 2005).
The leaf litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) and near the river bank (Points 1.2, 3.2 and 4.2) also allowed the reconstruction of the MAP of the area based on the LAA. The MAP estimates generally underestimated the real value by 11–188 mm and also they overestimated by 44–83 mm (Table 7). The underestimation of the real value is a behavior that had already been observed in a previous analysis of this material at the morphospecies level (Ricardi-Branco et al., 2015), and which is very common in other tropical forests (Burnham et al., 2005; Ellis and Johnson, 2013), reaching values higher than 400 mm (Burnham et al., 2005).
Estimates of the MAP in a determined area based on leaves/leaflets present in the leaf litter is mainly influenced by the edaphic and microclimatic conditions (Burnham, 1997), as well as the low representativeness of the leaves with greater leaf area of the canopy trees in the leaf litter (Greenwood, 1991, 1992; Burnham, 1994). This can be clearly seen when comparing the values obtained from the leaf litter collected under the canopy and near the river bank for each one of the sites (eg, Site I, Points 1.1 and 1.2), where we have a difference of 8–271 mm (Table 7). This is mainly because the percentage of leaves with greater leaf area tends to be lower in samples collected under the canopy (Supplementary Data 4).
The values obtained from the leaf litter samples collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) are very inconsistent (Table 7, Fig. 8). This is because the different fragments along the study area may have edaphic and soil moisture conditions quite variable (Batista, 1988; Mantovani et al., 1989), and because the species with greater leaf area may not be well
represented in the leaf litter (Greenwood, 1991). On the other hand, the values obtained from the leaf litter samples collected near the river bank (Points 1.2, 3.2 and 4.2) tend to be more consistent and accurate (Table 7, Fig. 8), reflecting better the MAP. This is because moisture is constant in this microhabitat due to the influence of the river during rainy periods (Mantovani et al., 1989), and the groundwater from the Tubarão and the Cristalino aquifers during the driest periods (Ricardi-Branco et al., 2015). Therefore, the microhabitat of provenance of the samples is the main influential factor in the MAP estimates, as well as in the MAT estimates.
The influence of the microhabitat is also observed when we group the samples for each of the microhabitats, since the value obtained from the litter collected under the canopy (Points 1.1, 2.1, 3.1 and 4.1) remains imprecise. On the other hand, the value obtained from the litter collected near the river bank (Points 1.2, 3.2 and 4.2) is much more accurate, reflecting better the MAP of the area (Table 7, Figure 8).
5. Conclusions
The riparian forest of Mogi Guaçu Ecological Station, São Paulo, Brazil, which is associated with the Cerrado biome, is very heterogeneous in composition and presents a very complex structure, which is clearly reflected in the leaf litter samples collected under the canopy and near the river bank, when they are analyzed individually and in grouped for each of the microhabitat. The characteristics observed in this leaf litter are very important, since they can be taken into account by paleobotanist when designing sampling strategies, and they also allow us to understand the nature and diversity of ancient forests, and make more accurate reconstructions.
The characteristics observed in the leaf litter collected are as follows:
1. The relation between the number of species and leaves/leaflets, the floristic composition and the number of leaves/leaflets by species present in each of the leaf litter samples collected under the canopy and near the river bank, either individually or in groups for each of the microhabitats, depend primarily on the site and microhabitat sampling and also the lateral dispersion of the leaves/leaflets produced by the wind.
2. In the leaf litter samples collected under the canopy and near the river bank, either individually or in groups for each of the microhabitats, we have that 2–5 species group a 60– 96% of all leaves/leaflets. Usually this is because the most important canopy species present
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high density and contribute the largest amount of leaf material, but this does not mean they are the only ones that are well represented.
3. In the leaf litter samples collected under the canopy and near the river bank, either individually or in groups for each of the microhabitats, we also have that a small proportion of all leaves/leaflets represent a very variable number of species. This is because in the area there is a great diversity of tree and climbing species that do not present a high density.
4. In the leaf litter samples collected under the canopy and near the river bank, either individually or in groups for each of the microhabitats, we can observe elements of the most important families in the area, as are Euphorbiaceae, Fabaceae and Myrtaceae, which group the greatest tree species richness, and Bignoniaceae and Sapindaceae, which group the greatest climbing species richness.
5. In the leaf litter samples collected under the canopy and near the river bank there is a proportion of 56–73% of tree species and 21–38% of climbing species. This high variability in proportions is a product of forest heterogeneity. On the other hand, when samples are grouped for each microhabitat we have that a 63% of the species are trees and a 32–33% climbing species. Therefore, it is possible to affirm that in the gouped samples the influence introduced by the forest heterogeneity in the proportions is attenuated.
6. The proportion of tree and climbing species present in individual leaf litter samples collected under the canopy and near the river bank represent only 5–16% of all richness of tree and climbing species of the area, and when they are grouped for each of the microhabitats is 20-35%. This poor reflection of all richness of tree and climbing species of the area is a product of the structural and floristic heterogeneity of the forest, and habitat disturbances.
7. In the leaf litter samples collected under the canopy and near the river bank, both individually or in groups for each of the microhabitats, the MAT, estimated from the LMA, underestimated the real value by 0.8–1.8 °C and the overestimated by 1.5–4.8 °C. Its accuracy depends of the microhabitat, being the leaf litter accumulated near the river bank the one that best reflects the MAT, since the penetration of solar radiation, and the humidity in this microhabitat is larger and more uniform.
8. In the leaf litter samples collected under the canopy and near the river bank, both individually or in groups for each of the microhabitats, the MAP, estimated from the LAA, underestimated the real value by 11-188 mm and overestimated by 44-83 mm. Its accuracy depends of the microhabitat, being the leaf litter accumulated near the river bank the one that best reflects the MAP, since the moisture is constant in this microhabitat throughout the whole year.
