Programa De Pós-Graduação Em Ecologia Perspectivas

INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA-INPA PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA

PERSPECTIVAS MACROECOLÓGICAS NAS ÁREAS ÚMIDAS DOMINADAS POR MAURITIA NA AMAZÔNIA

JOHN ETHAN HOUSEHOLDER

Manaus, Amazonas Junho, 2015 ii

JOHN ETHAN HOUSEHOLDER

PERSPECTIVAS MACROECOLÓGICAS NAS ÁREAS ÚMIDAS DOMINADAS POR MAURITIA NA AMAZÔNIA

Orientador: FLORIAN KARL WITTMANN

Tese apresentada ao Instituto Nacional de Pesquisas da Amazônia como parte dos requisitos para obtenção do titulo de Doutor em Biologia (Ecologia).

Manaus, Amazonas Junho, 2015 ii

Banca Examinadora do Trabalho Escrito

Nome – Institução Parecer

Paul Fine – Univ. California Berkeley Aprovada com Correções

Nigel Pitman – Duke University Aprovada com Correções

Bill Magnusson – INPA Aprovada com Correções

Camila Ribas - INPA Aprovada

Hans Ter Steege – Naturalis Aprovada Biodiversity Center, Netherlands

Banca Avaliadora da Defesa da Tese

Nome – Institução Parecer

Maria Teresa Fernandez Piedade – INPA Aprovado

Camila Ribas – INPA Aprovado

Mike Hopkins – INPA Aprovado

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Ficha catalográfica

H842 Householder, John Ethan

Perspectivas macroecológicas nas areas úmidas dominadas por Mauritia na Amazônia / John Ethan Householder. --- Manaus: [s.n.], 2015.

xi, 115 p. : il.

Tese (Doutorado) --- INPA, Manaus, 2015. Orientadores: Florian Karl Wittmann. Área de concentração: Ecologia.

1. Buriti. 2. Biogeografia. I. Título.

CDD 584.5

Sinopse: Utilizando a presença de Mauritia (Arecaceae) como planta indicadora para condições de inundação e/ou saturação permanente – uma situação abiótica extrema na região – a ecologia de comunidades e biogeografia da vegetação lenhosa de uma área úmida Amazônica dominada por palmeiras é investigada em ampla escala espacial.

Palavras Chave: Biogeografia; Buriti; Heterogeneidade de habitats; Turfeira; Pântano; Areia branca

Dedicatória

To my beautiful son, Julien Ernesto. Born April 8th, 2014. And his beautiful mother, Monica, my wife.

Agradecimentos

The following work would not have been possible if it were not for the significant contributions of a number of people and institutions. I especially thank my advisor, Florian Wittmann, for his willingness to guide me through all aspects of this work. I recognize that his contributions go well beyond that of mere academic guidance and I am eternally grateful for all the experiences I have shared with Florian, friend and colleague. I thank Maria Teresa Fernandez Piedade for her support, trust, and never-failing positive attitude. I thank John Janovec, former advisor and current friend and colleague. John provided me with the initial spark that lit the flame that has inspired me through this work of passion and love, and has continued to provide valuable guidance. A special thanks to Celso, Mario, and all the staff at MAUA working group for their important support. I am always amazed watching this incredible group work like a well-oiled machine even in the most difficult and uncomfortable working conditions. Also, thanks to Aline Lopes for her helpful considerations. I thank Mike Hopkins and INPA herbarium staff for the use of their facilities. I thank Mathias Tobler and BRIT staff for supporting my collection of images on the Atrium website. I also thank the growing number of taxonomic specialists who continue to provide species determinations. Thanks to Simon Queenborough for his collaboration on the NSF proposal, and his interest in my future academic endeavors. Also thanks to Bill Magnusson, Camila Ribas, Hans ter Steege, Nigel Pitman and Paul Fine for graciously reviewing this manuscript and making many excellent suggestions. I consider myself fortunate, especially as a foreigner, to have been able to fulfill a long-standing dream of experiencing and studying in some of the most wild, untrammeled, and beautiful places in the Brazilian Amazon. For this opportunity I am indebted to a number of locals who found the time to work with me, converse with me, and show me their beautiful country and its biological and ecological treasures. I am also indebted to several Brazilian institutions. I thank CNPq for generous financial support (process number 141727/2011-0 and Universal grant no. 475660/2011-0). I also thank the Ministério de Meio Ambiente (MMA) and Instituto Chico Mendes de Conservação de Biodiversidade (ICMBio) for permits and access to conservation areas. vi

Perspectivas macroecológicas nas áreas úmidas dominadas por Mauritia na Amazônia

Resumo

O gênero das palmeiras Mauritia L.f. (Arecaceae) é o componente principal de áreas pantanosas neotropicais e da vegetação de muitas savanas inundadas. A presença deste gênero indica condições de inundação permanente na superfície e/ou próximo à superfície do solo. No presente estudo, foram realizados inventários florísticos em comunidades lenhosas de áreas úmidas dominadas por Mauritia, os buritizais. Na Amazônia brasileira e peruana, um número total de 28 buritizais foi inventariado. O trabalho de campo resultou em mais de 3.000 coletas botânicas, e mais de 8.000 fotografias, publicamente acessíveis em herbário digital (http://atrium.andesamazon.org/). Mais de 40.000 indivíduos lenhosos foram levantados, distribuídos em 89 famílias, 318 gêneros e aproximadamente 750 espécies. Utilizando o gênero Mauritia como indicador de substratos permanentemente alagados, uma condição abiótica extrema na região, a ecologia da comunidade lenhosa deste importante habitat úmido Amazônico foi investigada ao longo de uma grande escala espacial em função de sua composição taxonômica, filogenética e biogeográfica. Os dados indicam que a comunidade de vegetação dos buritizais apresenta uma riqueza florística reduzida, consistente com o conhecimento disponível em literatura. Ao longo de ampla escala espacial, os resultados indicam que os buritizais apresentam uma alta variabilidade na composição florística entre diferentes sítios em comparação com a flora de terra firme. As analises filogenéticas revelaram que o uso do habitat de buritizais provavelmente é um atributo amplamente presente na filogenia de ecossistemas florestados Amazônicos. As analises biogeográficas mostraram que as comunidades demonstram um padrão consistente de substituição composicional ao longo de gradientes de estresse, com uma transição de linhagens majoritariamente Amazônicas em sítios florestados para linhagens majoritariamente extra- amazônicas em sítios arbustivos. É sugerido que o padrão de homogeneidade florística dos buritizais, como tradicionalmente notado, ocorre em conjunto com um padrão de alta diversidade taxonômica, filogenética e funcional, fato muitas vezes subestimado até o momento. Argumenta-se que as análises comparativas de comunidades de buritizais oferecem uma abordagem inovadora e única sobre os recentes modelos de diversidade especifica e ecossistêmica, que até o presente, baseiam-se quase que inteiramente em florestas de terra firme. Desta maneira, os resultados aqui apresentados contribuem tanto para as teorias de biodiversidade nos capítulos 1 e 2, quanto para a ciência aplicada no capitulo 3.

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Macroecological perspectives on Mauritia-dominated wetlands in the Amazon

Abstract

The palm genus Mauritia L.f (Arecaceae) is a principal component of Neotropical freshwater swamp and flooded-savanna vegetation. As such, these palms indicate near-permanent waterlogging at or near ground surface. In this study, expeditionary and exploratory research was undertaken to sample the woody vegetation communities of Mauritia-dominated wetlands (MDWs). A total of 28 MDWs were quantitatively sampled in the Brazilian and Peruvian Amazon. Field work resulted in >3000 botanical collections accompanied by >8000 photographic images made publically available through online resources (http://atrium.andesamazon.org/). Over 40,000 individual woody stems were documented, distributed among 89 families, 318 genera and ~750 woody species. Taking advantage of the indicator status of Mauritia for near-permanently waterlogged substrates – an extreme abiotic condition in the region - the community ecology of woody vegetation of this common Amazonian wetland habitat was investigated across a broad spatial scale regarding its taxonomic, phylogenetic, and biogeographic structure. Data indicate reduced local site richness in MDW vegetation communities, consistent with previous investigation. Over broad spatial scales results show that rather than being comprised of a predictable set of habitat specialists, MDWs exhibit high site-to-site compositional variability relative to surrounding upland forest vegetation. Community phylogenetic analyses reveal that the ability to occupy MDWs is widely distributed in a phylogenetically diverse array of Amazonian forest taxa. Biogeographic analyses reveal that assemblages demonstrate consistent patterns of compositional turnover along local stress gradients, transitioning from largely Amazonian-distributed lineages in forested sites to increasingly extra-Amazonian- distributed lineages in shrubby sites. I suggest that traditionally perceived patterns of community homogeneity of MDWs occur alongside previously underappreciated patterns of taxonomic, phylogenetic, and functional diversity. Taking the results together, I argue that comparative analyses of MDW communities offer unique insight into current models of Amazonian plant and ecosystem diversity that are based almost completely on upland forests, contributing to both Amazonian biodiversity theory (Chapter 1 and 2) and applied science (Chapter 3).

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Sumário

Lista de Figuras ...... ix

Introdução Geral ...... 1

Objetivos ...... 4

Capítulo I ...... 5

Capítulo II ...... 27

Capítulo III ...... 48

Síntese ...... 75

Referências bibliográficas ...... 76

Apêndice ...... 92

Anexos ...... 110

Lista de Figuras

Capítulo I

Figure 1. Map of MDW and terra firme sites examined in this study ...... 9

Figure 2. Histograms of the proportion of stems with dbh >10cm represented by palms in terra firme (above), and MDW (below) sites. In MDWs Mauritia accounts for 89% of all palm stems and 61% of all woody stems (dbh >10cm)...... 14

Figure 3. Box plots of pair-wise dissimilarities within and between MDW and terra firme sites at family and genus taxonomic ranks. Dissimilarities are additively partitioned between nested and turnover components following Baselga (2010). Dissimilarities based on abundance data are qualitatively similar and not shown...... 16

Figure 4. Taxonomic distinctness (D* and D+) of MDW (closed circles) and terra firme (open circles) sites considering the complete taxonomic hierarchy (4 divisions), or only its higher (order and superorder) or lower (genus and family) structures. Dashed segments give within-group means. Stars indicate significant differences (p <0.01) between MDWs and terra firme as revealed by t-tests. Morphospecies richness values of sites are based on a random sub-sample of 148 stems (the least number of stems in a single assemblage)...... 17

Figure 5. Two-dimensional NMDS solution of compositional data at the rank of family. Significant (p >0.5) vectors corresponding to the number of stems (left) and species (right) of each floristic group sensu Gentry(1982) were mapped onto the ordination. At the x

family level, almost half of the dissimilarity between MDW and terra firme is due to a nested structure (see figure 3b). However the relative contribution of nestedness to between-habitat compositional differences decreases rapidly with decreasing taxonomic rank (see figure 3e). Qualitative patterns of site and floristic group distributions are similar regardless of whether family or genus ranks, or abundance or presence-absence data are used...... 18

Capítulo II

Figure 1. Map showing locations of surveyed peatlands and white sands as well as the distribution of sites of the Gentry plot network used to assess distributional patterns of families along the elevation gradient. Boxed windows indicate the areas where peatland and white sand communities were sampled. Gentry sites are classified into two groups differentiated by site elevation (see map legend)...... 32

Figure 2. Histogram of abundance-weighted average scores of families along the axis of the non-metric multidimensional scaling of the Gentry plots, illustrating the wide breadth of biogeographic patterns of families present in the peat and white-sand habitats. The NMDS axis is highly correlated with site elevation (r = 0.93, p > 0.001), thus weighted-average scores describe the average relative position of families along the elevation gradient, where higher scores correspond to families with higher average elevational distributions. White bars indicate abundance-weighted averages of families present in the Gentry dataset. Grey bars indicated averages of families in the peat and white-sand habitats...... 35 xi

Figure 3. Distributions of raw values of the 8 variables used to describe site vegetation structure. Peatland (grey boxes) and white sand (white boxes) habitats are paired over each structural variable...... 36

Figure 4. Relationships between vegetation structure (PCA 1), species richness, biogeographic diversity (FDis), and community weighted means (CWM) of family NMDS scores of peatlands (top row) and whitesands (bottom row). R-squared and p values are derived from simple linear regressions...... 38

Capítulo III

Figure 1. The 250-km stretch of the main drainage tributary of the southern Peruvian Amazon where focal peatlands (black) are located. Inventoried peatlands are outlined. Peatland names (from west to east; Table 3) are COLO, CICRA, HUIT 1, HUIT2, LAGA, MERC, and BOLI. The inset map shows the location of the 76 plots obtained from the Gentry transect data in relation to the peatland study area. Black and gray triangles represent Gentry sites at elevations greater than and less than 1000 masl, respectively. The shaded area corresponds to the Chocó region included in the supporting analysis (See section 4.1.1)...... 53

Figure 2. Scatter plot of actual and expected elevations for 76 training sites (open circles) obtained from the Gentry transect data and seven peatland test sites (solid circles). Expected elevations are based on abundance-weighted averages of family-level elevational optima after deshrinking (See section 2.4). Scatter plots based on family presence/absence data show qualitatively similar patterns. Based on a cross-validation procedure used to obtain p values, peatlands appears to occur at significantly higher elevations due to a greater abundance and number of families with higher elevation optima (Table 3)...... 59 xii

Figure 3. Elevational distributions of 40 indicator genera on peat and mineral substrates. Box plot hinges extend only to the first and third quartiles. Within respective substrate types taxa are ordered by their mean elevation represented by a darkened band. The dashed vertical line at 658 m marks the mean of average elevations of all genera...... 61 1

Introdução Geral

A água, em sua quantidade, energia, química, sazonalidade e fonte, influencia um dos padrões de distribuição de espécies vegetais mais consistentes em escala local, regional e continental (Gentry, 1988; Casanova and Brock, 2000; Engelbrecht et al., 2007; Junk et al., 2011). Na Bacia Amazônica, a baixa inclinação topográfica e a alta precipitação anual interagem na formação de uma ampla variedade de habitats de áreas úmidas. Estimativas indicam que as áreas úmidas – áreas sujeitas à inundação temporária ou permanente – cobrem uma área que corresponde a um quinto a um terço da área da bacia Amazônica (Junk et al., 2011). Os corpos de água são responsáveis para uma grande parte da heterogeneidade de habitats na paisagem Amazônica (Mertes et al., 1995; Hess, 2003; Hamilton et al., 2007; Householder et al., 2012), promovem um elevado grau de endemismo ecológico nas espécies vegetais, e abrigam a mais rica flora das áreas úmidas do mundo inteiro (Kubitzki, 1989; Wittmann et al., 2006, 2013). Apesar disso, as áreas úmidas raramente são consideradas em teorias modernas de biodiversidade da região Amazônica (Salo et al., 1986; Dumont et al., 1990; Junk e Piedade, 2004).

Entre as áreas úmidas Amazônicas, o conhecimento científico concentra-se às áreas periodicamente alagáveis (várzea e igapó), enquanto o conhecimento sobre as áreas permanentemente inundadas (buritizais) é limitado. Enquanto a importância das áreas Amazônicas pantanosas é cada vez mais reconhecida pelo seu papel no ciclo de carbono global (Lähteenoja et al., 2012), a manutenção da diversidade biológica (Brightsmith and Bravo 2006; Householder et al., 2010; Tobler et al., 2010; Marshall et al., 2011), dinâmica local da água (Kelly et al., 2014), economia e saúde humana (Padoch, 1988; Hiraoka, 1999), e o entendimento sobre a vegetação e ambientes no passado (Roucoux et al., 2013; Householder et al., 2015), o conhecimento básico sobre a composição de sua vegetação ainda é escasso.

Áreas permanentemente inundadas da Amazônia muitas vezes abrigam florestas mono-dominantes ou savanas inundadas caracterizadas pela presença da palmeira do gênero Mauritia (buriti, Spruce, 1871; Junk and Furch, 1993; Kahn et al., 1993). Por causa de sua dominância em vastas áreas da bacia Amazônica, ter Steege et al. (2013) recentemente classificaram o gênero Mauritia como “hiper-dominante”. A extrapolação de dados locais deste estudo sugere que as áreas permanentemente inundadas por Mauritia (buritizais) cobrem 2

uma extensão entre 2-3 milhões de hectares na bacia Amazônica, e que a população de Mauritia conta com uma quantidade de cerca de 1.5 bilhões de indivíduos (ter Steege et al., 2013). Os buritizais ocorrem de forma disjunta entre as florestas de terra firme ou florestas periodicamente alagáveis (Householder et al., 2012). Excluído da maioria dos programas dos inventários florestais, este habitat Amazônico é paradoxalmente um dos menos estudados, apesar do seu ubiquidade. Assim, a presente tese apresenta a soma dos resultados de pesquisa exploratória que foi realizada para o descobrimento, identificação, descrição, catalogação, e biogeografia ecológica da composição e diversidade florística nos buritizais Amazônicos.

Fazendo uso das condições abióticas extremas (inundação permanente) juntamente a ampla distribuição, a presente tese especificamente direciona as questões para a diversidade da vegetação lenhosa e a composição de espécies dos buritizais em ampla escala espacial. Enquanto a ecologia moderna tradicionalmente explica a variação da diversidade e composição de comunidades em função de processos em escala local (Ricklefs, 2008), o principal objetivo desta tese visa o entendimento dos padrões de estrutura das comunidades de vegetação do ponto de vista evolucionário e biogeográfico. Neste contexto, a tese procura abordar os padrões de vegetação dos buritizais integralmente nos processos evolucionários, biogeográficos e geológicos que influenciaram as paisagens Neotropicais durante milhares de anos (e.g., Hoorn et al., 2010), para entender como estes processos históricos de ampla escala resultaram nas comunidades permanentemente inundadas (Ricklefs, 2008; Wiens, 2011). Postula-se que a análise dos padrões taxonômicos, filogenéticos, e da estrutura biogeográfica gera uma nova perspectiva sobre como estas (e outras) comunidades na região Amazônica foram formadas durante o tempo ecológico e evolucionário.

A tese se divide em três capítulos. Capitulo 1 é a base para os outros, porque combina uma série de análises exploratórias da íntegra da base de dados levantados, incluindo 28 sítios em buritizais na Amazônia peruana (sete sítios) e brasileira (21 sítios). Este capítulo analisa a resposta da comunidade dos buritizais aos fatores abióticos extremos, considerando a estrutura taxonômica, filogenética e biogeográfica em comparação com a vegetação de florestas de terra firme.

As análises do capitulo 1 revelaram que localmente, as comunidades de plantas ocorrendo nos buritizais demonstram uma diversidade biogeográfica maior do que as comunidades de plantas em florestas de terra firme. O capitulo 2 aborda este padrão com mais detalhe com base em hipóteses. Especificamente, uma série de argumentos ecológicos e 3

evolucionários é abordada para explicar que táxons (e os seus atributos ecológicos) que ocupam habitats extremos (por exemplo, sítios onde as condições ambientais contrastam fortemente das condições predominantes na bacia Amazônica) não são compartilhados com as florestas adjacentes que predominam a paisagem Amazônica, mas tem origens biogeográficas e afinidades mais amplas. Esta hipótese é testada ao longo de dois gradientes fisionômicos similares, turfeiras e florestas sobre areia branca, em quais Mauritia é o componente principal da vegetação.

O capitulo 3 usa conceitos similares aos capítulos anteriores, e mostra como o conhecimento da composição florística dos buritizais pode ser utilizado na ciência aplicada, especificamente na interpretação de dados palinológicos e a reconstrução da temperatura no passado.

Objetivos

1. Inventariar e descrever a diversidade florística em buritizias na Amazônia peruana e brasileira. a. Prover coleções das espécies em buritizais e incorporar em herbários locais. b. Prover acesso livre aos dados geo-espaciais, florísticos, ecológicos e das imagens das coleções botânicas levantadas no presente estudo, utilizando o

ATRIUM Biodiversity Information System (http://atrium.andesamazon.org/) 2. Comparar as comunidades de vegetação dos buritizais considerando sua estrutura taxonômica, filogenética e biogeográfica com outros tipos de habitats adjacentes para responder as seguintes perguntas:

a. Estão as assembleias de buritizais compostas por um conjunto previsível de táxones? b. Estão as assembleias de buritizais restringidos filogeneticamente? c. Quais são os padrões biogeograficosdo dos táxones dos buritizais e como diferem dos táxones da terra firme? d. Como as relações biogeograficas dos táxones que co-occorem localmente mudam ao longo de gradientes ambientais? e. Como alteração nas relações biogeográficas em assemblieas dos buritizais podem infuir inferência paleo-ecológica?

Capítulo 1

Householder, J.E.; Janovec, J.P.; Tobler, M. & Wittmann, F. 2015. Patterns of taxonomic, phylogenetic, and biogeographic structure of Mauritia-dominated wetlands in the Amazon region. Manuscript prepared for Journal of Vegetation Science

Patterns of taxonomic, phylogenetic, and biogeographic community structure of Maurita-dominated wetlands in the Amazon region

Abstract

Questions Mauritia-dominated wetlands (MDWs) – an extreme abiotic environment in the Amazon region - are characterized by near-permanent waterlogging and compositional uniformity of a single canopy dominant. To gain a more complete understanding of the ecological and evolutionary processes driving vegetation assembly in this common Amazonian habitat we compare the woody vegetation of MDWs to that of lowland terra firme forest using a combination of taxonomic, phylogenetic and biogeographic analyses.

Location The Amazon

Methods We use dissimilarity metrics to examine compositional turnover of trees and shrubs within and between MDWs and terra firme habitats. We use taxonomic distinctness to assess differences in the degree of evolutionary relatedness amongst locally co-occurring individuals and species among habitats. We use ordination methods to examine differences in compositional patterns among habitats with respect to biogeographically-defined floristic groups (sensu Gentry).

Results Relative to terra firme, MDWs were characterized by high site-to-site compositional variability of trees and shrubs. Taxonomic distinctness is highly variable in MDWs, but co- occurring species tend to be, on average, more distantly phylogenetically related than species in terra firme forest. Proportionally more stems and species in MDWs correspond to plant lineages possessing extra-Amazonian centers of distribution and richness than in plots in terra firme forest.

Conclusions High site-to-site compositional variability is consistent with individualistic species response to multiple stress gradients and a diversity of successional pathways in waterlogged environments as well as dispersal limitation among disjunct habitat patches. Patterns of community phylogenetics indicate that habit-use of MDWs is widespread among phylogenetically diverse taxa from Amazonian forests, consistent with environmental filtering of convergent traits. The relative predominance of taxa presenting extra-Amazonian distributions in MDWs in comparison to terra firme forest indicates that a diversity of biogeographic origins or affinities may provide these extreme wetland communities with a source of ecologically differentiated taxa more tolerant to local site conditions.

Keywords: monodominant; peatland; Neotropics; swamp; waterlogging

Introduction

Extended periods of waterlogging alter the availability of nutrients and soil oxygen to plants, and the type and concentration of phytotoxins (Parolin et al., 2004). Consequently, wetland plants are typically confronted with multiple abiotic stressors associated with inundation that are, for the great majority of vascular plant species, detrimental to growth and development. Because species differ considerably in their ecophysiological response to soil waterlogging, hydrological pattern is a major determinant of plant species distribution and assemblage composition (Junk et al., 2011).

In the Amazon, sites demonstrating near-permanent waterlogging are often dominated by Mauritia L.f. (Arecaceae) palms (Kahn, 1988; Junk et al., 2011). Including two Amazonian species, Mauritia flexuosa L.f. and Mauritia carana Wallace ex Archer, these palms are a principal component of freshwater swamps and waterlogged savannas throughout the Amazon basin (Kalliola et al., 1991; Lähteenoja and Page, 2011; Householder et al., 2012). They are collectively called aguajal in Peru, buritizal in Brazil, cananguchal in Colombia, morichal in Venezuela and morital in Ecuador (Kahn, 1991) . According to fossil evidence MDWs have likely been a dynamic feature of the northern South American subcontinent since at least the Paleocene (Rull, 1998). Today, they are increasingly recognized to play important roles in the global carbon cycle (Lähteenoja et al., 2012), the maintenance of biological diversity (Brightsmith and Bravo 2006; Householder et al., 2010; Tobler et al., 2010; Marshall et al., 2011), local water dynamics (Kelly et al., 2014), human economies and health (Padoch, 1988; Hiraoka, 1999), and our understanding of past vegetation and environments (Roucoux et al., 2013; Householder et al., 2015).

Despite their relevance to local and global societal concerns, the literature describing MDW vegetation communities is relatively scant (Endress et al., 2013; Pitman et al., 2014). Traditionally, studies have tended to emphasize two prominent and related features: (1) the tendency towards canopy mono-dominance of a handful of predictable specialist tree species and (2) a strong reduction in species diversity of woody vegetation relative to surrounding non-inundated forests. These emergent patterns are traditionally ascribed to the difficult site conditions that select species on the basis of their tolerance to waterlogging. Consequently, many features of species inhabiting MDWs (and other extreme wetland sites) are often purported to be adaptations evolved in response to flooded conditions (Parolin et al., 2000; 8

Parolin et al., 2004). However an understanding of which traits, how they evolved, and how they determine species distributions along complex hydro-edaphic gradients remains elusive (Wittmann et al., 2013; Pitman et al., 2014).

In this paper we present a novel dataset regarding quantitative vegetation surveys of 28 MDWs widely distributed across the Peruvian and Brazilian Amazon region. So as to gain a fuller understanding of the response of local MDW assemblages to the severe environmental constraints, we compare these waterlogged habitats to terra firme using a combination of taxonomic, phylogenetic and biogeographic analyses. We ask the following questions: (1) Relative to terra firme, are MDWs comprised of a predictable set of common tree and shrub taxa across a broad geographic range? (2) How do patterns of evolutionary relatedness amongst locally co-occurring species differ between MDW and terra firme forests? (i.e., are traits conferring habitat-use of MDWs phylogenetically conserved, thus assembling more closely related species?) (3) What biogeographic trends do MDW tree and shrub taxa demonstrate and how do these differ from trends in terra firme forest taxa? We argue that taken together, answers to these questions can lead to novel insights regarding the ecological and evolutionary processes that influence the diversity and compositional patterns of this common Amazonian habitat.

Methods

Vegetation Sampling We obtained quantitative data on vegetation of terra firme forests from an extensive vegetation plot network compiled by Alwyn Gentry and maintained by the Missouri Botanical Garden (Phillips and Miller, 2002). The Gentry transect data are based on a standard sampling method used across an extensive geographic area. Data were collected in 0.1-ha plots consisting of 10 contiguous 100 m2 (2 x 50-m) linear subplots where all woody individuals ≧ 2.5 cm DBH were recorded, including trees, shrubs and lianas (Table 1). Sequential subplots were placed end to end and oriented in random directions. We extracted data only from non-inundated sampling sites located in the Amazon region (Bolivia, Colombia, Ecuador, Peru, and Venezuela) with elevations <500 masl. A total of 35 sites met our criteria (Figure 1). The accuracy of species names provided in the dataset was assessed by cross-referencing voucher specimen numbers provided in the original dataset with current determinations of collections stored at the Missouri Botanical Garden and accessible through 9

the Tropicos database (http://www.tropicos.org). Most species have been identified to genus, however, many morphospecies concepts remain and these have not been standardized across sites. Species of Bamboo (Poaceae) were removed from analysis.

Figure 1. Map of MDW and terra firme sites examined in this study.

Quantitative data on the woody vegetation of MDWs was collected at 28 different sites in the Peruvian and Brazilian Amazon (Figure 1). Because MDWs have variable spatial extents and can become structurally so much smaller than terra firme forest, it was necessary to adapt standard sampling methods of terra firme forests in order to obtain representative samples of MDW woody vegetation. In MDWs woody vegetation can be lower-statured and reach reproductive size at much smaller stem diameters than in surrounding terra firme forest. In the most extreme sites many reproductive individuals may not even reach minimum dbh thresholds used in the most common standard vegetation sampling protocols (i.e., 2.5 cm or 10 cm). Furthermore, in extremely shrubby sites, the high density of small-stemmed individuals can become prohibitively time consuming to count. As a result of these features of MDW vegetation, we opted to modify standard minimum dbh criteria and sample shrubby 10

individuals in nested subplots of reduced size. The number of subplots used to sample individual sites also varied according to MDW size and occasionally, logistical difficulty (i.e., unsafe or impassable ground conditions). Table 1 summarizes important methodological differences between MDW and terra firme datasets.

Vegetation data of MDWs, including trees, shrubs and lianas, were collected in 0.18 – 0.4 ha plots consisting of 100 m2 nested subplots placed at ~100 m intervals following straight-line transects (Table 1). In MDWs located in Brazil, trees (dbh >10 cm) were sampled in linear 100 m2 (50 x 2-m) subplots. Shrubs, defined as woody vegetation with dbh <10 cm and height >1 m were sampled in nested 25 x 2 m subplots positioned in the center of its companion tree subplot. In Peruvian MDWs the same criteria for tree and shrub classes were maintained but sampled in square 100 m2 (10 x 10-m) and nested 5 x 5-m subplots, respectively. Species abundances at each MDW site were calculated as the total number of stems of each species in both tree and shrub nested subplots at each site. Voucher specimens were collected for all species. Fertile Peruvian specimens are deposited in the herbaria of the Botanical Research Institute of Texas (BRIT), the La Molina University Forestry Herbarium (MOL) and the San Marcos Museum of Natural History (USM). Fertile Brazilian specimens are deposited in the Herbário do Instituto Nacional de Pesquisas da Amazônia (INPA). Sterile specimens of all species are stored in MOL and INPA in Peru and Brazil respectively. All metadata and annotation history, as well as associated images from the field and herbarium are openly available through the Digital Herbarium of the Andes-Amazon Atrium Biodiversity Information System (http://atrium.andesamazon.org/index.php) under the project entitled "Aguajal Project".

For both terra firme forest and MDWs, species were identified to at least genus level. However, a number of morphospecies concepts remains and these have not been standardized across all sites. Consequently, comparisons among sites are restricted to genus and family ranks.

Table 1. Summary of the primary methodological differences between the Gentry plot data used to characterized terra firme forest and the MDW protocols.

Protocols Terra Firme MDW

Minimum inclusion Dbh < 2.5cm Height < 1m criteria

100m2 (trees) + 25m2 Plot size 100m2 (shrubs) Continuous lines Discontinuous plots, along oriented in random Plot arrangement straight-line transects directions

Square (Perivian sites) or Plot shape Linear Linear (Brazilian sites)

Plots per site 10 18-40 Total sites 35 28

Sites in terra firme and MDWs are widely distributed across the Amazon basin. Because differences in composition are expected to occur as a function of geographic distance we evaluated potential differences in the spatial distributions among sites between the two habitat types. This was accomplished by comparing the Euclidean distances of individual sites to their habitat group geographic centroid, the x-y position of which was calculated as the mean longitude and latitude of sites within each group (Anderson et al., 2006). A t-test was used to assess potential differences in the spatial extent of sampling among habitats.

MDWs are most readily distinguished by the relative dominance of a single species of aborescent palm, but specific thresholds to delimit the boundaries of what constitutes Mauritia dominance are not established and may vary among individual investigators. To quantitatively asses differences in the distribution of aborescent palms across terra firme forest and MDW sites in our dataset we used dbh > 10 cm subsets of the Gentry and MDW data to compare the relative proportion of palm stems (dbh > 10 cm) to the total number of tree stems (dbh > 10 cm). All other analyses were done including both trees (dbh > 10cm) and shrubs (dbh < 10cm) combined.

Compositional Variability

To examine the extent to which MDWs are comprised of a predictable set of common taxa we employed a series of comparative beta-diversity analyses. First, we examined 12

differences in the frequency distribution of genera and families in MDW and terra firme sites. We used Wilcoxon rank sums tests to asses differences in the frequency distribution of genera and families between MDW and terra firme forest. Terra firme was restricted to 28 random sites.

In a separate analysis, patterns of pairwise dissimilarities within and across MDWs and terra firme habitats were examined using abundance and presence-absence site by taxa matrices at both genus and family ranks. Dissimilarities were partitioned into separate turnover and nested components (Baselga, 2010) and differences within and between habitats examined visually due of the lack of independence between individual observations. To explicitly test for differences in compositional variation within MDW and terra firme habitats we employed a multivariate dispersion test, assessing the compositional distances of individual sites to their habitat group centroid in multivariate space using Bray-Curtis and Sorenson dissimilarities for abundance and presence-absence data, respectively (Anderson et al., 2006).

Phylogenetic Structure of MDWs

We examined patterns of community structure across MDW and terra firme sites with respect to a taxonomic hierarchy using the taxonomic distinctness metric of Clarke and Warwick (1998). Taxonomic distinctness (D*) is defined as the average evolutionary distance between any two individuals, conditional on them being from two different species. In the case of presence-absence data, taxonomic distinctness (D+) is defined as the average evolutionary distance between any two species. An attractive property of these indices is that they remove much of the overt influence of large differences in species abundance distributions and are robust to differences in richness and sampling effort (Clarke and Warwick, 1998). Relative differences in taxonomic structure across MDW and terra firme were assessed using t-tests.

A single taxonomic hierarchy including species from both terra firme and MDW transect data was created using genus, family, order, and superorder ranks in accord with Stevens (2015). To evaluate the contribution of higher and lower taxonomic ranks separately, the analysis was repeated while compressing the hierarchy to its two higher (orders and superorders) or lower (families and genera) rankings (Clarke and Warwick, 1999). Our main assumption in using a a taxonomic hierarchy is that taxonomic categories will, on average, reflect natural phylogenetic and morphological variation across taxonomic groups and species 13

(Robeck et al., 2000; Sepkoski and Kendrick, 1993). While clearly artificial constructs representing varying amounts of genetic and ecological differentiation, many classic plant taxonomic ranks (i.e., genera and families) have been largely confirmed to demonstrate monophyly and phylogenetic reality (Sepkoski and Kendrick, 1993; Robeck et al., 2000; APG, 2003).

Biogeographic Structure of MDWs

Based on the regional distribution patterns of species richness of the most important neotropical plant families Gentry (1982) distinguished 5 floristic groups: (1) Amazon- centered (2) Andean-centered (3) Laurasian (4) Southern Andean/South Temperate and (5) Dry. Gentry also proposed a small group of Guyana-centered taxa that had no representatives within the woody vegetation of our combined data. We acknowledge that modern advances in phylogenetics and the historical biogeography of lineages certainly offer potential to reevaluate some of Gentry’s initial origination hypotheses (e.g., Antonelli et al. 2009). However variation in richness patterns of lineages at large spatial scales are increasingly understood to be the result of niche differences playing out on ecologically heterogeneous landscapes over evolutionary time (Gentry, 1982; Crisp et al., 2009; Antonelli and Sanmartín, 2011). Expected correspondence between biogeographic pattern and the ecological niche suggests that regardless of interpretations concerning origination, Gentry’s classic groups may be useful indicators of highly conserved niche differences amongst the most important Neotropical plant families. Furthermore, in our analysis, groups 2-5 (non-Amazonian families) tend to show broadly similar qualitative pattern. Thus minor rearrangements among groups are not likely to alter our main results. As such, in the absence of a more modern synthesis of the regional patterns demonstrated by Gentry we have opted to use his original grouping with few alterations (see Appendix A).

To examine differences in the biogeographic patterns of co-occurring taxa in MDW and terra firme communities each species was assigned to one of the five major Neotropical floristic groups and the proportion of stems and species pertaining to each floristic group was calculated for each site. Species from families not considered by Gentry were removed from analysis. The resulting 5 vectors describing the distribution of stems and species among floristic groups were fitted onto a two-dimensional NMDS solution of the community site x taxa matrix in order to visualize distribution pattern of each floristic group with respect to compositional variation among sites. Differences in the variability of biogeographic relations 14

amongst locally co-occurring stems and species in terra firme and MDW habitats were assessed using the Simpson’s diversity metric.

Results

Distances from individual sites to their group centroid in geographic space revealed that sampling of both MDWs and terra firme was more or less equally widespread geographically (t =0.0038, p =0.997). The mean distance from individual MDW and terra firme sites from their respective group centroids were nearly equal at ~7.27 degrees. A total 22,514 stems were sampled in 28 MDWs, distributed among 318 genera and 89 families. In terra firme, 12,913 stems distributed among 605 genera and 113 families were sampled in 35 site.

As expected, MDW and terra firme habitats demonstrated divergent patterns in palm density (Figure 2). Mauritia accounted for, on average, 61% of all woody stems >10 cm dbh 15

and 89% of all palms (> 10 cm dbh) in MDWs. Only five other palm species reaching dbh >10 cm were present in the surveyed MDW plots, the most frequent being Euterpe precatoria and Mauritiella armata. In terra firme sites Mauritia accounted for only 4 individuals in a single plot, representing <1% of woody stems >10 cm dbh at this site. A total of 28 other palm species attaining dbh >10 cm were present in terra firme sites, the most frequent of which were Iriartea deltoidea, Oenocarpus bataua, and Astrocaryum sp.

Compositional Variability

The frequency distributions of taxa among MDW and terra firme sites differed, considering both genus (Wilcoxon rank sum test: W = 7572, n1 =n2 =28, p <0.01) and family ranks (W = 3795, n1 = n2 = 28, p >0.01). On average, genera and families tend to occur in proportionally fewer MDW sites relative to terra firme sites. For example, considering 28 sites in both habitat types, the average genus occupies 3.8 (median = 2) sites in MDWs and 5.4 (median = 3) sites in terra firme. Similarly, the average family occupies 8.7 (median = 7) and 12.7 (median = 11) sites in MDWs and terra firme respectively. Appendix A shows frequency distributions of taxa sampled in MDWs.

Multivariate dispersion tests revealed compositional variation across sites within MDW woody vegetation to be generally greater than terra firme. Habitat differences in genus level compositional variation were stronger for presence-absence data (F =30.2, p <0.001) than for abundance data (F =5.74, p =0.02). Differences in family level compositional variation were equally strong for both presence-absence (F =49.55, p <0.001) and abundance data (F =49.44, p <0.001). Examination of pair-wise dissimilarities partitioned into turnover and nestedness components further highlighted differences in compositional variation amongst habitats. The mean value of pair-wise dissimilarities within MDW habitat approached that of the mean of pairwise dissimilarities between MDW and terra firme, whether analyzed at family or genus rank (Figure 3a & d). MDWs exhibited proportionally greater nested structure than terra firme (Figure 3b & e), but this accounted for a smaller fraction of total beta-diversity relative to turnover (Figure 3c & f), and the degree of nestedness rapidly decreased with decreasing taxonomic rank (i.e., from family to genus).

Phylogenetic Structure

MDW plots tend to demonstrate high variability in taxonomic distinctness indices relative to terra firme plots (Figure 4). T-tests revealed that values for D* are consistently higher in MDWs regardless of which level of the taxonomic hierarchy was considered (p 16

<0.01). For D+, the range of values for MDWs consistently encompasses both the maximum and minimum values of all sites. Especially when deeper taxonomic ranks are considered MDWs tend to show, on average, reduced D+ values, however these were not significantly different from terra firme (p > 0.01 in all cases).

Figure 3. Box plots of pair-wise dissimilarities within and between MDW and terra firme sites at family and genus taxonomic ranks for presence-absence data. Dissimilarities are additively partitioned between nested and turnover components following Baselga (2010). Dissiilarities based on abundance data are qualitatively similar and not shown.

Biogeographic Structure

In an ordination of plots based on a two-dimensional solution with a stress of 0.21, the primary axis of variation reflected strong differences in composition between MDWs and terra firme at genus and family taxonomic ranks (Figure 5, only family-level is shown). The main axis of variation is strongly associated with a contrast between Amazonian-centered families (sensu Gentry) and non-Amazonian plant families, both in terms of the relative site stem abundance and richness of each floristic group within sites. In general, non-Amazonian plant families tend to contribute proportionally more stems and species in MDW sites 18

compared to terra firme sites, which are decidedly dominated by Amazonian-centered families. The the greater proportion (p <0.05) of the South Temperate floristic group in (b), but not (a), suggests that species of this group can become equally abundant in both MDW and terra firme (e.g., Myrtaceae can be an important shrubby component of terra firme), but contribute proportionally more to site richness in MDWs. Subsequent t-tests comparing Simpson’s diversity metric of floristic groups among habitats revealed elevated diversity of biogeographic relations in MDW communities relative to terra firme, both in terms of the number of individuals (p <0.001), and the number of species (p <0.001).

Figure 5. Two-dimensional NMDS solution of compositional data at the rank of family. Significant (p >0.05) vectors corresponding to the number of stems (left) and species (right) of each floristic group sensu Gentry(1982) were mapped onto the ordination. At the family level, almost half of the dissimilarity between MDW and terra firme is due to a nested structure (see figure 3b). However the relative contribution of nestedness to between-habitat compositional differences decreases rapidly with decreasing taxonomic rank (see figure 3e). Qualitative patterns of site and floristic group distributions are similar regardless of whether family or genus ranks, or abundance or presence-absence data is used.

Discussion

In sites where Mauritia palms are canopy-dominant, two environmental factors can almost always be predicted; substrates are near-permanently saturated and vertical water-level fluctuation are, in our experience, <2 m over an annual cycle. During community assembly extended waterlogging and associated stresses are known to be strong filtering mechanisms 19

that limit local communities to a handful of species possessing the appropriate attributes. Our results accord with this general view in the sense that MDW sites demonstrated reduced species richness. However, with the intent to deepen our understanding of ecological and evolutionary processes determining community structure in MDWs, we document and discuss three further patterns that have emerged from our analyses: (1) that MDWs exhibit high site- to-site variability, (2) that the ability to grow in MDWs appears to be a trait widely distributed in the phylogeny of Amazonian forests, and (3) MDW communities are characterized by taxa with centers of richness in extra-Amazonian regions.

Composition of MDWs exhibits high site-to-site variability

According to our data, on broad spatial scales MDWs can be as compositionally different to each other as they are to terra firme (Figure 3a). With the exception of the canopy dominant - present at all sites by methodological design - there appears to be little predictability in MDW vegetation composition when contrasted with terra firme, the latter habitat type appearing to be comprised of a much more predictable set of common taxa across broad spatial scales (e.g. Pitman et al. 2001; Macía and Svenning 2005). While several taxa widely recognized as common swamp specialists were frequently found (e.g. Calophyllum, Tapirira, etc.), their overall influence on beta-diversity metrics examined here are dwarfed by a multitude of less frequent taxa.

The high site-to-site spatial variability found here accords with other broad-scale comparisons of MDWs (Pitman et al., 2014) as well as paleoecological records that demonstrate abrupt temporal variation in composition and a diversity of developmental pathways (Lähteenoja and Page, 2011; Roucoux and Baker, 2012). Mauritia appears to be an exceptionally effective colonizer of waterlogged sites, tolerating a broad spectrum of environmental conditions associated with near-permanently saturated conditions. For example, edaphic conditions in our MDW plots varied from pure clay to pure sand or peat. Water depths at the time of visit ranged from just below ground surface to approximately two meters. Fire, to which adult individuals of Mauritia are resistant, was also a common disturbance in many MDWs. Any of these factors, even within single sites, individually or in combination, were observed to change frequently and abruptly, imposing observably strong filters on forest structure and composition. Consequently, the high spatial variability in MDW community composition likely involves the individualistic responses of species to multiple complex gradients associated with flooding. As a result of the habitat’s patchy spatial 20

organization, dispersal, immigration, and extinction processes may also be more variable in MDWs. These spatial processes are also likely to further contribute to high site-to-site compositional variability (MacArthur and Wilson, 1967; Leibold et al., 2004).

Habitat-use of MDWs is a trait widely dispersed in the phylogeny of Amazonian forests

Taxonomic distinctness varied with respect to the level of taxonomic information supplied as well as the degree to which species abundance distributions were taken into account. The range of taxonomic distinctness measures for MDWs often included both maximum and minimum values, however it is not clear the extent to which this is simply a matter of increased variability due to reduced species richness (Clarke and Warwick, 1999). There is a tendency for co-occurring species in MDWs to be, on average, more taxonomically distant than co-occurring species in terra firme, and significantly so when D* is considered.

We conclude that many phylogenetically unrelated species have converged on similar habitat use and that the traits conferring the ability to survive on permanently waterlogged substrates are widespread in the phylogeny of Amazonian forests. We find little evidence to suggest that severe ecological filters clump phylogenetically related species during assembly of MDW communities. We maintain that while permanent waterlogging strongly modifies the structure of MDW communities by constraining the number species that locally co-occur, it does not restrict the phylogenetic tree of its community.

Extra-Amazonian taxa characterize a common Amazonian habitat

The biogeographic patterns of lineages are determined by the balance of speciation, extinction, and dispersal processes as they occur on an environmentally heterogeneous template (Rosenzweig, 1995; Roy et al., 2009; Wiens, 2011). Correspondence between the biogeographic history of a lineage and ecological traits (Gentry, 1982; Williams-Linera, 1997) suggests that large-scale biogeographic pattern may result principally from deterministic ecological processes acting on phylogentically conserved traits that regulate the abiotic and biotic conditions in which individuals can disperse, establish and reproduce at local scales (Crisp et al., 2009).

With this in mind, we suggest that a diversity of biogeographic relations may provide a source of ecologically differentiated taxa for the assembly of local MDW communities (Ackerly, 2003; 2004). Near-permanent waterlogging provokes severe alterations in the 21

immediate abiotic environment through changes in oxygen supply to roots, the bioavailabity of resources, and introduces numerous other associated stresses. If the species (and their associated traits) that colonize these altered sites do not already exist within local pools, they must either evolve from those species already existing in situ or be recruited from species pools where these traits already exist. Consequently, we propose that severe shifts in predominating ecological filters imposed by local waterlogging may heavily modify the pool from which MDW assemblages tend to be recruited.

Our interpretation accords with several ecological and floristic studies noting that many of the most typical Amazonian wetland taxa and communities possess atypical functional trait values and extra-Amazonian distribution patterns (Prance, 1979; Kubitzki, 1989; Burnham et al., 2001; Wittmann et al., 2013; Householder et al., 2015). Our analyses suggest that evolutionary stasis and habitat tracking of a deeply conserved niche - perhaps associated with stress in general - may also help explain the ‘fit’ of wetland organisms to their semi-aquatic environments and should be considered in tandem with hypotheses emphasizing adaptive processes.

Acknowledgments

The manuscript was developed and written with funding provided to the corresponding author by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ-141727/2011-0). Field work was made possible by funding from CNPQ (Universal grant no. 475660/2011-0), the Discovery Fund of FortWorth, Texas, the Gordon and Betty Moore Foundation (grant no. 484), the U.S. National Science Foundation (grant no. 0717453), and the Programa de Ciencia y Tecnologia—FINCYT (grant number PIBAP- 2007–005). We thank Maria Teresa Fernandez Piedade and the MAUA working group for providing logistical support. We thank Sy Sohmer, Cleve Lancaster, Pat Harrison, Keri Barfield, Renan Valega, Jason Wells and Will McClatchey, and the general staff of the Botanical Research Institute of Texas (BRIT) for providing important institutional support and infrastructure. We thank Fernando Cornejo, Piher Maceda, Javier Huinga and Angel Balarezo for research assistance in the field. We thank various Peruvian institutions, including the Instituto Nacional de Recursos Naturales (INRENA), the Dirección General de Flora y Fauna Silvestre (DGFFS), the Ministerio de Agricultura (MINAG), and the Ministerio del Ambiente (MINAM) for research, collection, and export permits during the course of this 22

project. We also thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for permits, logistical support, and access to conservation areas in Brazil.

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Capítulo 2

Householder, J.E.; Janovec, J.P.; Tobler, M. & Wittmann, F. 2015. Shrubby sites are more biogeographically diverse than forested sites in two extreme Amazonian habitat types. Manuscript prepared for Journal of Biogeography

Shrubby Habitats are more Biogeographically Diverse Than Forested Habitats in Two Extreme Amazonian Habitat Types

Abstract

Aim Because the biogeographic patterns of plant lineages reflect the evolutionary constraints and conserved adaptations of their constituent species, examination of local communities within a biogeographic framework can provide novel insight into the ecological and evolutionary processes that structure them. Here, we examine patterns of biogeographic community structure of woody vegetation communities along physiognomic gradients in two extreme abiotic environments in the Amazon region.

Location Amazonia

Methods Making use of a publically available vegetation dataset we model distribution patterns of plant families within a geographic window spanning the Andes-Amazon elevational gradient. We apply this model to examine the variability of biogeographic relations amongst locally co-existing species along similar physiognomic gradients in two floristically independent and edaphically stressful habitats in lowland Amazonia - white sands and peatlands.

Results We find common patterns in both habitats. In forested sites, variation in the biogeographic relations of locally co-occurring taxa is low, becoming increasingly variable in sites with shrubby physiognomies.

Main Conclusions We propose that because forest ecosystems have featured prominently in the evolutionary history of lowland Amazonia many species well-suited to forested site conditions in peatlands and whitesands have evolved in situ, resulting in low observed variability in biogeographic diversity in forested sites. In contrast, higher observed diversity of biogeographic relations in shrubby habitat might be explained by both adaptive shifts of locally derived forest taxa as well as evolutionary conservatism and exaptation of taxa that have diversified in regions ecologically distinct from lowland Amazonia. Thus we suggest a high diversity of biogeographic histories may provide ecologically differentiated taxa for the colonization of environmentally extreme habitat types in the Amazon. We further suggest that our results provide an ecological basis that can contribute to our understanding of some outstanding features of biogeographic pattern in the Andes-Amazon region.

Keywords: Andes; community structure; habitat heterogeneity; heath; neotropics; peatland; swamp; white sand;

Introduction

The biogeographic history of a lineage is determined by the balance of speciation versus extinction events and dispersal processes as they occur on an environmentally heterogeneous template of regional to global proportions. Niche conservatism, the strong tendency to retain ancestral ecological characteristics, has been viewed as a useful guiding principle for understanding how these processes operating on large spatial and temporal scales result in biogeographic pattern (Roy et al., 2009; Wiens, 2011). For example, long-standing biome stasis of lineages is expected to result principally from deterministic ecological processes acting on conserved traits that determine the abiotic and biotic conditions in which individuals can disperse, establish and reproduce at local scales (Crisp et al., 2009). One prediction of the niche-conservatism framework is that heritable traits associated with the ecological niches of species mediate distribution patterns of taxa across geographic scales (local to global), conceptually linking the historical (i.e. dispersal, speciation and extinction) processes that shape large-scale macro-ecological pattern of entire lineages to local processes (i.e. habitat sorting and competition) that shape species distribution on smaller scales (Ricklefs and Latham, 1992; Roy et al., 2009; Wiens, 2011).

Most modern local assemblages are built up over time by members from lineages possessing disparate biogeographic legacies, thus providing testing grounds to better understand how local assemblages are influenced by the evolutionary and biogeographic history of their respective lineages. To the extent that locally co-existing species retain an ancestral niche adapted to disparate climatic and environmental contexts, we might reasonably expect extrinsic evolutionary processes to influence the local assembly of species as they are sorted along environmental gradients (Ackerly, 2004; Stephens and Wiens, 2009; Wiens, 2011). For example, in northern temperate forests, species from clades with tropical biogeographic affinities tend to break bud later than clades with entirely temperate distributions, presumably because delayed leaf flushing decreases potential losses caused by late, unexpected frosts (Lechowicz, 1984). The differential timing of bud break between tropical vs. temperate clades at local scales suggests that increased susceptibility to frost is an aspect of the tropical niche that has been highly conserved – even in lineages that have been able to break the tropical-temperature divide - and that biogeographic pattern of entire clades can be a predictor of the ecological behavior of constituent species (Harrison and Grace, 2007). 30

We develop a strategy to quantifiably examine vegetation assemblage structure within a biogeographic framework in two edaphically specialized lowland Amazon habitat types, white sands and peatlands. These patchily distributed Amazonian vegetation communities are notable for reductions in physical stature relative to surrounding tall and wet forests. Despite many descriptions of this classic physiognomic pattern (Kalliola et al., 1991), little is known concerning the origins and evolution of the species that occupy different positions along the physiognomic gradient. Strong species and trait turnover are expected, exemplified by the fact that free-standing woody plant forms have not evolved the adequate traits necessary for persistence in increasingly marginal sites. Considering that the occupation of increasingly stressful, shrubby habitats represents an increasingly large departure from the range of ecological strategies that has generally been successful throughout the evolutionary history of tall, closed-canopy rainforests, we might predict that many taxa in shrubbier environments (and their associated traits) will not be shared with the surrounding forests, but will have wider biogeographic origins and affinities. Thus we examine the biogeographic variability of local assemblages along the physiognomic gradient in two independent vegetation communities, peatlands and white sands, asking whether assemblages in more open-canopied and low-statured sites are more biogeographically diverse than those of forested sites.

Methods

Habitat Description and field sampling

Vegetated peatlands in the Amazon form in sites exhibiting perennially waterlogged substrates and minimal water level oscillations. Organic substrates derived from the biomass of plants growing in situ accumulate under hypoxic conditions induced by inundation (Page et al., 2011; Householder et al., 2012). No extensive mapping of modern Amazonian peatlands is currently available, but Ruokolainen et al. (2001) provide an initial basin-wide estimate of 150,000 km2 deduced from satellite imagery. The majority of these are expected to occupy the subsiding foreland basin region in the Western Amazon, although small patches exist throughout the basin (Draper et. al., 2014). The white-sand vegetation community occupies sites on nutrient deprived sands. Sandy soils are potentially well-drained, but episodic sheet flooding and/or high water tables may be present depending on local site conditions. White- sand habitat covers approximately 210,000km2 of the Amazon basin, the majority of which is found in the Rio Negro region in the Northern and Central Amazon (Ter Steege and Sabatier, 31

2000). Both habitat types have a distinctly patchy distribution pattern and are embedded within a matrix of tall, closed-canopy forests.

Peatland and white sand habitats were systematically sampled in Southwest and Central Amazonia respectively (Figure 1). Seven peatlands were sampled along a 250km lowland stretch of the Madre de Dios River meander belt in southeast Peru. Accumulation of thick peat (3 - 9 m in depth) and dominance of a single palm indicator species (Mauritia flexuosa) suggested relatively similar edaphic conditions characterized by perennial substrate saturation and limited water-level oscillations. Strong physiognomic transitions from low- statured swamp forest to herbaceous savannahs characterized most visited peatlands and are readily detectable in satellite imagery (Hamilton, 2005; Householder et al., 2012). Two white-sand habitats, spaced approximately 250 km apart, were located in the Rio Negro region (Jau National Park and Uãtuma Sustainable Development Reserve). Both possessed substrates with sand fractions exceeding 90% of total dry weight (mean ± sd = 94.4% ± 20; Householder unpublished data). Physiognomic transitions from low-statured forest to shrubland were present.

In peatlands, trees (dbh > 10 cm) were sampled in 10 x 10-m square plots. Shrubs, which we defined as woody vegetation with dbh < 10 cm and height > 1 m were sampled in nested 5 x 5-m plots positioned on the center of its companion tree plot. The same criteria for tree and shrub classes were maintained in white-sand sites, but plants were sampled in 50 x 2- m and 25 x 2-m nested plots, respectively. Variation in physiognomic and environmental conditions within plots was minimal. Total plot abundance of each species was estimated by summing the number of stems in both tree and nested shrub plots. Consecutive plots in both habitat types were placed at ~100 m intervals following straight-line transects in an attempt to capture the entire physiognomic gradient apparent at each site. Six structural variables, including percent coverage and height of tree, shrub and herb strata were visually estimated in each plot. Stem density of both trees and shrubs were tallied and included as additional structural variables. We surveyed 147 nested plots more or less equally distributed in the seven peatlands and 41 nested plots, also equally distributed among two white-sand sites.

Figure 1. Map showing locations of surveyed peatlands and white sands as well as the distribution of sites of the Gentry plot network used to assess distributional patterns of families along the elevation gradient. Boxed windows indicate the areas where peatland and white-sand communities were sampled. Gentry sites are classified into two groups differentiated by site elevation (see map legend).

Developing a Biogeographic Framework

We limit our geographic window to the Andes-Amazon region. Strong floristic turnover along the Andes-Amazon elevation gradient represents one of the most outstanding features of neotropical biogeography (Gentry, 1982; Hoorn et al., 2010; Antonelli and Sanmartín, 2011). Gentry (1982) classified the majority of the most important Neotropical plant families as either ‘clearly’ Amazonian or Andean according to the geographic distributions of constituent species, further noting the contrasting life-histories between these two biogeographically defined groups. Strong ecological filters are expected to select species on the basis of their tolerance to highly variable abiotic conditions along mountain slopes (Körner, 2007). As a consequence, morphological traits (Luo et al., 2005; Moser et al., 2007), and life history characteristics (Lieberman et al., 1996; Klimes, 2003) are non-randomly distributed. Because these tend to be evolutionarily conserved within lineages, more closely related species often have more similar elevational distributions, resulting in strong 33

phylogeographic structure along the Andes-Amazon elevation gradient (Gentry, 1982; Enquist et al., 2002; Punyasena et al. 2008). As such, we propose that a simple assessment of family-level elevation distribution provides a straightforward metric of the biogeographic pattern of taxonomic groups, as well as general predictor of species’ ecological behavior (Ackerly, 2003; Harrison and Grace, 2007; Punyasena et al., 2008).

To produce this metric we first collated a subset of the Gentry transect data maintained and made available through the Missouri Botanical Garden. Gentry transect data were collected in 0.1 ha plots consisting of 10 contiguous 50 x 2 m linear subplots where all woody individuals > 2.5 cm dbh were reported. Sequential subplots placed end to end were oriented in random directions. We only used plots from the Andes-Amazon region (Colombia, Venezuela, Ecuador, Peru, Brazil and Bolivia) including 80 sites at elevations ranging from 10 to 3200 masl. Sites located in semi-deciduous, dry forest, or savanna regions were excluded from the model. The accuracy of species determinations provided in the dataset was assessed by cross-referencing voucher numbers provided in the original dataset with current determinations of collections stored at the Missouri Botanical Gardens and made accessible through the Tropicos website (http://www.tropicos.org/Home.aspx). Taxonomic nomenclature was standardized to Tropicos (Stevens 2015) and merged at the taxonomic rank of family. Variation in plot composition of the Gentry dataset was condensed to a single ordination axis using non-metric multidimensional scaling and its correlation to elevation subsequently described by Pearson’s r. Distribution patterns of each family along this gradient were represented by a single parameter computed as the mean of site ordination values weighted by relative plot abundance of the family. As an independent check, we compared our results to the biogeographic hypothesis of Gentry (1982), with the expectation that Andean families would demonstrate higher weighted averages along the NMDS axis relative to Amazonian families. The resulting weighted average family elevation scores derived from the Gentry transect data were used as a quantitative measure of species’ biogeographic dissemblance within the peat and white sand datasets. Species of the same family were assigned the same score, reflecting their shared ancestry and biogeographic legacy.

Examining Biogeographic Variability

We used Functional Dispersion (FDis) as a metric of the variability of biogeographic relations within local peat and white-sand assemblages (Laliberté and Legendre, 2010). 34

Conceptually, FDis is the mean distance in weighted average elevation scores of species within plots to the centroid of all species. Samples of locally co-existing species possessing similar weighted-average elevation scores will have lower FDis values than those comprised of species with highly divergent scores. The metric is not influenced by species richness but does incorporate information on the abundance distribution by shifting the position of the centroid according to species relative abundances. To understand how FDis varies with physiognomy we used linear regression on the primary axes of a principal component analysis (PCA) performed on the correlation matrix of the eight structural variables measured in the field.

Results

We sampled 6,868 and 3,566 stems in peatland and white-sand habitat respectively. Comparison of the vegetation data at the generic level suggests that the two floras are taxomonically distinct. Of 205 genera identified, including both habitat types, less than one fifth (18%) are shared. A total of 76% (n=117) and 58% (n = 51) of genera in peatland and white sands were unique, accounting for 76% and 57% of species within each habitat type respectively. No species were shared between habitats.

Using the Gentry transect data we found a high correlation (r = .93, p < 0.001) between the single NMDS ordination axis (stress = 0.22) and site elevation. Weighted average elevation scores of families ranged from approximately -2 to +2. Families occurring in peatlands and white sands spanned the entire spectrum of families present in the Gentry transect data (Figure 2). Andean families (sensu Gentry [1982]) had significantly higher weighted averages than Amazon-centered families as revealed by a t-test (p > 0.001). In peatlands, species from Onagraceae (2 spp.), Chloranthaceae (1 sp.), Aquifoliaceae (2 sp.), Rosaceae (1 sp.), and Araliaceae (1 sp.) demonstrated the highest family elevation distributions. On white sands high elevation families were represented by species from Asteraceae (2 spp.), Aquifoliaceae (1 sp.), Pentaphyllaceae (3 spp.), Araliaceae (2 spp.) and Primulaceae (2 spp.). Combined, the top 15 high elevation families in peatlands and white sands represented 29% of all individuals and 18% of all species. The 15 families with the lowest weighted average scores accounted for 10% of all individuals and 9% of species. Andean and Amazonian families (sensu Gentry) accounted for almost equal fractions of individuals and species. All families present in the peatland and white-sand data, their 35

weighted average NMDS score, biogeographic classification according to Gentry (1982), and the numbers of species and stems are given in Appendix B.

Figure 2. Histogram of abundance-weighted average scores of families along the axis of the non-metric multidimensional scaling of the Gentry plots (white bars), illustrating the wide breadth of biogeographic patterns of families present in the peat and white-sand habitats (grey bars). The NMDS axis is highly correlated with site elevation (r = 0.93, p > 0.001), thus weighted-average scores describe the average relative position of families along the elevation gradient, where higher scores correspond to families with higher average elevational distributions.

Table 1. Loadings of the 8 variables used to describe vegetation structure on the primary axis of the PCA in peatland and white sand habitats. Loadings are highly correlated between habitats, and in both cases describe a transition from taller forested sites with reduced herbaceous layers to shrubby sites with increasing density of smaller- stemmed, low-statured individuals and a well developed herbaceous layer.

Loadings on first PCA axis Structural Variables Peatlands White sands

Count Shrub 0.453 0.634

Count Tree 0.278 -0.432

Cover Herb 0.339 0.384

Cover Shrub 0.269 0.681

Cover Tree -0.472 -0.438

Height Herb 0.196 0.356

Height Shrub -0.192 -0.412

Height Tree -0.48 -0.413 37

We observed strong physiognomic gradients in both habitat types, with tree, shrub, and herb covers ranging from 0 to almost 100% (Figure 3). Loadings on the primary axes of the structural variables were highly correlated between habitat types (r = 0.77, t = 2.837, df = 6, p = 0.02), describing similar transitions from tall forested habitats with shadier understories (decreased herb cover) to open-canopied shrublands with high understory light incidence (Table 1). Variation in tree stem density accounted for the principal structural difference between habitats. Relative to white sands, shrubby communities in the peatlands we studied tended to possess more stunted trees with larger stem diameters, likely due to the dominance of low-statured individuals of the arboreal palm Mauritia flexuosa in shrubby peatland sites. The forest-shrubland transition explained the majority (58%) of structural variation in white sand habitat and 32% in peatlands. Secondary axes were not interpretable and showed no associations with tested variables; thus we do not consider them further.

Peatland and white-sand communities showed divergent local richness patterns with forest structure (Figure 4). On white sands, local richness declined strongly with increasing shrubbiness, while a weak positive relationship with shrubbiness was found in peatlands. The structural gradients described by the primary PCA axis (forest-shrub transition) accounted for a significant proportion of variance in the diversity of biogeographic relations among co- existing individuals (FDis) in peatlands (r2 = 0.30, p <0.001) and white sands (r2 = 0.21, p<0.001). In both cases FDis tended to increase with increasing shrubbiness (Figure 4). Variation in biogeographic relations was positively associated with an increase in the community weighted mean of NMDS scores in both peatlands, and white sands. 38

Discussion

The strong tendency for families with lower weighted-average elevation scores, hereafter referred to as lowland families, to dominate in more forested sites is consistent with the long evolutionary history of forests in lowland Amazonia (Fine and Ree, 2006; Hoorn and Wesselingh, 2010). Because forest ecosystems have featured prominently in the evolutionary history of lowland Amazonia, we might expect them to have evolved many species well- suited to the predominating lowland environmental conditions (Pärtel et al., 2007). These species ultimately form the species pools from which forested communities are locally assembled, both in peatlands and white sands.

While tree growth forms are expected to dominate where resources are abundant and competition for light places a premium on vertical height (King, 1990; Koch et al., 2004), shrubby growth forms tend to dominate where plant strategy shifts towards nutrient/resource conservation (Coomes, 1997; Lavorel and Garnier, 2002). During community assembly strong filters in shrubby habitat select species on the basis of their tolerance to increasingly stressful, low-productivity edaphic conditions, thus assembling species with similar niches 39

(Buckland and Grime, 2000; Fukami et al., 2005; Grime, 2006). This is clearly expressed in shrubby environments, even upon casual observation, as strong trait convergence in many phylogenetically distantly related species that tend to demonstrate, amongst other attributes, low rates of growth, photosynthesis, nutrient absorption, and high concentrations of secondary metabolites (Coomes and Grubb, 1996; 1998).

Across a range of climates and ecosystems, convergent suites of attributes are found within edaphically stressed and low-productivity sites, brought about by constraints for competing functions (Reich et al., 1997). Considering the many edaphic parallels between high-elevation forest habitat and lowland shrublands, including low mineral nutrition, phenolic soil toxicity, reduced decomposition, low nitrogen mineralization and waterlogged soils, it seems reasonable to expect similar filters to impose strong convergent effects on species traits and, over time, to have selected for several common ecological attributes (Grubb, 1977; Coomes and Grubb, 1996; Coomes, 1997; Bruijnzeel and Veneklaas, 1998; Tanner et al., 1998). In shrubby lowland habitat, strong filters have likely operated over evolutionary time scales to alter the regional pool from where species (and their traits) can be recruited. We thus interpret the increasing abundance of species from high elevation families in shrublands, and not forested sites, to be a consequence of evolutionary stasis and habitat tracking of an ancestral high-elevation niche on a heterogeneous, lowland Amazonian landscape (e.g., Pillon et al., 2010).

Many previous studies that have tended to highlight strong niche differentiation of species in edaphically specialized Amazonian habitat types and thus underscore the strong potential for underlying environmental variability to lead to phenotypic diversification and speciation (i.e., niche evolution) (Gentry, 1981; 1988; Tuomisto et al., 1998; Fine et al., 2005). Some of our findings are not inconsistent with this notion, as we find lowland families - presumably with long-standing adaptations to forested conditions - to form integral components of shrubby habitat. Many of these are highly specialized, ecological endemics with clear phenotypic differentiation from con-familial species occupying tall forested habitats (Fine et al., 2005; 2010). While the capacity for natural selection to lead to adaptation across strong environmental gradients has certainly shaped modern community composition of shrubby and edaphically distinct Amazonian habitat types, our analysis suggests that the strong tendency for species to retain their ancestral niche may be equally important. That is, the tendency for locally co-existing species in shrubby habitat to demonstrate more diverse biogeographic relations could be explained by both adaptive shifts 40

of locally derived lowland forest taxa combined with evolutionary conservatism and exaptation from high Andean (or other) regions.

Based on our data, we cannot distinguish between an alternative hypothesis that may also explain higher observed biogeographic diversity in shrubby habitat. We found that the ecological differentiation of species with high Andean or low Amazonian biogeographic tendencies is broadly expressed along local physiognomic gradients in the lowlands. This suggests the possibility that the major niche differences responsible for the geographic separation of Andean and Amazonian floristic components (sensu Gentry) on the modern geophysical template could be even more ancient than Neogene mountain building, a rather recent phenomenon relative to the origins of modern neotropical families (Hooghiemstra and van der Hammen, 1998; van der Hammen and Hooghiemstra, 2000). Andean upheaval during the Neogene was responsible for an explosive period of plant diversification and is thought to account for half of the modern Neotropical flora. New high-elevation-adapted species would have arisen from low-elevation ancestors (Gentry, 1982). However, not all taxonomic groups took part in this evolutionary phenomena, evident in the highly dichotomous (i.e., Andean vs Amazonian) Neotropical biogeographic pattern. Based on our findings, it is plausible that long-standing ecological filters in the lowlands could have set the stage for such a selective dispersal into newly forming Andean habitat, suggesting an ecological basis for one of the most prominent neotropical floristic patterns on modern landscapes. To the extent that this scenario is true, the severely small plant richness characterizing edaphically stressful habitats, such as peatlands and white sands, on modern lowland landscapes may not be commensurate with their historical contributions to Neotropical floristic diversity.

Limits of the Data

Our analysis is clearly limited by the specific taxonomic and geographic windows we have applied to describe biogeographic pattern. Our entire framework rests on the assumption that the taxonomic groups examined here approximate natural phylogenetic and morphological divisions that are highly conserved for long periods of evolutionary time (Sepkoski and Kendrick, 1993). Our examination of biogeographic pattern, limited to the Andes-Amazon region, obviously does not represent the entire spatial distributions of all families considered. We thus assume that differences in spatial distributions along a strong elevational gradient are sufficient to broadly capture important niche differences among 41

families that will, in turn, determine individual species expansion and colonization ability in the environments they occupy. It is not clear how consideration of other temporal and geographic scales would alter or reinforce observed patterns. However, in comparably stressful hydro-edaphic conditions in other Amazonian habitat types, several authors have noted increasing abundances of taxonomic groups more typical of extra-Amazonian regions – especially from dry forest and savanna habitat (Prance, 1979; Kubitzki, 1989; Wittmann et al., 2013) - suggesting that expansion of the geographic window could reveal similar pattern as that observed here.

Another limitation is that the structural gradients examined here do not encompass the entire range of forest physiognomies in the Amazon. Few values of tree cover and tree height, for example, in forested peatlands and white sands reach the stature of terra firme forests that typically occupy clay or loam substrates in the Amazon. However taller forests on clayey substrates are well-known to form assemblages comprised of a predictable set of dominant lowland families (Gentry 1988; Terborgh and Andresen, 1998; Pitman et al., 2001; Macía and Svenning, 2005; ter Steege et al., 2013) unlikely to yield high values of biogeographic diversity as examined here. Overall, we expect that truncation of the taller range of the forest-shrubland gradient would tend to decrease our ability to detect significant biogeographic structure. This may explain the reduction in explained variance in white sands where the range of many key structural variables (tree height and cover especially) was low relative to peatlands. Nevertheless, our results were still statistically robust and we consider that patterns will only become more apparent with increasing physiognomic variation.

Acknowledgments

Botanical Research Institute of Texas (BRIT) for providing important institutional support and infrastructure. We thank Fernando Cornejo, Piher Maceda, Javier Huinga and Angel Balarezo for research assistance in the field. We thank various Peruvian institutions, including the Instituto Nacional de Recursos Naturales (INRENA), the Dirección General de Flora y Fauna Silvestre (DGFFS), the Ministerio de Agricultura (MINAG), and the Ministerio del Ambiente (MINAM) for research, collection, and export permits during the course of this project. We also thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for permits, logistical support, and access to conservation areas in Brazil.

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Capítulo 3

Householder, J.E.; Wittmann, F.; Tobler, M. & Janovec J,P. 2015. Montane bias in lowland Amazonian peatlands: Plant assembly on heterogeneous landscapes and potential significance to palynological inference. Palaeogeography, Palaeoclimatology, Palaeoecology DOI: 10.1016/j.palaeo.2015.01.029

Montane bias in lowland Amazonian Peatlands: plant assembly on heterogeneous landscapes and potential significance to palynological inference

Abstract

Past temperature changes in tropical mountain regions are commonly inferred from vertical elevational shifts of montane indicator taxa in the palynological record. However temperature is one of several abiotic factors driving the low-elevational limits of species and many montane taxa can occur in warmer lowlands by tracking appropriate habitat types, especially highly flooded wetlands. In this paper we explore ways in which lowland habitat heterogeneity might introduce error into paleo-temperature reconstructions, based on field data of seven modern peatland vegetation communities in the southern Peruvian Amazon (~200 masl). Peat-rich substrates are common edaphic transitions in pollen cores and provide detailed records of past vegetation change. The data show that indicators of modern peatlands include genera with montane as well as lowland distributions, while indicators of surrounding forests on mineral substrates have predominantly lowland distributions. Based on family-level analyses we find that modern peatland vegetation communities have taxonomic compositions appearing to be 389m to 1557m (mean = 1050 ± 391m) above their actual elevations due to a high abundance and number of families with high elevation optima. We interpret the relatively higher prevalence of montane elements in modern peatlands as habitat tracking of a conserved montane niche in heterogeneous lowland landscapes. We suggest that both high moisture availability and stressful edaphic conditions of peatland habitat may explain the montane bias observed. To the extent that fossilization provides a better record of past vegetation that occurred proximate to the site of deposition, we suggest that habitat tracking of montane elements may introduce a cool bias in lowland paleo-temperature reconstructions based on pollen proxies.

Keywords: Amazon Andes; Climate History; Gentry; Montane; Peatland; Wetland

Highlights

- We examine modern woody vegetation in peatlands within a biogeographic framework - Modern peatland vegetation is a combination of highland and lowland elements - Montane elements are more frequent and abundant in peatlands relative to surrounding forest types - Habitat variation may introduce cool biases into temperature reconstruction based on pollen proxies

1. Introduction

Climatic interpretation of fossil pollen assemblages along elevational gradients plays a prominent role in our understanding of neotropical climate change, especially in paleo- temperature reconstruction (Farrera et al., 1999; Weng et al., 2004). Many taxa tend to reach their highest diversity and abundance along a limited elevational range as they track appropriate conditions along mountain slopes. Terrestrial pollen records document the vertical migration of stenothermic taxa in response to past climate change, so knowledge of adiabatic lapse rates can be used to convert elevational shifts to temperature change. This method is standard practice and has been especially important in quantifying past temperature depression from the down slope migration of neotropical montane elements during Pleistocene glacial periods (Bush et al., 1990; Colinvaux et al., 1996; Groot et al., 2011).

The contemporary distribution patterns of higher-level taxa (e.g., families and genera) along mountain slopes are expected to be the result of niche differences across space, however we know little about specific ecological factors underlying these distribution patterns (Körner, 2007; Wiens 2011). While temperature is often assumed to play a prominent role, this single variable is likely only one of a variety of abiotic and biotic factors that drive the lower elevational range limits of montane taxa (Grubb, 1971; Bush, 2004; Körner, 2007; Wiens, 2011). For example, on modern landscapes a number of montane indicator taxa with characteristic peaks in diversity and abundance in high elevation regions are also represented in nearby Amazonian lowlands by one to few species, including Hedyosmum (Chloranthaceae), Panopsis (Proteaceae), Podocarpus (Podocarpaceae), Salix (Salicaceae), Ternstroemia (Pentaphylaceae), Ilex (Aquifoliaceae), and others (Colinvaux et. al., 2000; Van der Hammen and Hooghiemstra, 2000; Marchant et al., 2002). While these montane taxa are exceedingly rare in most lowland forest types, they can become abundant in stressful edaphic conditions, and especially in highly flooded wetland habitats (Steyermark, 1979; Gentry, 1982; Oliviera-Filho and Ratter, 1995; Marchant et al., 2002). Apparent tracking of many montane elements to particular lowland habitats suggests that the abiotic and biotic conditions in which they can successfully disperse and regenerate on lowland landscapes may be constrained by a highly conserved niche (Ackerly, 2004; Wiens and Donoghue, 2004; Harrison and Grace, 2007; Pillon et al., 2010; Wiens et al., 2010; Wiens, 2011).

The ecological and evolutionary processes that determine how montane elements are assembled on modern heterogeneous lowland landscapes may be relevant to palynological 51

inference, and especially paleo-temperature inference, in at least two ways. First, the quality of paleo-temperature interpretation is dependent upon an adequate understanding of the drivers of species low-elevational range limits, which are often poorly known (Körner, 2007). To the extent that montane elements tend to occupy lowland sites that are most suitable to their conserved phenotypes (Ackerly, 2004; Wiens, 2011), increased understanding of the ecological conditions in which they occur in the lowlands can reveal insight into factors ̶ other than temperature ̶ that might influence distribution patterns of montane elements through time. Second, habitat tracking of an ancestral niche on heterogeneous lowland landscapes can strongly alter the taxonomic composition and biogeographic signatures of local vegetation communities during community assembly, independent of regional climate change (Prance, 1979; Kubitzki, 1989; Pyke et al., 2001; Wittmann et al., 2013). Because vegetation directly occupying fluvial or depositional sites (i.e., wetland vegetation) is known to contribute disproportionately to pollen sums, the ecological sorting processes operating at local scales have the potential to influence the biogeographic signature of fossil assemblages and, in turn, the climate interpretations made from them (Burnham et al., 2001; Berrio et al., 2002; Marchant et al., 2009). In some cases, alternative interpretations of past climate change seem to have been fueled by disagreement over the importance of climatic versus local ecological processes in explaining compositional shifts in fossil pollen assemblages through time (Colinvaux et al., 2000; Van der Hammen and Hooghiemstra, 2000; Punyasena et al., 2011).

In this study, we develop a biogeographic framework to examine the modern taxonomic composition of peatland habitat in the southern Peruvian Amazon. Peat-rich substrates are commonplace in pollen records and have provided detailed accounts of past vegetation (e.g. Liu & Colinvaux, 1985; Colinvaux et al., 1996). Making use of a publically available network of woody vegetation inventories established across a wide elevational gradient we examine the degree to which the taxonomic compositions of woody peatland communities reflect that which would be expected given their actual elevation.

2. Methods

2.1 Study Region

The peatland system considered in this paper is located within the subsiding Beni- Mamore foreland basin below 250 masl in the Department of Madre de Dios in the Amazon region of southern Peru (Figure 1). The main drainage tributary is the Madre de Dios River, an actively meandering white-water river entrenched within alluvial deposits corresponding to the late Neogene (Campbell et al., 2006). Non-flooded terra firme as well as seasonally flooded forests dominate the landscape. Satellite imagery combined with ground truthing revealed more than 250 peatlands occupying a combined area > 290 km2 (Householder et al., 2012; Janovec et al., 2013) and distributed along a 250-km stretch of the modern meander belt of the Madre de Dios River from the Andean foothills eastward to the Bolivian border. Individual peatlands range from <10 to 3500 ha. Mean peat thickness of individual peatlands range from 0.85 to 3.04 m, however maximum thickness of up to 9 m was registered (Householder et al., 2012). The peatlands are replenished continuously by ground water, with above-ground water-level fluctuations typically less than 1 m (Goulding et al., 2007; Householder et al., 2012). The climate is humid tropical with annual rainfall varying between approximately 1,200 and 3,300 mm and a strong dry season between August and October (Foster et al., 1994). 53

Figure 1. The 250-km stretch of the main drainage tributary of the southern Peruvian Amazon where focal peatlands (black) are located. Sampled peatlands are outlined. Peatland names (from west to east; Table 3) are COLO, CICRA, HUIT 1, HUIT2, LAGA, MERC, and BOLI. The inset map shows the location of the 76 plots obtained from the Gentry transect data in relation to the peatland study area. Black and gray triangles represent Gentry sites at elevations greater than and less than 1000 masl, respectively. The shaded area corresponds to the Chocó region included in the supporting analysis (See section 4.1.1).

2.2 Vegetation Sampling

Peatland vegetation was sampled in seven of the largest permanently saturated peatlands distributed along a 250-km east-west gradient, each accessed through 1-4 km transects that in most cases traversed the entire peatland. Each transect was oriented to cross individual peatlands in the direction parallel with the main axis of habitat variation as judged by changes in pixel values exhibited by multispectral Landsat TM imagery configured to bands 3, 4, and 5. Spectral differences reflect changes and transitions in vegetation structure ranging from mixed palm swamp forest to open boggy grasslands with stunted woody plants (Householder et al., 2012; Janovec et al., 2013). 54

Quantitative vegetation inventory was carried out in nested plots distributed at 100-m intervals along each transect. A total of 148 plots were installed in the seven peatlands studied, with 18-30 plots sampled in each. Trees and shrubs were sampled in nested 10 x 10- m and 5 x 5-m square plots respectively, where trees are defined as woody plants with DBH ≧ 10cm and shrubs broadly defined as woody plants with DBH <10 cm and >1 m in height. To calculate abundance, we counted the number of stems of each species in each nested plot. Voucher specimens were collected for all species and deposited in the herbaria of the Botanical Research Institute of Texas (BRIT), the La Molina University Forestry Herbarium (MOL), and the San Marcos Museum of Natural History (USM). All metadata and annotation history, as well as associated images from the field and herbarium are openly available through the Digital Herbarium of the Andes-Amazon Atrium Biodiversity Information System (http://atrium.andesamazon.org/index.php) under the project entitled "Aguajal Project".

Data of vegetation on non-peat substrates was obtained from an extensive vegetation plot network compiled by Alwyn Gentry and maintained by the Missouri Botanical Garden (Phillips and Miller, 2002). The Gentry transect data are unique because they are based on a standard sampling method used across an extensive geographic area and a diversity of habitats. Over the last two decades, the data have been used in a number of plant macroecological studies (e.g., Enquist and Niklas, 2001; Enquist et al., 2002; Punyasena 2008a). Gentry inventory data were collected in 0.1-ha plots consisting of 10 contiguous 2 x 50-m linear subplots where all woody individuals ≧ 2.5 cm DBH were recorded, along with the occasional individuals with DBH down to 1 cm. Sequential subplots were placed end to end and oriented in random directions. We extracted data only from sampling sites located in the Andes-Amazon region (Bolivia, Colombia, Ecuador, Peru, and Venezuela) with elevations ranging from 10 to 3200 masl. A total of 76 sites met our criteria, with 31 located above 1000 m, and 38 lowland sites below 500 m (Appendix C). Lowland samples were undertaken in wetland (n=8) and terra firme (n=30) habitats. Sites on the margins of our region of interest corresponding to Bolivian savanna and dry forest were excluded as seasonal drought is expected to drive floristic differences there. Sites on the Pacific slope were also excluded. The accuracy of species names provided in the dataset was assessed by cross-referencing voucher specimen numbers provided in the original dataset with current determinations of collections stored at the Missouri Botanical Garden and accessible through the Tropicos database (http://www.tropicos.org). 55

Plant nomenclature of both Gentry and peatland plot data was standardized to Tropicos and analyzed at the taxonomic rank of family. For the peatland data, tree and shrub subplots were merged by calculating the sum of family abundances in each peatland. A matrix of relative abundances was calculated initially, but we were concerned with potential biases in abundance estimates caused by a nested plot design and differences in minimum size criteria in the peatland and Gentry inventories (see Table 1 for a summary of important methodological differences). To account for this, presence/absence matrices were constructed for comparison.

Table 1. Summary of the primary methodological differences between the Gentry plot data used to model distribution patterns of families along the elevation gradient and the peatland plots.

Methodology Gentry Peatland

Minimum Dbh < 2.5cm Height < 1m inclusion criteria 100m2 (trees) + Plot size 100m2 25m2 (shrubs)

Plot Continuous lines Discontinuous plots oriented in random along main arrangement directions environmental gradient

Plot shape Linear Square

Plots per site 10 18-30

Total sites 76 7

2.3 Development of the Biogeographic Framework

Using the Gentry transect data, we modeled the biogeographic pattern of individual families along the elevation gradient using two parameters, their elevation optima (abundance weighted mean elevations), and their weighted standard deviation of elevation (a measure of elevational range). Previous assessments of the Gentry transect data have demonstrated strong taxonomic structure along the elevation gradient, presumably driven by strong abiotic gradients that sort species according to highly conserved ecological niches (Gentry 1982; Enquist et al., 2002; Punyasena 2008b). We thus assume that such a straightforward 56

assessment of family-level elevational distribution provides a coarse metric by which to compare biogeographic patterns of taxonomic groups, as well as providing a useful predictor of differences in the ecological response of species (Ackerly, 2003; Harrison and Grace, 2007; Punyasena, 2008b).

2.4 Community Analysis

We used community-weighted averages of family elevation optima to quantify biogeographic tendencies of peatland vegetation assemblies. Thus, peatlands that possess an abundance of taxa with high elevation optima will have higher community-weighted averages. This approach provides a practical and intuitive metric, expressed as an expected elevation, by which to examine community structure within a biogeographic framework. We used the difference between expected elevations based on community-weighted means and observed site elevations to evaluate the degree to which the taxonomic compositions of peatlands differed from what would be expected given their observed elevations.

A specially designed cross-validation procedure was developed to test the specific hypothesis that individual peatlands possess a taxonomic composition statistically different from what would be expected given their actual elevation. Specifically, the Gentry data were repeatedly partitioned into validation and training sets, where individual validation sites were sub-sampled with probability of 0.1 drawn from a random binomial distribution. Newly derived family elevation optima developed with the remaining training sites were used to calculate community-weighted averages of validation sites. A probability distribution of calculated differences between observed and expected elevations was generated through 1000 iterations and used to calculate p values.

One inherent issue of the weighted-averaging approach is a potential contraction in the range of calculated expected elevations as a result of double averaging (of both families and communities). To account for this, we examined two (inverse and classical) deshrinking correction factors, as suggested by ter Braak and van Dam (1989). We also examined the potential undue influence of families with patchy or very wide elevation ranges by alternatively down-weighting families by their weighted standard deviation. These variants of community-weighted elevation optima were modeled as a function of observed site elevations using standard linear regression. A cross-validation procedure was used to estimate regression model errors of both simple and down-weighted community means by iteratively removing 10 random sites from the training set. A randomization procedure (van der Voet, 57

1994) was used to assess the difference in root mean square errors and we chose the correction factor that best reproduced observed site elevations. Model construction and evaluation was performed in R version 3.0.2 (R Core Team, 2013) using the package rioja (Juggins, 2012).

2.5 Analysis of Indicator Taxa

An additional analysis examined the degree of habitat specificity of genera in peat vs. mineral substrates in the lowlands. Information about forest types and substrates of Gentry transects were extracted from voucher specimens. All Gentry transects within a 400-km radius of the peatlands and below 700 m elevation were included. The merged data included 14 sites, seven from each of the Gentry and peatland datasets. Indicator values, measured as the product of the relative frequency and relative average abundance in peat vs. non-peat substrate groups, were calculated for each genus using the R package labdsv (Roberts, 2010) and following the methods of Dufrene and Legendre (1997). Elevational distribution ranges of 20 genera with the highest significant indicator values for each substrate class were assessed by comparing herbarium collection records in the online database of the Global Biodiversity Information Facility (GBIF; http://www.gbif.org). Records were filtered to include only South American specimens deposited in the Missouri Botanical Garden, and those with obvious georeference errors were excluded.

3. Results

We found that after applying a deshrinking correction factor, community-weighted averages of family elevation optima, hereafter referred to as expected elevations, closely predicted observed site elevations of the Gentry transect (Table 2). Down-weighting by family elevational ranges tended to decrease explained variance and increase the root mean square error, suggesting that even widely distributed taxa are likely to have clear abundance patterns along the elevational gradient. Models based on family abundances tended to outperform those based on presence-absence data. Inverse deshrinking resulted in slightly lower root mean square errors and a slightly higher proportion of explained variance, independent of whether the abundance or presence/absence matrix was used, so this deshrinking correction method was used throughout (Table 2).

Table 2. Comparison of community-weighted average regression models of expected and actual elevations of the Gentry transect data. Root mean square error (RMSE) and explained variance (r2) are presented for relative abundance or presence/absence matrices using inverse (I) or classical (C) deshrinking (D/S) and with or without tolerance down weighting.

Matrix Downweight D/S RMSE r2

I 228.1 0.95 No Relative C 234.5 0.95 Abundance I 244.6 0.94 Yes C 252.5 0.94 I 254.3 0.93 No Presence / C 263.2 0.93 Absence I 277.8 0.92 Yes C 289.5 0.92

Differences between expected and observed elevations ranged from 389 to 1557 m (mean ± sd = 1050 m ± 391) for the abundance matrix and 313 to 906 m (mean ± sd = 693 m ± 240) for the presence/absence matrix (Fig. 2 and Table 3). The cross-validation procedure showed that in most cases these differences were significantly higher (Table 3). Details about all families, including their elevational optima and number of stems in peatlands, are detailed in Appendix D. 59

Figure 2. Scatter plot of actual and expected elevations for 76 training sites (open circles) obtained from the Gentry transect data and seven peatland test sites (solid circles). Expected elevations are based on abundance-weighted averages of family-level elevational optima after deshrinking (See section 2.4). Scatter plots based on family presence/absence data show qualitatively similar patterns. Based on a cross-validation procedure used to obtain p values, peatlands appear to occur at significantly higher elevations due to a greater abundance and number of families with higher elevation optima (Table 3).

A total of 371 woody genera were found on either or both organic peat and mineral substrate classes in the 14 lowland sites. Of these, 272 (73%) were restricted to a single substrate type. Eighty genera occurred in peatlands, 61% of which did not occur on mineral substrates and 291 genera occurred on mineral substrates, 77% of which did not occur on peat substrates. According to the indicator analysis, 20% of the 371 genera were significant indicators of one of the two substrate types. Thirty percent (n= 24) of the genera present on peat were significant indicators of peat (p < 0.01) and 18% (52) of genera occurring on 60

mineral substrates were significant indicators of that substrate. Over 118,000 unique herbarium collection records were accessed through the GBIF website to explore the elevational distribution of all indicator genera. Indicator genera of forests on mineral substrates are mostly restricted to low elevations. In contrast, indicator genera of peat substrates exhibit montane, lowland, and widespread elevational distributions (Fig 3).

Table 3. Differences between expected and actual elevations of each peatland where quantitative inventories were performed. Expected elevations are based on abundance-weighted and presence-absence averages of family-level elevation optima after deshrinking (See section 2.4). Expected elevations exceed actual elevation in all cases. Significance is based on an iterative cross-validation procedure (see section 2.4).

Matrix Abundance Presence/Absence

Prediction Prediction Peatland Significance Significance error (m) error (m) BOLI 389 0.06 313 0.09

CICRA 1557 <0.001 868 <0.001 COLO 761 <0.001 517 0.031

HUIT1 930 <0.001 512 0.053 HUIT2 1301 <0.001 831 0.012

LAGA 1290 <0.001 903 <0.001 MERC 1124 <0.001 906 0.003

4. Discussion

The biogeographic distributions of plants are closely linked to physiological responses to climate, which are often highly conserved within lineages. The high explanatory power of the regression model tested in this study confirms this to the extent that family-level composition of modern vegetation varied predictably along the elevational gradient. However, due to increased frequency and abundance of families with preference for high elevation habitats modern lowland Amazonian peatland assemblies demonstrated expected elevations of 313 to 1557 m above actual elevations, significantly higher relative to non-peat habitat types. The consistently high elevations predicted for peatlands based on both 61

abundance and presence/absence data demonstrate that rather than rare exceptions, montane elements are abundant and taxonomically diverse in lowland peats, relative to surrounding forests.

Figure 3. Elevational distributions of 40 indicator genera on peat and mineral substrates. Box plot hinges extend only to the first and third quartiles the median is indicated by a darkened band. Within respective substrate types taxa are ordered by their mean elevation. The dashed vertical line at 658 m marks the mean of average elevations of all genera.

The results are further supported by a local comparative analysis of peatland composition and the surrounding forests, which demonstrated that floras on peat substrates are a mixture of both montane and lowland indicator taxa. In addition to the mid-high elevation forest genera identified by the indicator analysis (Cestrum, Cybianthus, Graffenriedia Hedyosmum, Ilex, Myrcia and Nectandra), other montane elements are also common in peatlands, such as Begonia (Begoniaceae), Centropogon (Campanulaceae), Coccosypselum (Rubiaceae), Cyathea (Cyatheaceae), Isoetes (Isoetaceae), Myrsine (Primulaceae), Polypodium (Polypodiaceae) and Talauma (Magnoliaceae). However they were either not within the top 20 indicators, occurred at reduced frequency, or did not meet minimum size criteria. Nonetheless, the data show that montane taxa represent an important component of peatland vegetation, a pattern we refer to as "montane bias.”

4.1 Palynological Relevance

Interpretation of down slope migration apparent from the palynological record must ultimately be framed within our understanding of the drivers of species low-elevational range limits. While these remain poorly understood for most species they are widely expected to include a combination of factors that are abiotic (e.g., temperature and moisture) and biotic (e.g., competition, predation, parasitism, dispersal) (Körner, 2007; Wiens, 2011). During paleo-temperature reconstruction it is often assumed that temperature change outweighs other potentially important drivers, even though alternative hypotheses can often not be fully rejected (Van der Hammen and Hooghiemstra, 2000; Bush et al., 2004; Punyasena et al., 2011). We propose that examination of the conditions in which montane taxa occupy modern lowland landscapes can reveal insight into the factors – other than temperature- that might influence their low-elevation limits. Our arguments are based on the premise that biogeographic patterns result from the tendency for species to retain their ancestral niche that, in turn will determine the ability of species to expand and colonize in changing environments (Ackerly, 2004; Wiens and Graham, 2005; Harrison and Grace, 2007; Wiens, 2011). While it is plausible that individual species within higher taxa can behave idiosyncratically, rendering family membership a poor predictor of ecological behavior (Silvertown et al., 2001) our results suggest otherwise. The tendency for montane taxa to prefer particular lowland habitat types seems best interpreted as habitat tracking of an ancestral, montane niche on a heterogeneous lowland landscape. Below we suggest that high moisture availability and stressful edaphic conditions characterizing peatlands may be important factors contributing to the observed montane bias. 63

4.1.1 Moisture availability

The montane bias in modern lowland peatlands, characterized by year-round soil moisture, suggests moisture availability to be a critical factor influencing the current lowland distributions of montane taxa. For example, the distribution of the majority of extant species of Hedyosmum in cool, moist habitat of mid-high elevation Andean forests is expected to be a consequence of constraints induced by poor stem wood hydraulic capacity and susceptibility to drought cavitation (Antonelli and Sanmartín, 2011). Where it occurs in hot and highly seasonal lowland regions it is invariably limited to moist microsites, such as permanently saturated peats (this study), waterlogged sands, and riparian habitats (Todzia, 1988). Thus, our findings are consistent with the idea that the distribution of montane forests and their taxa are highly sensitive to changes in plant water-energy balance (Bruinjzeel and Veneklaas, 1998).

Because both ambient temperature and available moisture interact to define plant water-energy balance, downhill distributional shifts of plant species apparent from the pollen record may not be adequately explained by considering reductions in past temperature in isolation (Bush et al., 2004). Increases in available moisture that limit the duration and severity of drought conditions during key seasonal and plant developmental phases may contribute to lower elevation limits of montane taxa. Downhill niche tracking of a suitable water-energy balance either as a result of regional increases in precipitation ̶ as suggested for glacial western Amazonia (Cheng et al., 2013) ̶ or moist microsite conditions might be challenging to distinguish from a pure temperature response (Bush et al., 2004).

We used the Gentry transect data to further test the idea that moisture availability can significantly influence the lower-elevation limits of montane taxa. Using the same cross- validation procedure described in section 2.4, we examined model prediction errors of data from 12 Gentry transect sites located in the Chocó, a lowland region distributed from southern Panama to northern Ecuador (Fig. 1). The region was separated from the Amazon basin due to the uplift of the Eastern Cordillera of the Andes Mountains (Behling et al., 1998; Hoorn et al., 2010). Annual precipitation exceeds 4000 mm/yr and typically reaches >7500 mm near the foothills of the Pacific slopes of the Andes. Even during the driest months droughts persisting longer than one week are extremely rare (West, 1957). The mean annual temperature is about 26–27°C, with a minimal 1°C difference between the coldest and the warmest months (Snow, 1976). If increased moisture availability influences the ability of 64

montane plant taxa to persist at lower elevational limits, then we might expect these to have lower distributions on rainy western Pacific slopes relative to Amazonian slopes. Indeed, expected elevations based on abundance-weighted community averages of family elevation optima were significantly higher than expected for 10 out of 12 Chocó sites (p <0.05 as the critical value). Differences between actual and expected elevations ranged from -217 m to +695 m with a mean (± sd) of 445 m (± 234 s.d.). The higher expected elevations for the Pacific slope lowland sites are the result of the presence of several plant taxa that are mostly restricted to higher montane forests on the Amazonian side. Using presence/absence data, only four of 12 plots had significantly higher expected elevations. Differences between expected and actual elevations ranged from -384 m to +525 m with a mean (± sd) of 325 m (±268 s.d.). While we cannot eliminate the possibility that other ecological and historical factors are driving the patterns observed for the Chocó, this preliminary analysis corroborates previous botanical observation of the tendency for montane elements to exhibit lower elevational limits in this pluvial region and for moisture availability to influence the lower- elevation limits of plant taxa (Gentry, 1982; Van der Hammen and Hooghiemstra, 2000; Hooghiemstra et al., 2012). Comparing results of pluvial Chocó sites to peatland sites, we see that while both tend to demonstrate higher expected elevations using family abundance data, proportionally fewer Chocó sites show significantly higher (p <0.05) elevations using presence/absence data. Thus, peatlands are distinguished by their high diversity of montane taxa that are distributed among a greater number of families, at least on the spatial scale of small plots considered here. These results further highlight the important contribution of montane elements to this lowland habitat type.

4.1.2 Edaphic Associations

While temperature is largely expected to determine the physiological limits of the upper elevational ranges of plant species, their lower distributional limits are expected to be determined primarily by competition rather than by excessively high temperature (Grubb, 1971; 1977; Coomes and Allen, 2007; Prior and Bowman, 2014). Peatlands in the Amazonian lowlands are structurally and edaphically characterized by short-statured canopies, decreased productivity, extremely acidic soils, saturated substrates, limited fertility, phenolic soil toxicity, and reduced decomposition and nitrogen mineralization (Waughman, 1980; Runge, 1983; Page et al., 1999; Läteenoja et al., 2009; Householder et al., 2012). Interestingly, these hydrologically induced edaphic conditions are quite similar to the climate- driven edaphic conditions characteristic of montane sites (Grubb, 1977; Edwards, 1982; 65

Bruijnzeel and Veneklaas, 1998; Tanner, 1998; Unger et al., 2010). Confronting potentially similar limitations to growth and survival along increasingly stressful ranges of elevation and hydrological gradients, it is not unreasonable to expect convergent effects on species traits (Chapin et al., 1993; Reich et al., 1997). Montane elements in modern lowlands are likely to be better competitors in edaphically extreme lowland habitats than in a tall, productive, and diverse terra firme forest matrix. By altering resource bioavailability, predation and parasitism in such ways that favor montane species, edaphic transitions on heterogeneous lowland landscapes can shift competitive dynamics at range boundaries and potentially significantly decrease the lower limits of montane distributions (Jaeger, 1971; Breirs, 2003; Gaston, 2003; Parmesan, 2006; Holt and Barfield, 2009).

With this in mind, to the extent that montane elements invaded past lowland environments, their migrations may have been largely accommodated by marginal, highly flooded, stressful, and patchily distributed habitat types. Indeed, by expanding the geographic window it is clear that many important montane indicator taxa (e.g., Alnus, Betula, Ericaceae and Weinmannia) are better known as bog and fen wetland indicators in their native temperate zones (USDA NRCS, 2013). As the ecological distributions of montane taxa become increasingly constrained to specialized edaphic conditions towards the limits of their lower elevation ranges, immigration and extinction processes are likely to be more variable. Variation in species propagule dispersal, metapopulation dynamics, and the spatial configuration of appropriate habitats in past landscapes may be important in explaining the extent of past downslope plant migration (Leibold et al., 2004).

4.1.3 Pollen Proxies on Heterogeneous Amazonian Landscapes

Estimates of glacial phase neotropical temperature depression using fossil pollen proxies vary greatly, ranging from ~5°C to 9°C relative to modern (Farrera et al., 1999; Bush et al., 2004a; Ballantyne et al., 2005). While such wide variability poses problems for elucidating a more accurate vision of past climate, we suspect that it is consistent with high neotropical habitat heterogeneity. For example, we have argued that in modern lowland landscapes habitat tracking of a montane niche can lead to local vegetation communities on particular hydro-edaphic conditions to possess a higher abundance and diversity of montane elements relative to surrounding forest types. Using an adiabatic lapse rate of 6.5°C/km, the modern flora occupying peat substrates possesses a biogeographic signature resembling forests that are, on average, 2.1 - 2.3 °C cooler based on the mean differences between 66

observed and expected elevations of presence-absence and abundance models respectively. While clearly not reflecting modern paleoecological methods ̶ pollen sums reflect both local vegetation as well as that derived from surrounding uplands ̶ it does show a strong effect of habitat heterogeneity on the biogeographic composition of local plant communities. However, because fossilization can leave a better record of certain habitat types than others, a cool bias in lowland paleotemperature estimates may be more prevalent than appreciated to date. Assuming a montane bias in similar neotropical environments in the past, our data establish the possibility ̶ at least under depositional conditions characterized by the accumulation of peat ̶ that pollen assemblages in Amazonian lowlands can potentially appear to be more "montane", and thus cooler, independent of plant response to temperature. In this sense our interpretations are consistent with other findings that have suggested habitat-related errors in estimating past temperatures from plant macrofossils. For example, in lowland Ecuadorean Amazon, Burnham et al. (2001) demonstrated that traits analysis of woody plants growing around lakes and rivers leads to an underestimation of mean annual temperatures by 2.5°C - 5°C due to the high proportion of toothed leaves in these flooded habitats.

The ecological processes that sort montane elements on heterogeneous lowland landscapes may point towards a potential cool bias of pollen proxies in reconstructing past temperature in the Neotropics. Indeed, reviews of pollen-based proxies of glacial tropical South America tend to show greater minimum (cooler) temperature depressions relative to both non-pollen proxies (e.g., Stute et al., 1995) and other tropical regions (Farrera et al., 1999; Ballantyne, 2005). While explanations of these patterns may be revealed by a refined understanding of how climate works, efforts to improve our understanding of how tropical ecosystems and their biota uniquely evolve and interact along local gradients may be informative as well.

5. Acknowledgments

The manuscript was developed and written with funding provided to the corresponding author by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ-process number 141727/2011-0). We thank the Max Planck Institute for Chemistry and Maria Teresa Fernandez Piedade for providing a productive, hospitable work environment. Field research was made possible by funding from the Discovery Fund of Fort Worth, Texas, the Gordon and Betty Moore Foundation (grant no. 484), the U.S. National 67

Science Foundation (grant no. 0717453), and the Programa de Ciencia y Tecnologia— FINCYT (co- financed by the Banco Internacional de Desarollo, BID) grant number PIBAP- 2007–005. We thank Sy Sohmer, Cleve Lancaster, Pat Harrison, Will McClatchey, the board of directors, administration, development, and general staff of the Botanical Research Institute of Texas (BRIT) for providing important institutional support and infrastructure over the years. We are grateful to Jason Wells, Amanda Neill, Keri Barfield, and Renan Valega for logistical support, assistance, and discussion during various phases of this research. We also thank Fernando Cornejo, Piher Maceda, Javier Huinga, Angel Balarezo, and Fausto Espinoza for assisting in different phases of field research. Finally, we appreciate various institutions for ongoing research, collection, and export permits during the course of this project, including the former Instituto Nacional de Recursos Naturales (INRENA), the Dirección General de Flora y Fauna Silvestre (DGFFS), the Ministerio de Agricultura (MINAG), and the Ministerio del Ambiente (MINAM).

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Síntese

Fazendo uso das condições abióticas extremas consistentes (inundação permanente), e a ampla distribuição, a presente tese especificamente direciona as questões para a diversidade da vegetação lenhosa e a composição de espécies em buritizais em ampla escala espacial. Os resultados indicam que (1) as comunidades de vegetação dos buritizais são caracterizadas por uma alta variabilidade composicional entre os sítios; (2) o uso do habitat pantanoso é um atributo funcional amplamente distribuído na filogenia das florestas Amazônicas; e (3) as comunidades de plantas dos buritizais são caracterizadas por linhagens com distribuição não- Amazônica. A inundação e fatores estressantes múltiplos associados fortemente selecionam indivíduos que dispõe de atributos funcionais para este tipo de condição abiótica. Enquanto muitas espécies da filogenia das florestas Amazônicas aparentemente adquiriram os atributos funcionais necessários para tolerar as condições abióticas nas áreas pantanosas, os sítios mais extremos são consistentemente compostos por linhagens de distribuição extra-amazônica. As comunidades demonstram um padrão de substituição composicional ao longo de gradientes de estresse, um padrão que é interpretado com a presença de um nicho ancestral profundamente conservado – possivelmente associado a fatores estressantes em geral – na paisagem heterogênea da Amazônia. Argumenta-se que as análises comparativas de comunidades de vegetação de buritizais oferecem uma abordagem única sobre os recentes modelos de diversidade especifica e ecossistêmica, que até o presente, baseia-se quase que inteiramente em florestas de terra firme. Estima-se que as áreas úmidas Amazônicas cobrem uma área entre 20 - 30% da bacia e são responsáveis por uma grande parte da heterogeneidade de habitats na escala de paisagem. Assim, os resultados sobre a vegetação das áreas pantanosas e a heterogeneidade dos habitats podem ter uma grande importância para entender os processos biogeográficos e evolucionários na Amazônia e nos Neotropicos em geral. Especificamente, as áreas úmidas e outros tipos de habitats extremos possivelmente alteram as condições abióticas e assim definem quais espécies (e atributos funcionais associados) podem ser recrutadas e de onde elas estão sendo recrutadas. Argumenta-se que estes processos atuaram na paisagem Amazônica durante tempo evolucionário, e definiram localmente as comunidades de vegetação nos buritizais (capítulos 1,2,3), assim como os padrões de diversidade em geral (capítulo 2). 76

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APÊNDICE A - List of identified families and genera documented in MDWs, their frequency in 28 sites, total number of stems, and floristic group. "Ama" = Amazon-Centered; "And" = Northern Andean-Centered; "Dry" = Dryland Centered; "Lau" = Laurasian; "SouTmp" = Southern Andes/South Temperate Centered

Freq- Total Floristic Taxa uency Stems Group (n =28)

Acanthaceae 1 1 And Aphelandra 1 1 Anacardiaceae 18 1123 Ama Anacardium 4 17 Campnosperma 3 130 Spondias 2 2 Tapirira 15 974 Annonaceae 20 516 Ama Anaxagorea 2 12 Annona 7 64 Cremastosperma 2 6 Duguetia 1 2 Ephedranthus 1 1 Guatteria 13 86 Heteropetalum 1 8 Pseudoxandra 4 61 Rollinia 1 3 Unonopsis 2 4 Xylopia 5 263 Apocynaceae 17 178 Ama Couma 1 1 Galactophora 2 8 Himatanthus 8 56 Lacmellea 1 16 Macoubea 2 5 Macropharynx 1 2 Malouetia 2 10 Mandevilla 1 2 Marsdenia 2 3 Odontadenia 2 4 Tabernaemontana 2 64 Aquifoliaceae 11 262 Lau Ilex 11 262 Araceae 11 489 And Montrichardia 9 484

Philodendron 2 5 Araliaceae 13 111 And Dendropanax 7 86 Schefflera 7 25 Arecaceae 28 4223 Ama Astrocaryum 2 16 Attalea 3 13 Bactris 9 146 Euterpe 10 179 Iriartea 1 1 Mauritia 28 3763 Mauritiella 9 98 Oenocarpus 1 1 Socratea 4 6 Asteraceae 7 195 And Chromolaena 1 1 Gongylolepis 2 181 Mikania 1 1 Rolandra 1 1 Vernonia 2 9 Wedelia 1 2 Begoniaceae 1 1 And Begonia 1 1 Bignoniaceae 23 1092 Ama Jacaranda 1 1 Tabebuia 17 1020 Bixaceae 2 3

Cochlospermum 2 3 Ama2 Boraginaceae 8 86 Lau Cordia 8 86 Burseraceae 17 338 Ama Protium 16 333 Trattinnickia 2 5

Calophyllaceae 13 394 And1 Calophyllum 11 310 Caraipa 3 84 Campanulaceae 1 2 And Centropogon 1 2 Caryocaraceae 4 31 Ama Caryocar 4 31

Celastraceae 4 27 ?3 Cheiloclinium 1 1 Salacia 3 26 Chloranthaceae 7 1087 Lau Hedyosmum 7 1087

Chrysobalanaceae 15 292 Ama Couepia 1 3 Exellodendron 2 8 Hirtella 11 103 Licania 7 155 Parinari 3 23

Clusiaceae 23 663 And1 Chrysochlamys 4 16 Clusia 18 389 Garcinia 2 3 Havetiopsis 1 4 Symphonia 9 190 Tovomita 3 61 Combretaceae 6 28 Ama Buchenavia 4 19 Combretum 2 5 Terminalia 2 4 Connaraceae 2 16 Ama Connarus 2 15 Rourea 1 1 Convolvulaceae 1 2 Ama Evolvulus 1 2 Cyatheaceae 3 63 Cyathea 3 63 Dichapetalaceae 2 2 Ama Dichapetalum 1 1 Tapura 1 1 Dilleniaceae 14 121 Ama Curatella 3 7 Davilla 6 58 Doliocarpus 5 49 Tetracera 2 7 Dioscoreaceae 1 6 N a Dioscorea 1 6 Ebenaceae 5 184 Ama Diospyros 5 184 Elaeocarpaceae 9 56 Ama Sloanea 9 56 Erythroxylaceae 9 283 Dry Erythroxylum 9 283

Euphorbiaceae 22 246 Ama4 Alchornea 12 111 Caperonia 1 2 Conceveiba 1 1 Conceveibum 1 1

Croton 3 4 Hevea 7 52 Hura 3 3 Mabea 5 39 Manihot 1 1 Maprounea 1 1 Micrandra 1 12 Nealchornea 1 4 Pera 6 15 Fabaceae 28 1261 Ama Abarema 1 1 Acosmium 4 59 Aeschynomene 6 62 Aldina 2 23 Andira 2 4 Campsiandra 1 4 Canavalia 2 2 Chamaecrista 2 7 Clitoria 2 8 Copaifera 1 1 Crudia 2 30 Dalbergia 10 71 Dimorphandra 2 30 Erythrina 2 2 Etaballia 1 13 Galactia 2 39 Hydrochorea 3 10 Inga 11 104 Machaerium 11 89 Macrolobium 9 129 Macrosamanea 7 167 Ormosia 9 85 Paramachaerium 1 2 Parkia 2 26 Peltogyne 1 1 Pentaclethra 1 1 Platymiscium 2 3 Pterocarpus 9 129 Senna 1 2 Swartzia 6 54 Tachigali 2 3 Taralea 1 5 Vataireopsis 1 1 Vigna 1 1 Zygia 7 90 Gentianaceae 1 1 Lau 96

Coutoubea 1 1 Humiriaceae 5 79 Ama Humiria 4 67 Humiriastrum 1 8 Sacoglottis 2 4

Hydroleaceae 1 1 ?5 Hydrolea 1 1

Hypericaceae 8 27 And1 Vismia 8 27 Icacinaceae 2 83 Ama Emmotum 2 83

Lamiaceae 3 30 Lau6 Aegiphila 1 2 Vitex 2 28 Lauraceae 24 295 Ama Aiouea 1 16 Aniba 1 1 Endlicheria 10 65 Licaria 1 4 Nectandra 8 74 Ocotea 14 130 Pleurothyrium 2 3 Lecythidaceae 11 98 Ama Cariniana 6 10 Eschweilera 2 11 Gustavia 2 4 Lecythis 5 73 Linaceae 3 22 unassigned Hebepetalum 1 14 Roucheria 3 8 Loganiaceae 8 68 Ama Bonyunia 1 21 Potalia 3 5 Strychnos 5 42 Lythraceae 4 14 Lau Cuphea 4 14 Magnoliaceae 3 11 Lau Talauma 3 11 Malpighiaceae 14 299 Ama Blepharandra 1 19 Bunchosia 2 4 Burdachia 3 76 Byrsonima 6 175 Heteropteris 4 18 Hiraea 1 7

Malvaceae 24 826 Ama7 Byttneria 2 9 Catostemma 1 4 Ceiba 1 3 Hibiscus 2 2 Luehea 1 30 Lueheopsis 7 364 Melochia 2 47 Mollia 2 3 Pachira 9 296 Pavonia 2 50 Pseudobombax 4 10 Scleronema 1 1 Sterculia 3 3 Theobroma 3 4 Marantaceae 1 2 And Ischnosiphon 1 2 Marcgraviaceae 2 31 And Marcgravia 1 17 Souroubea 7 14 Melastomataceae 25 1788 And Aciotis 5 85 Bellucia 4 8 Blakea 1 1 Clidemia 9 133 Graffenrieda 4 285 Henriettea 6 317 Macairea 3 52 Miconia 14 226 Mouriri 2 7 Pachyloma 4 37 Pterolepis 3 5 Rhynchanthera 3 289 Tococa 15 341 Meliaceae 8 65 Ama Guarea 1 3 Trichilia 8 62 Menispermaceae 4 5 Ama Abuta 3 3 Sciadotenia 1 2

Monimiaceae 1 1 And8 Mollinedia 1 1 Moraceae 15 649 Ama Batocarpus 1 1 Brosimum 1 145 Ficus 12 221

Maquira 5 45 Perebea 1 4 Sorocea 7 233 Myristicaceae 19 370 Ama Iryanthera 2 37 Otoba 1 1 Virola 18 332 Myrtaceae 19 601 SouTmp Calyptranthes 4 83 Eugenia 11 325 Myrcia 14 191 Nyctaginaceae 3 38 And Guapira 1 29 Neea 2 9 Ochnaceae 21 360 Ama Lacunaria 1 1 Ouratea 20 344 Quiina 3 9 Wallacea 1 6 Olacaceae 5 47 Ama Aptandra 3 42 Chaunochiton 1 4 Minquartia 1 1 Onagraceae 12 116 SouTmp Ludwigia 12 116 Opiliaceae 2 2 not treated Agonandra 2 2 Orchidaceae 1 8 And Vanilla 1 8 Passifloraceae 2 2 And Passiflora 2 2

Pentaphylacaceae 5 149 Lau9 Ternstroemia 5 149

Phyllanthaceae 16 195 Ama4 Amanoa 9 120 Discocarpus 1 1 Hyeronima 2 10 Phyllanthus 5 51 Richeria 3 13

Picramniaceae 1 1 Ama10 Picramnia 1 1

Picrodendraceae 2 5 Ama4 Podocalyx 2 5 Piperaceae 11 70 And Piper 11 70

Polygalaceae 5 27 Ama Bredemeyera 1 3 Polygala 1 1 Securidaca 3 23 Polygonaceae 15 218 Ama Coccoloba 11 203 Symmeria 2 4 Triplaris 3 11

Primulaceae 12 317 And11 Cybianthus 12 310 Myrsine 1 6 Stylogyne 1 1 Proteaceae 2 17 SouTmp Panopsis 2 17 Rosaceae 1 3 Lau Prunus 1 3 Rubiaceae 27 949 And Bothriospora 1 11 Carapichea 1 2 Chomelia 1 1 Coussarea 2 5 Duroia 9 47 Faramea 2 7 Ferdinandusa 4 83 Genipa 4 22 Henriquezia 1 59 Isertia 6 54 Ixora 2 43 Kotchubaea 1 2 Malanea 3 22 Manettia 1 2 Pagamea 4 147 Palicourea 9 94 Posoqueria 4 28 Psychotria 13 182 Randia 1 1 Remijia 1 1 Retiniphyllum 3 74 Rudgea 4 13 Sabicea 7 25 Simira 2 10 Sipanea 1 1 Stachyarrhena 2 12 Uncaria 1 1 Rutaceae 1 1 Ama Ticorea 1 1

100

Sabiaceae 1 10 Lau Ophiocaryon 1 10

Salicaceae 19 304 ?12 Casearia 8 23 Hasseltia 1 1 Laetia 9 276 Tetrathylacium 2 3 Xylosma 1 1 Sapindaceae 8 113 Ama Allophylus 1 2 Cupania 3 8 Matayba 2 10 Paullinia 1 46 Talisia 2 46 Toulicia 1 1 Sapotaceae 8 423 Ama Chrysophyllum 1 4 Ecclinusa 1 1 Elaeoluma 2 112 Manilkara 2 130 Micropholis 2 4 Pouteria 6 170

Simaroubaceae 7 35 Ama10 Simaba 7 35

Siparunaceae 8 72 And8 Siparuna 8 72 Smilacaceae 6 16 unassigned Smilax 6 16 Solanaceae 7 37 SouTmp Cestrum 6 31 Solanum 1 6 Strelitziaceae 5 67 unassigned Phenakospermum 5 67

Tetrameristaceae 1 15 ?9 Pentamerista 1 15 Thymelaeaceae 1 1 unassigned Schoenobiblus 1 1 Trigoniaceae 1 1 Ama Trigonia 1 1

Urticaceae 6 35 ?13 Cecropia 5 23 Coussapoa 2 10 Pourouma 1 2 Violaceae 4 22 Ama Amphirrhox 1 1

101

Corynostylis 2 16 Leonia 1 1 Rinorea 1 4 Vitaceae 1 1 Lau Cissus 1 1 Vochysiaceae 9 89 Ama Erisma 4 34 Qualea 4 54 Ruizterania 1 1 44933

1 Guttiferae of Gentry (1982) is currently split into Clusiaceae, Calophyllacaceae, and Hypericaceae. Andean designation was maintained for all three. 2 Gentry recognized Cochlpspermaceae as distinct family, designated as Amazon-centered 3 Gentry recognized these genera as Hippocrateaceae which he designated as Amazon-centered. However familial distinction is not supported by molecular phylogeny and currently is merged with Celastraceae, designated as Laurasian by Gentry. Due to inconsistencies we dropped these genera from analysis. 4 Euphorbiaceae of Gentry (1982) is currently split into Euphorbiaceae, Phyllanthaceae and Picrodendraceae. The designation of Amazon-centered for this group was maintained. 5 Hydrolea was traditionally placed into Hydrophyllaceae within the Solanales and recognized as Laurasian by Gentry. Molecular phylogenies have placed the genus in Boraginales. We removed Hydrolea from the biogeographic analysis. 6 Gentry defined Lamiaceae (Labiate) as Laurasian, however it now includes genera from Verbenaceae, the latter left unclassified by Gentry. Results did not differ whether this family was removed from analysis or maintained as Laurasian. 7 Gentry considered Bombacaceae, Sterculiaceae, and Tiliaceae (all Amazon-centered) as distinct from Malvaceae. The former families make up the majority of species and stems, thus we recognized this group as Amazon-centered. 8 As circumsribed by Gentry, genera of Monimiaceae are now split with Siparunaceae. Mollinedia are medium-sized trees in coastal Brazil, Andean cloud forests, and occasionally lowland Amazonia. Siparuna is widespread in both lowland Amazonia and Andean forests. We maintained the Andean designation of Mollinedia and Siparuna. 9 Theaceae, designated as Laurasian by Gentry, but noted to have orginated in South America by Raven and Axelrod (1974) traditionally included Ternstroemia and Pentamerisita. Ternstroemia and extra-Amazonian, mostly montane genera (i.e., Freziera and Symplococarpon) are included in Pentaphyllaceae, thus we maintain it's designation as Laurasian. Pentamerista is closely related to Pelliciera mangroves, now both included in Tetrameristaceae. We left this family unassigned. 10 Picramniaceae was treated together with Simaroubaceae by Gentry. We maintained their status as Amazon-centered as designated by Gentry. 11 Primulaceae was considered separate from Myrsinaceae by Gentry, designated as Laurasian and Andean- centered respectively. The genera considered here all belong to the old Myrsinaceae, thus we designated the family as Andean-centered for our purposes. 12 Salicaceae, designated as Laurasian by Gentry, now includes Salix as well as genera from Flacourtiaceae, designated as Amazon-centered. We left this family undesignated. 13 Gentry designated the family the as Andean-centered, but based on our reading it was not clear where he placed the genera considered here (i.e. Moraceae or Urticaceae). We performed the anaysis with Urticaceae as Andean-centered and unassigned, with no qualitative differences in the results.

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APÊNDICE B - A list of families present in either one or both peatland and white sand inventories. NMDS scores refer to the abundance weighted average values of each family along the single non- metric multidimensional scaling (NMDS) axis. This axis was shown to be highly correlated to site elevation (r = 0.93). Weighted averages were taken as a quantitative metric of each family’s relative position along the elevation gradient. Weighted average NMDS scores were compared to Gentry’s (1982) original biogeographic hypotheses as an independent check of family level biogeographic pattern (see Appendix 1, Chapter 1 for designations used). Total number of stems and species are also presented for peatland and white sand habitats.

White Sands Peatlands NMDS Family Scores No. No. No. No. Indiviuals Species Individuals Species

Anacardiaceae -0.72431265 855 1

Annonaceae -0.69627025 90 6 333 13

Apocynaceae -0.76418538 29 4 4 2

Aquifoliaceae 1.3272275 24 1 181 2

Araceae 0.25797656 2 1

Araliaceae 1.02570789 17 2 79 1

Arecaceae -0.48623415 169 4 763 7

Asteraceae 1.51551583 186 2 1 1

Begoniaceae 0.92308575 1 1

Bignoniaceae -0.82049378 2 1 487 1

Burseraceae -0.84529484 137 3 34 4

Campanulaceae 0.57691755 2 1

Chloranthaceae 1.47271208 1087 1

Chrysobalanaceae -0.7922732 107 4 1 1

Clusiaceae 0.33274476 116 7 97 6

Combretaceae -0.94342565 7 3

Connaraceae -0.83456539 2 2

Convolvulaceae -0.90029108 2 1

Dichapetalaceae -0.45664322 1 1

Dilleniaceae -0.8193651 39 2 8 2

Ebenaceae -0.79209879 24 1 3 2

Elaeocarpaceae -0.13317294 5 1 50 2

Erythroxylaceae -1.27834496 281 3 103

Euphorbiaceae -0.44899636 4 2 64 8

Fabaceae -0.79989656 165 12 116 19

Humiriaceae -0.79441072 66 3

Icacinaceae -0.22822155 83 1

Lamiaceae -0.17675241 2 2

Lauraceae 0.19285144 100 7 104 10

Lecythidaceae -0.7543784 10 1

Loganiaceae -0.79454954 2 1

Lythraceae -1.46792895 6 1 7 1

Magnoliaceae 0.21308336 11 1

Malpighiaceae -0.76154036 147 2 1 1

Malvaceae* -0.6861447 253 6 383 7

Marantaceae -0.80715672 2 1

Marcgraviaceae -0.13461892 14 1

Melastomataceae 0.74632058 113 5 540 11

Meliaceae -0.49063759 5 1

Menispermaceae -0.76371031 2 1

Monimiaceae -0.20668019 1 1

Moraceae -0.59825008 145 1 417 9

Myristicaceae -0.57300369 26 1 26 5

Myrtaceae -0.17895616 182 6 151 6

Nyctaginaceae -0.72998913 29 1 9 1

Ochnaceae -0.76141457 132 2 6 1

Olacaceae -0.85472504 4 1

Onagraceae 1.63935151 14 2

Passifloraceae 0.07812318 1 1

Pentaphylacaceae* 1.09712718 114 3

Piperaceae 0.39682192 30 4

Polygalaceae 0.11226581 22 2 4 2

Primulaceae 0.88918767 208 2 97 4

Rosaceae 1.24420313 3 1

Rubiaceae 0.14443203 222 8 231 14

Sapindaceae -0.6572372 51 6 48 3

Sapotaceae -0.77839444 349 7 4 4 104

Simaroubaceae -0.9267483 3 1

Solanaceae 1.01100545 31 3

Trigoniaceae -1.70940457 1 1

Urticaceae -0.49953894 4 3

Violaceae -0.80851788 1 1

Vochysiaceae -0.55668926 26 1 8 1

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APÊNDICE C - Alphabetical list of Gentry transect data used to asses family-level biogeographic patterns along the elevational gradient. Habitat descriptions were obtained from botanical voucher specimens accessed through Tropicos. Boldfaced sites were used in the indicator analysis (Section 2.5). Inventory sites located within the Chocó biogeographic province (italicized) are appended at the end.

Elevation Site Latitude Longitude Country Habitat Description (m)

Achupall 3°27'S 78°22'W Ecuador 2090 Tepui-like bromeliad sward with scattered small trees

Allpahua 3°50'S 73°25'W Peru 130 Tropical Moist Forest (Iquitos - Nauta road) Altodemi 10°55'N 73°50'W Colombia 1180 Tropical premontane wet forest (Magdalena) Altosapa 7°10'N 75°54'W Colombia 2660 Montane oak Forest Antado 7°15'N 75°55'W Colombia 1560 Cloud Forest Araracua 0°25'S 72°20'W Colombia 200 Mature forest over yellow clay

Arcating 0°25'S 72°19'W Colombia 250 High campina forest on white sand soil near air field.

Cabezade 10°20'S 75°18'W Peru 320 Sandy river terraces Campano 11°08'N 74°01'W Colombia 1685 Tropical lower montane wet forest Candamo 13°30'S 69°50'W Peru 800 Ridge top forest with cloud forest aspect Carpanta 4°35'N 73°40'W Colombia 2900 High Andean cloud forest ceroneb1 0°50'N 66°11'W Venezuela 140 Mature forest on sandy "ultisol" ceroneb2 0°50'N 66°11'W Venezuela 140 Mature forest on sandy "ultisol" Cerroayp 4°35'S 79°32'W Peru 2750 Montane cloud forest Cerroesp 10°28'N 72°50'W Colombia 2560 Tropical montane wet forest Chirinos 5°25'S 78°53'W Peru 1780 Remnant patch of Podocarpus forest Chorrobl 6°10'S 78°45'W Peru 2430 Cloud Forest Cochacas 11°52'S 71°22'W Peru 380 Mature forest on alluvial soil Colorado 9°58'N 75°10'W Colombia 240 Disturbed moist forest Colosoi 9°30'N 75°22'W Colombia 300 Forest on limestone. Primary forest on white clay soil with thick root mat. Not Constanc 4°15'S 72°45'W Peru 160 inundated. Cuangos 3°29'S 78°14'W Ecuador 1500 Cloud Forest Cueras 6°40'N 76°30'W Colombia 1670 Cloud Forest Cueva 6°40'N 76°30'W Colombia 350 Mature forest on rich soil on rocks Cutervo 6°10'S 78°40'W Peru 2200 Montane cloud forest Cuyas 4°32'S 79°44'W Peru 2410 Disturbed cloud forest Cuzcoama 12°35'S 69°09'W Peru 200 Mature forest on alluvial soil Dureno 0°05'N 75°45'W Ecuador 300 Tropical Moist Forest (Napo) Elcorazo 0°36'N 77°42'W Ecuador 3200 Disturbed montane cloud forest on volcanic soil Elpargo 6°30'S 79°31'W Peru 3000 High Andean forest Encanto 14°38'S 60°42'W Bolivia 240 Subtropical moist forest Farall 3°30'N 76°35'W Colombia 1930 Tropical lower montane moist forest fincam 2°16'N 76°12'W Colombia 2280 Mature montane forest fincaz 3°32'N 76°35'W Colombia 1960 Tropical lower montane moist forest hachimal 3°38'N 76°33'W Colombia 1860 Tropical lower montane moist forest huamani 0°40'S 77°40'W Ecuador 1150 Tropical premontane moist forest humboldt 8°45'S 75°02'W Peru 270 Tropical moist forest 106

incahuar 15°55'S 67°35'W Bolivia 1560 Steep cloud forest with dry season indiana 3°30'S 73°02'W Peru 130 Well-drained forest on good soil. jatunsac 1°04'S 77°36'W Ecuador 450 Non-alluvial, red clay soil jenarohe 4°55'S 73°45'W Peru 115 Upland forest on well-drained soil kennedy 11°05'N 74°01'W Colombia 2600 Tropical montane wet forest lagenoa 11°05'S 75°25'W Peru 1140 Mature forest remnant laplanad 1°08'N 77°58'W Colombia 1750 Premontane wet forest laraya 8°20'N 74°55'W Colombia 20 Tropical moist forest madidi 13°35'S 68°46'W Bolivia 280 Subtropical wet forest madidiri 13°35'S 68°40'W Bolivia 370 Ridge top manaure 10°22'N 73°08'W Colombia 540 Streamside moist forest remnant maquipuc 0°07'N 78°37'W Ecuador 1630 Mature cloud forest mariquit 5°15'N 74°50'W Colombia 560 Disturbed wet forest remnant miazi 4°18'S 78°40'W Ecuador 850 Floodplain forest along Rio Nangaritza mishnfl 3°56'S 73°27'W Peru 130 Non-inundated lowland forest mishws 3°59'S 73°27'W Peru 150 White sand forest murri 6°35'N 76°50'W Colombia 980 Mature cloud forest nangarit 4°18'S 78°40'W Ecuador 930 Forest pasochoa 0°28'S 78°25'W Ecuador 3020 Mature montane forest rioheath 12°50'S 68°50'W Peru 200 Forest near edge of savannah riomanso 7°30'N 76°05'W Colombia 200 Tropical wet forest rionegro 9°50'S 65°40'W Bolivia 100 Mature forest on sandy clay riotavar 13°21'S 69°40'W Peru 400 Moist lowland forest on ridge sabanaru 10°30'N 72°55'W Colombia 2940 Forest just below paramo sacram 16°18'S 67°48'W Bolivia 2450 Dense ridge top cloud forest shiringa 10°20'S 75°10'W Peru 300 Wet lowland forest on clay sietecue 4°35'N 73°40'W Colombia 2350 Andean cloud forest sucusari 3°15'S 72°55'W Peru 140 Mature terra firme forest tahuampa 3°57'S 73°31'W Peru 130 Seasonally inundated tahuampa forest tamblat2 12°50'S 69°17'W Peru 250 Tropical premontane wet forest (Swamp trail) Tropical premontane wet forest (Rio Tambopata at mouth o tambo 12°50'S 69°17'W Peru 200 D'Orbigny tamboall 12°50'S 69°17'W Peru 260 Alluvial forest tambupl 12°49'S 69°43'W Peru 280 Terra Firme tarapoto 6°40'S 76°20'W Peru 500 Dry forested slopes overlooking Río Huallaga uchire 10°10'N 65°32'W Venezuela 150 Tropical lower montane wet forest vencer 5°45'S 77°40'W Peru 1850 Wet lower montane forest yanam1 3°39'S 72°57'W Peru 105 Mature non-inundated forest on laterite yanam2 3°28'S 72°50'W Peru 130 Mature forest on yellowish lateritic soil yanamtah 3°28'S 72°50'W Peru 120 Seasonally inundated tahuampa forest amotape 4°09'S 80°37'W Peru 700 Chocó anchicay 3°45'N 76°50'W Colombia 300 Chocó bilsa 0°37'N 79°51W' Ecuador 280 Chocó calima 3°56'N 77°08'W Colombia 50 Chocó centinel 0°37'S 79°18'W Ecuador 650 Chocó esmerald 0°54'N 79°37'W Ecuador 150 Chocó jauneche 1°16'S 79°42'W Ecuador 70 Chocó 107

perromue 1°36'S 80°42'W Ecuador 480 Chocó riopal1 0°36'S 79°22'W Ecuador 200 Chocó riopal2 0°35'S 79°22'W Ecuador 200 Chocó sansebas 1°36'S 80°42'W Ecuador 550 Chocó tutunend 5°46'N 76°35'W Colombia 80 Chocó

108

APÊNDICE D - Alphabetical list of families present in peat communities, their calculated elevational optima, and their total number of stems.

Elevational Elevational Total Optima Optima Number (Abundance (Presence of Stems Weighted) Absence) Family Anacardiaceae 593.3854 652.6316 855 Annonaceae 441.0999 647.193 333 Apocynaceae 493.0688 642.8182 4 Aquifoliaceae 2355.0417 1853.2609 181 Araceae 1595.0441 1347.9268 2 Araliaceae 2038.2402 1365.0962 79 Arecaceae 789.9211 876.6406 763 Asteraceae 2410.2626 1598.2222 1 Begoniaceae 1952 2032.5 5 Bignoniaceae 398.3834 646.6379 487 Boraginaceae 695.7576 798.5106 3 Burseraceae 291.1667 345.4545 34 Calophyllaceae 359.7126 494.5652 40 Campanulaceae 1610 1618.3333 2 Celastraceae 634.698 760.6731 4 Chloranthaceae 2491.7787 2170.4762 1087 Chrysobalanaceae 295.0432 460 1 Clusiaceae 1434.398 1158.1579 97 Combretaceae 297.0323 348.5294 7 Connaraceae 229.5041 255.9375 2 Cyatheaceae 1710.7642 1280.8889 63 Dichapetalaceae 727.5397 595.5769 1 Dilleniaceae 214.1739 268.4848 8 Ebenaceae 268.2 320.3333 3 Elaeocarpaceae 890.0362 772.0833 50 Erythroxylaceae 440.3409 382.9167 281 Euphorbiaceae 874.8231 817.7344 64 Fabaceae 379.2353 705.1587 116 Hypericaceae 1483.1818 1201.25 4 Lamiaceae 1195.2027 880.1852 2 Lauraceae 1375.1708 1078.913 104 Lecythidaceae 394.5533 576.8421 10 Linaceae 468.4146 423.9286 1 Loganiaceae 274.6711 248.5714 2 Lythraceae 240 240 7 Magnoliaceae 1632.5 1454 11 Malpighiaceae 511.0177 483.2292 1 Malvaceae 542.9225 621.3158 383 109

Marantaceae 258.4 292 2 Marcgraviaceae 1129.4505 1071.4516 14 Melastomataceae 1875.4962 1148.1343 540 Meliaceae 798.6979 876.0833 5 Menispermaceae 342.2519 452.1429 2 Monimiaceae 1080.4032 901.75 1 Moraceae 611.4446 784.0476 417 Myristicaceae 507.1563 592.1569 26 Myrtaceae 1132.7434 911.3492 151 Nyctaginaceae 560.4492 487.7778 9 Ochnaceae 430.8333 386.6667 6 Onagraceae 2628.4211 2606.6667 14 Passifloraceae 1180 750 1 Phyllanthaceae 1504.2733 1199.3243 5 Piperaceae 1661.148 1186.0377 30 Polygalaceae 1607.2727 2271.1111 4 Polygonaceae 565.5191 1286.7308 64 Primulaceae 2041.0519 717.3171 97 Rosaceae 2322.2581 360 3 Rubiaceae 1413.2514 1906.6667 231 Rutaceae 555.1961 970.4795 1 Salicaceae 637.0153 1326.1429 15 Sapindaceae 669.0143 2200 48 Sapotaceae 395.5526 757.9839 4 Siparunaceae 713.794 326.1364 23 Smilacaceae 829.2857 848.9189 8 Solanaceae 2162.6165 1180 31 Strelitziaceae 100 318.75 3 Thymelaeaceae 1243.3333 2005.5556 1 Trigoniaceae 248.5714 1227.1429 1 Urticaceae 721.6878 271.9231 4 Violaceae 358.3953 470 1 Vochysiaceae 726.7901 1155 8

Instituto Nacional de Pesquisas da Amazônia - INPA Programa de Pós-graduação em Ecologia

Avaliação de tese de doutorado

Título: “MACROECOLOGICAL PERSPECTIVES ON MAURITIA-DOMINATED WETLANDS IN THE AMAZON” Aluno: JOHN ETHAN HOUSEHOLDER Orientador: Dr. Florian Karl Wittmann Co-orientador:

Avaliador: NIGEL PITMAN

Por favor, marque a alternativa que considerar mais apropriada para cada ítem abaixo, e marque seu parecer final no quadro abaixo

Muito bom Bom Necessita revisão Reprovado Relevância do estudo ( x ) ( ) ( ) ( ) Revisão bibliográfica ( ) ( x ) ( ) ( ) Desenho amostral/experimental ( ) ( x ) ( ) ( ) Metodologia ( ) ( ) ( x ) ( ) Resultados ( ) ( x ) ( ) ( ) Discussão e conclusões ( ) ( x ) ( ) ( ) Formatação e estilo texto ( ) ( x ) ( ) ( ) Potencial para publicação em ( x ) ( ) ( ) ( ) periódico(s) indexado(s)

PARECER FINAL

( ) Aprovada (indica que o avaliador aprova o trabalho sem correções ou com correções mínimas)

( x ) Aprovada com correções (indica que o avaliador aprova o trabalho com correções extensas, mas que não precisa retornar ao avaliador para reavaliação)

( ) Necessita revisão (indica que há necessidade de reformulação do trabalho e que o avaliador quer reavaliar a nova versão antes de emitir uma decisão final)

( ) Reprovada (indica que o trabalho não é adequado, nem com modificações substanciais)

_Chicago______, __20 de abril de 2015_____,

______Local Data Assinatura

Comentários e sugestões podem ser enviados como uma continuação desta ficha, como arquivo separado ou como anotações no texto impresso ou digital da tese. Por favor, envie a ficha assinada, bem como a cópia anotada da tese e/ou arquivo de comentários por e-mail para [email protected] e [email protected] ou por correio ao endereço abaixo. O envio por e-mail é preferível ao envio por correio. Uma cópia digital de sua assinatura será válida.

Endereço para envio de correspondência:

Albertina Pimentel Lima PPG-ECO/CBIO/INPA Av. André Araújo nº 2936 69.067-375 - Manaus-AM

Instituto Nacional de Pesquisas da Amazônia - INPA Graduate Program in Ecology

Referee evaluation sheet for PhD thesis

“Title: “MACROECOLOGICAL PERSPECTIVES ON MAURITIA-DOMINATED WETLANDS IN THE AMAZON” Candidate: JOHN ETHAN HOUSEHOLDER Supervisor: Dr. Florian Karl Wittmann Co-supervisor:

Examiner: Paul Fine

Please check one alternative for each of the following evaluation items, and check one alternative in the box below as your final evaluation decision.

Needs Excellent Good Satisfactory Not acceptable improvement Relevance of the study (X) ( ) ( ) ( ) ( ) Literature review ( X ) ( ) ( ) ( ) ( ) Sampling design ( ) ( ) (X) ( ) ( ) Methods/procedures ( ) ( ) (X) ( ) ( ) Results ( ) ( ) ( X ) ( ) ( ) Discussion/conclusions ( ) ( ) (X) ( ) ( ) Writing style and ( X ) ( ) ( ) ( ) ( ) composition Potential for publication in ( ) ( ) (X) ( ) ( ) peer reviewed journal(s)

FINAL EVALUATION ( ) Approved without or minimal changes

(X )Approved with changes (no need for re-evaluation by this reviewer)

( ) Potentially acceptable, conditional upon review of a corrected version (TheT candidate must submit a new version of the thesis, taking into account the corrections asked for by the reviewer. This new version will be sent to the reviewer for a new evaluation only as acceptable or not acceptable)

( ) Not acceptable (This product is incompatible with the minimum requirements for this academic level)

______Berkeley, California, May 18, 2015 Place Date Signature Additional comments and suggestions can be sent as an appendix to this sheet, as a separate file, and/or as comments added to the text of the thesis. Please, send the signed evaluation sheet, as well as the annotated thesis and/or separate comments by e-mail to [email protected] and [email protected] or by mail to the address below. E-mail is preferred. A scanned copy of your signature is acceptable.

Mailing address:

Albertina Pimentel Lima PPG-ECO/CBIO/INPA Av. André Araújo nº 2936 69.067-375 - Manaus AM Brazil

Comments:

Instituto Nacional de Pesquisas da Amazônia - INPA Programa de Pós-graduação em Ecologia

Avaliação de tese de doutorado

Títul Título: “MACROECOLOGICAL PERSPECTIVES ON MAURITIA-DOMINATED WETLANDS IN THE AMAZON” Aluno: JOHN ETHAN HOUSEHOLDER Orientador: Dr. Florian Karl Wittmann Co-orientador:

Avaliador: CAMILA CHEREM RIBAS - INPA

Por favor, marque a alternativa que considerar mais apropriada para cada ítem abaixo, e marque seu parecer final no quadro abaixo

Muito bom Bom Necessita revisão Reprovado Relevância do estudo ( X ) ( ) ( ) ( ) Revisão bibliográfica ( X ) ( ) ( ) ( ) Desenho amostral/experimental ( ) ( X ) ( ) ( ) Metodologia ( ) ( X ) ( ) ( ) Resultados ( ) ( X ) ( ) ( ) Discussão e conclusões ( ) ( X ) ( ) ( ) Formatação e estilo texto ( X ) ( ) ( ) ( ) Potencial para publicação em ( ) ( X ) ( ) ( ) periódico(s) indexado(s)

PARECER FINAL

( X ) Aprovada (indica que o avaliador aprova o trabalho sem correções ou com correções mínimas)

( ) Aprovada com correções (indica que o avaliador aprova o trabalho com correções extensas, mas que não precisa retornar ao avaliador para reavaliação)

( ) Necessita revisão (indica que há necessidade de reformulação do trabalho e que o avaliador quer reavaliar a nova versão antes de emitir uma decisão final)

( ) Reprovada (indica que o trabalho não é adequado, nem com modificações substanciais)

MANAUS, 20 DE ABRIL DE 2015

Endereço para envio de correspondência:

Instituto Nacional de Pesquisas da Amazônia - INPA Programa de Pós-graduação em Ecologia

Avaliação de tese de doutorado

Título: “MACROECOLOGICAL PERSPECTIVES ON MAURITIA-DOMINATED WETLANDS IN THE AMAZON” Aluno: JOHN ETHAN HOUSEHOLDER Orientador: Dr. Florian Karl Wittmann Co-orientador:

Avaliador: WILLIAM ERNEST MAGNUSSON

Por favor, marque a alternativa que considerar mais apropriada para cada ítem abaixo, e marque seu parecer final no quadro abaixo

Muito bom Bom Necessita revisão Reprovado Relevância do estudo ( x ) ( ) ( ) ( ) Revisão bibliográfica ( x ) ( ) ( ) ( ) Desenho amostral/experimental ( ) ( x ) ( ) ( ) Metodologia ( ) ( x ) ( ) ( ) Resultados ( x ) ( ) ( ) ( ) Discussão e conclusões ( ) ( x ) ( ) ( ) Formatação e estilo texto ( ) ( x ) ( ) ( ) Potencial para publicação em ( x ) ( ) ( ) ( ) periódico(s) indexado(s)

PARECER FINAL

( ) Aprovada (indica que o avaliador aprova o trabalho sem correções ou com correções mínimas)

( x ) Aprovada com correções (indica que o avaliador aprova o trabalho com correções extensas, mas que não precisa retornar ao avaliador para reavaliação)

( ) Necessita revisão (indica que há necessidade de reformulação do trabalho e que o avaliador quer reavaliar a nova versão antes de emitir uma decisão final)

( ) Reprovada (indica que o trabalho não é adequado, nem com modificações substanciais)

Manaus 03/04/2015

______, ______, ______Local Data Assinatura

Endereço para envio de correspondência:

Albertina Pimentel Lima PPG-ECO/CBIO/INPA

Instituto Nacional de Pesquisas da Amazônia - INPA Graduate Program in Ecology

Referee evaluation sheet for PhD thesis

“Title: “MACROECOLOGICAL PERSPECTIVES ON MAURITIA-DOMINATED WETLANDS IN THE AMAZON” Candidate: JOHN ETHAN HOUSEHOLDER Supervisor: Dr. Florian Karl Wittmann Co-supervisor:

Examiner: Hans ter Steege

Please check one alternative for each of the following evaluation items, and check one alternative in the box below as your final evaluation decision.

Needs Excellent Good Satisfactory Not acceptable improvement Relevance of the study ( x ) ( ) ( ) ( ) ( ) Literature review ( ) ( x ) ( ) ( ) ( ) Sampling design ( x ) ( ) ( ) ( ) ( ) Methods/procedures ( x ) ( ) ( ) ( ) ( ) Results ( x ) ( ) ( ) ( ) ( ) Discussion/conclusions ( ) ( x ) ( ) ( ) ( ) Writing style and ( ) ( x ) ( ) ( ) ( ) composition Potential for publication in ( x ) ( ) ( ) ( ) ( ) peer reviewed journal(s)

FINAL EVALUATION ( x ) Approved without or minimal changes

( ) Approved with changes (no need for re-evaluation by this reviewer)

( ) Potentially acceptable, conditional upon review of a corrected version (The candidate must submit a new version of the thesis, taking into account the corrections asked for by the reviewer. This new version will be sent to the reviewer for a new evaluation only as acceptable or not acceptable)

( ) Not acceptable (This product is incompatible with the minimum requirements for this academic level)

Edinburgh, 26/03/2015, Place Date Signature

Additional comments and suggestions can be sent as an appendix to this sheet, as a separate file, and/or as comments added to the text of the thesis. Please, send the signed evaluation sheet, as well as the annotated thesis and/or separate comments by e-mail to [email protected] and [email protected] or by mail to the address below. E-mail is preferred. A scanned copy of your signature is acceptable.

Mailing address:

Albertina Pimentel Lima PPG-ECO/CBIO/INPA Av. André Araújo nº 2936 69.067-375 - Manaus AM Brazil