Neogene paleoecology and biogeography of a Malvoid pollen in northwestern South America

Journal Pre-proof Neogene paleoecology and biogeography of a Malvoid pollen in northwestern South America

Bruno S. Espinosa, Carlos D'Apolito, Silane A.F. Silva-Caminha, Marcos G. Ferreira, Maria L. Absy PII:

S0034-6667(19)30112-5

DOI:

https://doi.org/10.1016/j.revpalbo.2019.104131

Reference:

PALBO 104131

To appear in:

Review of Palaeobotany and Palynology

Received date:

15 April 2019

Revised date:

9 September 2019

Accepted date:

24 October 2019

Please cite this article as: B.S. Espinosa, C. D'Apolito, S.A.F. Silva-Caminha, et al., Neogene paleoecology and biogeography of a Malvoid pollen in northwestern South America, Review of Palaeobotany and Palynology(2019), https://doi.org/10.1016/ j.revpalbo.2019.104131

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© 2019 Published by Elsevier.

Journal Pre-proof Neogene paleoecology and biogeography of a Malvoid pollen in northwestern South America

Bruno S. Espinosaa * ([email protected]), Carlos D’Apolitoa ([email protected]), Silane A. F. Silva-

([email protected]), Maria L. Absyb

Faculty of Geosciences, Universidade Federal de Mato Grosso,

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([email protected])

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Caminhaa ([email protected]), Marcos G. Ferreirab

Av. Fernando Corrêa da Costa s/n, Coxipó, Cuiabá-MT 78060b

Laboratório de Palinologia (COBIO), Instituto

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900, Brazil;

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Nacional de Pesquisas da Amazônia (INPA), Av. André Araújo 2936, Petrópolis, CEP 69067-375 Manaus-AM, Brazil;

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*Corresponding author

ABSTRACT

Western Amazonian landscapes evolved dynamically during the Neogene. Large wetlands developed responding to Andean uplift what promoted the rise and diversification of many plant groups. One such group is the well documented Malvoid pollen Malvacipolloides maristellae from the Miocene of northwestern South America. In the present contribution, we compared

Journal Pre-proof the botanical affinity among fossil and extant Malvoid, reconstructed past distributions of the taxa and their relative abundance throughout the Neogene-Quaternary, and interpreted the biogeographical and paleoecology of the group. We found similar pollen morphologies among the fossil and 14 extant Malvoids, mainly Allosidastrum, Sphaeralcea, Monteiroa,

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Malvella, and Wissadula. These belong to the Malveae tribe

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(subtribes Abutilinae and Malvinae), which are extra-Amazonian,

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mostly found in drier-colder settings, in full light environments

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(savannahs, forest edges), and tolerating varied oligotrophic and hydric stress soils. We recorded widespread Miocene populations

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of the fossil, from western Amazonia to coastal Venezuela, with

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high abundances in the early Miocene, when the group first appeared, then dropped significantly from the late Miocene

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onwards. The gradual demise of M. maristellae is attributed to the

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negative effects of brackish water inundations and the gradual increase of humidity and forest cover following the decline of wetlands that narrowed the open, light-demanding ecological niche exploited by M. maristellae. In the Pliocene-Quaternary, no records were found in western Amazonia, attesting to its final displacement outside the forest structure. In its northern extension (Venezuela and Colombia), the fossil survived for longer due to

Journal Pre-proof available open-dry environments that developed in the latest Neogene.

Keywords: Amazonia, Neogene, Malvaceae, Malveae, Paleoecology, Paleobiogeography

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1. INTRODUCTION

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The northwestern corner of South America responded to

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the Andean orogeny with dynamic changes in its geography and

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ecosystems in the last ~23 million years (Ma). During the early Miocene (23 to 16 Ma) and middle Miocene (16 to 11.6 Ma) the

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Andean forelands subsided and formed a vast wetland system of

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low gradient rivers, floodplains and mega-lakes—the Pebas system (Wesselingh et al., 2002; Hoorn et al., 2010). The Pebas

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environments predominated in western Amazonia and harbored a

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rich fauna (Monsch, 1998; Lundberg et al., 1998, 2010; Cozzuol, 2006; Salas-Gismondi, 2016; Antoine et al., 2007; Latrubesse et al., 2010; Negri et al., 2010; Aureliano et al., 2015; Wesselingh et al., 2002; Wesselingh, 2006; Wesselingh and Ramos, 2010; Gross et al., 2015; Linhares et al., 2017) and plant diversity akin to modern forests (Hoorn, 1993; Hoorn, 1994a, 1994b; Hoorn, 2006; Silva-Caminha et al., 2010; Salamanca et al., 2016; Leite et al., 2017).

Journal Pre-proof Global climate during the Miocene was warmer than that of today (Zachos et al., 2001; You et al., 2009; Zhang et al., 2013). Empirical climatic data from the Pebas phase is restricted to oxygen isotopes from bivalve shells that point to an intense hydrological cycle as in the present day, implying humid climate conditions during the early Miocene (Kaandorp et al., 2005).

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However, the orographic barrier that led to a wetter climate

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developed from the middle and late Miocene (Poulsen et al. 2010;

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Barnes et al. 2012). Vegetation data from pollen studies (Hoorn,

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1993; Hoorn, 1994a, 1994b; Hoorn, 2006; Silva-Caminha et al., 2010; Salamanca et al., 2016; Leite et al., 2017), despite still

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lacking knowledge of the majority of botanical affinities, and fossil

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wood from the Miocene Solimões Formation (Pons and De Franceschi, 2007; Kloster et al., 2015) provide evidence of lowland

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vegetation that can be attributed to Terra Firme and floodplain

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forests, as well as palm marshes and aquatic vegetation. In the early Miocene, however, spikes of the Malvaceae fossil pollen Malvacipolloides maristellae (Muller et al., 1987) Silva-Caminha et al., 2010 were hypothesized to indicate drier or more seasonal climatic conditions given the extra-Amazonian, dry habitat distribution of the related, extant taxon Abutilon (Salamanca et al., 2016). More recently, Hoorn et al. (2019) expanded the possible botanical affinities to include other Abutilinae genera and pointed

Journal Pre-proof to two scenarios for parental paleoenvironments, one typical of the Pebasian system such as freshwater lacustrine settings and openwater floodplains, the second being the newly formed Andean slope environments. Abutilon and related genera are herbs to subshrubs with a predominantly extra-Amazonian distribution in drier climates (Esteves and Takeuchi 2015; Hoorn et al., 2019),

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although some can also grow in parts of Amazonia and other

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humid forests like the Atlantic Forest in southeastern Brazil

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(Takeuchi and Esteves, 2012). Given the infrequent peak

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abundances of the fossil in the early to middle Miocene records in western Amazonia and Venezuela (Lorente, 1986; Salamanca et

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al., 2016; Hoorn et al., 2019), and in light of the dry habitats

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occupied by extant Abutilinae, there are possible climatic implications for the Pebas system that need testing. Here, we

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reconstruct the paleobiogeography of M. maristellae, carry out a

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morphometric study to assess possible botanical affinities and review the biogeography of extant related taxa in order to gain insights into paleoenvironments of the M. maristellae populations in northwestern Amazonia. We posit three simple scenarios for such paleoenvironments, 1) the Pebas system, 2) Andean slope environments, and 3) drier parts of Amazonia (i.e. cratonic area and pre-Pebas floodplains).

Journal Pre-proof 1.1.Malvacipolloides maristellae Malvacipolloides maristellae was formally described by Muller et al. (1987) as Echitricolporites maristellae, and later transferred to the genus Malvacipolloides Anzótegui and Garalla 1986 by Silva-Caminha et al., 2010 due to Echitricolporites Van der Hammen 1956 being an invalid genus. This pollen is

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characteristic for its spiny, 3–4-colporate morphology (Jaramillo

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and Rueda 2019), large spines, well developed costae (Muller et

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al., 1987), thicker exine underneath spines forming a “cushion”,

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and longer spines near colpi (Silva-Caminha et al., 2010). Lorente (1986) and Anzótegui and Garralla (1986) identified

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morphological similarity of Malvacipolloides with the Malvaceae.

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Malvaceae is a eurypalynous family, with pollen morphologies of diverse aperture types and numbers (3–5–6-colporate; 2–3–4-

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porate; colporoidate; periporate) as well as ornamentation

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(reticulate, foveolate, verrucate, spiny) (Salgado-Labouriau, 1973; Barth, 1975; Christensen, 1986; Cuadrado 2006). The subfamily Malvoideae, particularly tribe Malveae, possesses pollen with the greatest similarity to M. maristellae, given the spiny pattern of ornamentation and the swollen base of the exine beneath the spines (Saad, 1960; Barth, 1975). Examples of such morphology are Abutilon, Bakeridesia, Callianthe and Herissantia (Salamanca et al., 2016; Hoorn et al., 2019), which have been proposed to have

Journal Pre-proof probable affinities with M. maristellae. These taxa compose clades within tribe Malveae, particularly sub-tribes Abutilinae and Malvinae that have North American origins in the Paleogene with later migrations into South America during the Neogene (Hoorn et al., 2019).

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2. METHODS

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2.1.Botanical affinity

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In order to find the botanical affinity of M. maristellae we

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followed two approaches. First, we reviewed the available modern pollen identification guides, atlases and palynological studies in

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the Neotropics and searched for spiny-tricolp(or)ate morphologies.

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Second, the list of candidate taxa was collected in herbaria for morphometric comparisons carried out with multivariate statistics

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(see below). Our focus was primarily on spiny-tricolporate pollen,

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but also included colpate and stephanocolp(or)ate grains. There is a limited number of publications that illustrates and/or describes the complete pollen flora of a given area (e.g. the Barro Colorado pollen guide of Roubik and Moreno, 1991), or the Neotropics (Bush and Weng, 2007), therefore we also included more restricted publications. Some spiny-tricolporate pollen could be readily disregarded from our analysis because, despite matching the two basic characters (tricolporate and spiny), they differ significantly in

Journal Pre-proof morphology, e.g. the Asteraceae and Cordia spp. (Boraginaceae), among others.

2.2.Herbaria and laboratory procedures Pollen samples from herbarium vouchers were collected for 28 species belonging to 11 genera found in the literature revision

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(see Results). Herbaria visited were the Central Herbarium of the

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Federal University of Mato Grosso (UFMT), the Botanical

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Museum Herbarium in Curitiba (MBM), and the Herbarium of the

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National Institute for Amazon Research (INPA). Names were confirmed with Tropicos® (Tropicos.org, 2018) and updated when

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necessary. Floral buds and anthers were stored in paper envelopes

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and then subjected to acetolysis (Erdtman, 1960). Residues were mounted on slides following Salgado-Labouriau (1973) and

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deposited in the pollen reference collection of the Paleontology

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and Palynology Laboratory at UFMT. The list of species collected and analyzed can be found in Table 1.

2.3.Morphometric analysis Descriptions and measurements of pollen characters were performed with a Nikon E200 and photomicrographs were taken with a Canon EOS Rebel t5 on a Zeiss Axioplan2 microscope at 100× magnification (using a Plan Neofluar 1.30 oil objective lens

Journal Pre-proof and differential interference contrast [DIC]). Terminology followed Punt et al. (2007). Measurements were made in polar view because all fossil specimens are in polar position. Most extant specimens were also found in polar view only. A model of the generic morphology of the pollen studied here can be found in Fig. 1. The characters that were measured consisted of the following:

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equatorial diameter in polar view (Edm_pv), colpus aperture (Cpa),

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colpus length (Cpl), spine density (Ed), inter-spine distance (Id),

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apocolpium side (Ap), length of longest spine (Sl1), length of

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shortest spine (Sl2), width of wide base (Sw1), width of narrow base (Sw2), costa width (Cw), costa length (Cl), thickest columella

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thickness (C1), thinnest columella thickness (C2), nexine (Ne),

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columella height (Co), tectum (Te). Spine density (Ed) was measured by counting the number of spines in a given area of the

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grain (see Fig. 1). A total of 25 grains were measured per species

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when possible, this includes 25 randomly taken measurements of the grain dimensions (Edm_pv) and ten of all other characters. The equatorial diameter (Edm_pv) does not include the spine length. We also counted the number of apertures (colpores) and classified the spine shape according to three basic types detected (see Fig. 1). Fossil specimens measured for the morphometric study are from the Solimões Formation boreholes 1AS-27-AM (SilvaCaminha et al., 2010), 1AS-31-AM (Kachniasz and Silva-

Journal Pre-proof Caminha, 2016), 1AS-105-AM (Jaramillo et al., 2017), and the Patos outcrop (Latrubesse et al., 2010). Pollen dimensions from the holotype of M. maristellae, reported in Muller et al. (1987), were also used. All specimens analyzed, their measurements and metainformation can be found in Appendix Table 1. In total, 26 specimens of the fossil and 685 of extant genera were measured

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2.4.Multivariate analyses

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(11 genera and 28 species).

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A multivariate approach was taken to determine the similarity relationships of the fossil M. maristellae and extant

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genera. We applied Principal Components Analyses (PCA) to the

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data using the ‘vegan’ package (Oksanen et al., 2018) for the R statistical environment. Three PCAs were run with data prepared

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differently: PCA-1 contains the raw data; PCA-2 contains a log-

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transformed version of the raw data; and PCA-3 contains data where measurements were divided by Edm_pv. The latter was used to eliminate the effect of size, which was seen to be extremely large (see Results). We included in the analyses all characters that had at least two measurements per species and used the mean value per character per species. Apocolpium side (Ap) was not included because it implies different length relationships when grains are 3-,

Journal Pre-proof 4- or 5-aperturate (e.g. longer Ap in triaperturate grains, shorter Ap in 5-aperturate grains). Spine density (Ed) was not included because it showed consistently much higher values for the fossils than for extant species, which is likely a result of taphonomic

2.5.Distribution of extant genera

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compression of fossil pollen.

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We mapped extant genera listed from the botanical affinity

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comparisons using occurrences from the Global Biodiversity

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Information Facility (GBIF; GBIF.org 2018) and contrasted them against South American biomes (Olson et al., 2001; Hijmans et al.,

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2017). Bioclimatic variables were derived for each occurrence

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from WorldClim (Fick and Hijmans, 2017) using ‘raster’ (Hijmans 2018) for R (R Development Core Team 2018) and compared with

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means of the same variables from western Amazonia fossil

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localities (Appendix Table 2). For each extant genus, we also produced distribution

models using the bioclim algorithm. Models were run with the dismo package (Hijmans et al., 2017) for R and used the 20 bioclimatic variables from WorldClim plus altitude (Fick and Hijmans, 2017). Models used occurrences from GBIF, which were cleaned with CoordinateCleaner (Zizka et al., 2019) and duplicate records were deleted.

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2.6.Mapping the spatial and temporal distribution of Malvacipolloides maristellae The upper Tertiary pollen records of northern South America were revised and occurrences of M. maristellae were compiled (Appendix Table 2). Relative chronologies (biozones)

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vary slightly for each locality, therefore we standardized them

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using age markers from the palynological zonation of Jaramillo et

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al. (2011) (Appendix Table 3). Comparisons were made using the

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following Miocene time intervals: early (23.03 to 15.97 Ma), middle (15.97 to 11.63 Ma) and late (11.63 to 5.3 Ma). Along with

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occurrence, abundance data (pollen counts), when available, were

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used to create abundance maps for the early, middle and late Miocene and Pliocene in order to visualize trends in the temporal

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distribution of M. maristellae. Abundances were calculated per

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sample (proportion of M. maristellae relative to total pollen counts) then averaged among all samples from a time interval per site. Small pollen counts (<100) were not included. Sites belonging to one of the time intervals in northwestern South America but without the occurrence of M. maristellae were also searched and plotted in the maps (Appendix Table 4). Data from numerous sites from the literature, mainly from Venezuela (Lorente, 1986), were obtained from pollen diagrams, therefore these data are

Journal Pre-proof approximate percentages relative to pollen counts. Finally, we reviewed the Quaternary and Holocene pollen records from the Amazon and surrounding biomes in search for Malvaceae pollen with morphologies similar to M. maristellae (Appendix Table 4). This revision was restricted to publication with lists of taxa, detailed diagrams or raw counts available. We also searched for

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the extant genera in Pleistocene-Holocene records using the

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Neotoma Paleoecology Database (http://www.neotomadb.org).

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3. RESULTS 3.1.Botanical affinity

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We found 14 valid Malvaceae genera that match the

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colporate-spiny morphology of M. maristellae, these are the following: Abutilon, Allosidastrum, Bakeridesia, Bastardiopsis,

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Briquetia, Callianthe, Herissantia, Kearnemalvastrum, Malvella,

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Monteiroa, Sidastrum, Sphaeralcea, Tarasa and Wissadula (Table 2). These genera belong to tribe Malveae of the Malvaceae. Some other genera have similar morphologies, but apertures are colpate or porate only, colpi long, spines short, or a combination of these, therefore not a match with the fossil. Some of those morphologies are illustrated and described in the database of Bush and Weng (2007): Cordia curassavica (Boraginaceae), C. nodosa (Boraginaceae), Harrisia martini (Cactaceae), Aegiphila

Journal Pre-proof quararibeana (Lamiaceae), Robinsonella mirandae (Malvaceae), Scleronema micranthum (Malvaceae), Piranhea trifoliata (Picrodendraceae), Podocalyx loranthoides (Picrodendraceae), Coutarea hexandra (Rubiaceae) and Metternichia princeps (Solanaceae). Dombeya wallichii (Malvaceae) is similar overall but triporate (Bush and Weng, 2007).

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Kearnemalvastrum (Malvaceae) is generally similar to the

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fossil but of very restricted distribution (Appendix Fig. 1) with

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only two unique records in South America. Tarasa (Malvaceae) is

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restricted to high altitudes mostly in the Central Andes, its pollen can be tricolporate and similar to M. maristellae but is normally

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microspiny (or spinulose sensu Erdtman, 1952 (Punt et al., 2007))

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and with ornamented interspinal surfaces (Cuadrado and Boilini, 2006). We did not analyze the morphometrics of these two genera.

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Additionally, Briquetia was not found with available floral buds in

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any herbarium voucher checked. All the remaining genera have at least one species in our analyses (Table 1).

3.2.Multivariate analyses PCAs produced variation that is mostly condensed in the first axis with only minor variation in axis two. In PCA-1 (raw data), pollen diameter explained 95.5% of the variation of axis one (Fig. 2A). Diameters vary from 26 to 97 µm, smaller sizes are

Journal Pre-proof found in the fossil (26-(38.7)-54 µm) and in Sphaeralcea species (33–(51.3)–63 µm), which places them on the extremity of PCA-1 axis one (Fig. 2A). Smaller grains are also found in Monteiroa (43–(48.4)–56 µm) and Allosidastrum (45–(47.8)–52 µm) (Fig. 2A). In PCA-2 (log-transformed data), spine characteristics (Sl1,

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Sl2, Sw1, Id) and columella height (Co) explained 63.8% of the

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variation of axis one. Axis 1 polarized a similar group of genera as

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in PCA-1: Allosidastrum, Monteiroa and Sphaeralcea (Fig. 2B).

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Total spine length (Sl1) varies from 2.5 to 12 µm (fossil: 2.5– (3.8)–5.3 µm; Allosidastrum: 3–(3.5)–4 µm; Monteiroa: 3–(4.1)–5

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µm; and Sphaeralcea: 3–(5.1)–8 µm). Length of shortest spine

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(Sl2) varies from 1 to 8.5 µm (fossil: 1–(2.8)–3 µm; Allosidastrum: 2–(2.6)–3 µm; Monteiroa: 2–(3)–4 µm; and Sphaeralcea: 2–(3.7)–

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6.5 µm). Total spine width (Sw1) varies from 1 to 7.5 µm (fossil:

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1–(2.5)–3 µm; Allosidastrum: 1.5–(1.8)–2 µm; Monteiroa: 2– (2.7)–3 µm; and Sphaeralcea: 1–(2.3)–4 µm). Inter-spine distance (Id) varies from 1 to 16 µm (fossil: 1–(2.3)–4 µm; Allosidastrum: 1.5–(2.1)–3 µm; Monteiroa: 1.5–(2.6)–4 µm; and Sphaeralcea: 1.7–(3.4)–6 µm). Finally, columella height (Co) varies from 0.2 to 3 µm (fossil: 0.2–(0.57)–1 µm; Allosidastrum: 0.7–(0.8)–1 µm; Monteiroa: 0.5–(0.6)–1 µm; and Sphaeralcea: 0.5–(0.7)–1 µm).

Journal Pre-proof In PCA-3 (measurements proportional to pollen size), spine characteristics (Sl1, Sl2 and Id) explained 70.4% of the variation of axis one. A greater number of genera are closer to M. maristellae in PCA-3: Monteiroa, Sphaeralcea, Malvella, Callianthe and Wissadula (Fig. 2C). Measurements proportional to pollen size are shown in Fig. 3.

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Categorical variables (number of colpores and spine type;

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Fig. 4) were used to complement the metric data multivariate

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analyses. They show that a majority of the genera is exclusively or

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almost exclusively tricolporate, and that most spines belong to the simplest morphology (type 1, Fig. 1). The fossil displays all colpus

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numbers (3, 4 and 5) but mostly is tricolporate; based on this

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character all genera would be matches with the fossil, except perhaps Malvella and Monteiroa that have a colpus number

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centered at four, contrary to the three in the remaining genera.

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Interestingly, we only found the fossil and Wissadula to display five colpores. Regarding spine type, the fossil only has type 1, all genera would fit the fossil, except perhaps Bakeridesia and Callianthe that only have type 2 (Fig. 1). Our three Callianthe (Table 1) plus C. striata and C. monteiroi analyzed by Hoorn et al. (2019; Plate I, fig. 7-10 and Plate IV, Fig. 6) have spines with a rounded tip (type 2).

Journal Pre-proof 3.3.Distribution of extant genera More than 5,560 unique occurrences were found for the extant genera; they exhibit a predominantly extra-Amazonian distribution with few occurrences in southern and eastern Amazonia near ecotone regions (Appendix Fig. 1). Various South American biomes harbor populations of the studied genera: the

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cerrado, caatinga, Atlantic forest, chaco, pampas and montane/pre-

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montane Andean forests. Wide altitudinal ranges characterize the

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genera, from sea-level to ~4,600 m.a.s.l, however the bulk of

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occurrences is restricted to elevations below 700 m.a.s.l. (Fig. 5). The climate, when compared to present-day western Amazonia,

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was drier and colder (Fig. 6). Bioclimatic data from Amazonian

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sites and the locations of combined genera are consistently different from each other: annual precipitation

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(Amazonian=~2,500 mm, extant genera=~1,100 mm; t-test,

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df=29.5, p<0.001); precipitation of the driest quarter (Amazonia=~400 mm, extant genera=~115 mm; t-test, df=29.1, p<0.001); mean annual temperature (Amazonia=~26°C, extant genera=~21°C; t-test, df=56.2, p<0.001); and mean temperature of the coldest month (Amazonia=~19.8°C, extant genera=~12.1°C; ttest, df=36, p<0.001). When analyzed individually, extant genera are also significantly different from modern Amazonian values (p<0.001), except the precipitation of the driest quarter for

Journal Pre-proof Monteiroa (mean=~360 mm; t-test, df=44.6, p>0.1); and the mean annual temperature (~25.6°C; t-test, df=33.7, p=0.37) and mean temperature of the coldest month (~20°C; t-test, df=50, p>0.5) for Allosidastrum. There were only two sites for Kearnmalvastrum; both had climate similar to present-day western Amazonian sites, but statistical testing is not robust with such a small sample size.

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Distribution models of the combined extant genera (Fig. 7)

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indicate that the greatest climatic suitability encompasses areas in

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the present-day central Brazilian cerrado, Atlantic Forest, caatinga,

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southern Amazonia and ecotone regions (including the Chiquitano dry forest area and the Beni savannah), several small regions in the

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high Andes and coastal regions of Colombia and Venezuela.

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Probable occurrences inside the Amazon biome are restricted to the southwestern region and are driven by the present-day

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distributions of Abutilon, Allosidastrum, Briquetia, Dombeya,

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Sidastrum and Wissadula (Appendix Fig. 2). A smaller probability also exists in the dry corridor of eastern Amazonia, which is driven by the present-day distribution of Allosidastrum and Briquetia (Appendix Fig. 2). The core of the Amazon, and especially western Amazonia where there are many fossil localities recording M. maristellae, have negligible occurrence probabilities for the extant genera.

Journal Pre-proof There is limited information available on specific habitats for species of the genera above. Collections with notes on environment, habitat, edaphic and overall vegetation characteristics (‘habitat’ column in GBIF records) are summarized in Table 3. These habitats indicate that the Malveae genera studied are mostly shade-intolerant and tolerate poor soils and hydric stress (both dry

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and waterlogged soils). In most cases they are found in open

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savannah and dry forest vegetation types, and when in dense

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evergreen forests, they tend to be found in clearings or forest

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edges.

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3.4.The spatial and temporal distribution of

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Malvacipolloides maristellae The Miocene distribution of M. maristellae was

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reconstructed based on 253 pollen localities in northwestern South

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America, of which 103 contained the fossil (Fig. 8; Appendix Table 2). The fossil is present in Venezuela, Colombia, Brazil and Peru since the early Miocene (n=50, or 50% of all early Miocene sites), throughout the middle (n=39, or 39.4% of all middle Miocene sites) and late Miocene (n=18, or 28.1% of all late Miocene sites). It has also been found in two Pliocene localities in Venezuela.

Journal Pre-proof Amongst all fossiliferous localities, mean abundance data show a decrease from the early to late Miocene (early: 3.1%; middle: 1.73%; late to 1.43%), being significant from early to late (t-test, df=49, p<0.03), but not from early to middle (t-test, df=61.6, p>0.07) or middle to late (t-test, df=53.8, p>0.4). Maximum averages per site were of ~15.5% in the early Miocene,

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~12.6% in the middle and 2.6% in the late Miocene. This decrease

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in frequency of occurrence and mean abundance per site is clearly

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visible in the abundance maps of Fig. 8.

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In addition, infrequent peak abundances were observed in many samples. In the early Miocene, there are samples in the

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Colombian Amazon with ~20% (Salamanca et al., 2016), in the

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Colombian llanos with up to 27.5% (Hoorn et al., 2019), and in Venezuela with 40% in one locality (B-188) and >10% in three

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other localities (Lorente, 1986) (Appendix Table 3). In the middle

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Miocene in the Solimões Formation and in Venezuela, these abundances top around 6%, but in the Colombian llanos there are still samples with peaks up to ~33%. In the late Miocene, however, the maximum abundances in samples drop to 2%-8% in all regions (Appendix Table 3). The 89 Quaternary pollen studies of Amazonia and other South American biomes reviewed in this study (Fig. 8; Appendix Fig. 3 and Table 4) lacked any of the Malveae genera identified as

Journal Pre-proof similar to M. maristellae. One high Andean locality was found to contain Abutilon-type pollen (Wille et al., 2001), but that could not be confirmed, and one site in southern Brazil (Masetto and Lorscheitter, 2016) has a fractured Malvaceae pollen similar to the genera studied here but described as triporate. No other locality recorded morphologies similar to M. maristellae, including biomes

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where many species of the extant genera are living today

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(Appendix Fig. 1 and 3).

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4. DISCUSSION

Because the fossil was found to present 3, 4 and 5

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apertures, we will refer to it as the M. maristellae complex, which

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represents a pollen group. We prefer that approach rather than including in our analyses the southern South American

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stephanocolporate morphologies like Baumannipollis Barreda

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1993, as we are not analyzing those specimens herein.

4.1.Botanical affinity interpretations All extant genera assessed have the same basic morphological configuration similar to the M. maristellae complex (Plates I-III) and hence could be potentially assigned as botanical affinities. One complication in determining botanical affinity is intra-specific variation of the morphological space. Some species

Journal Pre-proof of Sphaeralcea, Callianthe, Herissantia and Wissadula appear separated from each other in the PCAs (Fig. 2), meaning species of one genus can be closer to species of other genera rather than to other species of its own genus. Such complexity hampers a clear generic delimitation. Problems in generic delimitations have arisen in some of the published Malveae phylogenies (e.g. Tate et al.

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2005; Areces-Berazain and Ackerman, 2016). Nevertheless,

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morphometric analyses have shown a tendency for Allosidastrum,

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Sphaeralcea, Monteiroa, Malvella, and Wissadula as best matches.

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Wissadula and the fossil were the only groups that contained 5colporate specimens; therefore, an affinity with Wissadula is

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highlighted.

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Callianthe seems to have stable spine morphology among the three species herein (Table 1) plus two different species in

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Hoorn et al. (2019). They all differ from the fossil spine type;

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therefore, we disregard Callianthe as a potential match. Size played a major role in separating some genera. Size is

an important measure in pollen morphology but can be affected by some processes like the phase of ontogenetic development (larger sizes in mature pollen). All floral buds and anthers collected for our analyses were completely formed, pollen exine displayed full stratification, was rigid and spines were large and well formed, which are evidence of late ontogeny in pollen (Takahashi and

Journal Pre-proof Kouchi, 1988; Blackmore et al., 2007). Moreover, many taphonomic aspects can impact fossil pollen preservation like thermal maturation (Traverse, 2007) and pollen fracturing (Arai, 2017). However, the M. maristellae specimens measured were well preserved, entire, with fully developed stratification, entire spines, no signs of corrosion and displayed pale yellow exine (=low

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thermal maturation; Traverse, 2007) (Plate I).

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Hoorn et al. (2019) described specimens of M. maristellae

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in detail. They found a similar size range (34.9–43.3 µm) and

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overall similar measurements for spines and exine as in the present study. The authors defined clear differences in morphology among

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M. maristellae and Asteraceae and the subfamilies of Malvaceae,

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except Malvoideae. Within Malvoideae, Hoorn et al. (2019) highlighted the tricolporate genera Abutilon, Bakeridesia,

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Callianthe and Herissantia as close relatives to the fossil. Only

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tricolporate grains of M. maristellae were recorded by Hoorn et al. (2019). Here, we show that both fossil and extant genera vary from three- to five-colporate and at least 14 genera match the M. maristellae complex. Critically, the fact that all colpore numbers are present in the fossil record could indicate that M. maristellae represents a group of Malvoideae genera including the subtribe Abutilinae (Abutilon, Callianthe, Malvella, Wissadula), but also subtribe Malvinae (Sphaeralcea and Monteiroa (Tate et al., 2005)).

Journal Pre-proof

4.2.Neogene distribution and paleoecology of the Malvacipolloides maristellae complex The paleodistribution of M. maristellae in northwestern South America shows the following marked pattern: a) wider distribution during the early and middle Miocene; b) highest

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relative abundances in the early Miocene; c) rare occurrences and

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low abundance in the late Miocene-Pliocene; and d) absence in the

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late Pleistocene/Holocene pollen records of Amazonia (Fig. 8,

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Appendix Tables 2, 3 and 4). Furthermore, we noticed no distribution of extant genera identified as similar to the fossil in

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western Amazonia (Fig. 7, Appendix Fig. 1 and 2). This pattern

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can be summarized as a rapid expansion following the appearance of the fossil in the early Miocene, and a later gradual decline until

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complete extirpation in western Amazonia. The same trend is

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observed in Venezuela (Fig. 8), but in that region, extant genera with affinity are still recorded (Fig. 7, Appendix Fig. 1 and 2). This paleodistribution evolution reflects the development and demise of the Pebas system of wetlands in western Amazonia (Wesselingh et al., 2002; Hoorn et al., 2010). The system had its climax in the early and middle Miocene with mega-lakes and marshes, which were followed by an active megafan-avulsive system in the late Miocene and Pliocene (Latrubesse et al., 2010; Gross et al., 2011).

Journal Pre-proof We suggest, in line with Hoorn et al. (2019) and based on the results presented here, that the M. maristellae pollen group represents herbaceous plants that occupied the more open environments, which favored shade-intolerant plant groups, much like the extant Abutilinae and Malveae genera that opportunistically occupy disturbed or naturally open areas like

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savannahs, dry forests and clearings, among others (see Results

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3.3.). This interpretation favors scenarios 2 and 3 (see

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Introduction), i.e. newly formed Andean slope environments and

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drier parts of Amazonia (sensu Hoorn et al., 2019), and therefore is indicative of an efficient transport from these areas into

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depositional sites in the Pebas system. In addition, some authors

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have suggested wet-dry seasonality (Latrubesse et al., 2010; Salamanca et al., 2016), which could create favorable

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environments for Malveae populations in the Pebas settings.

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Open environments were also present in the late MiocenePliocene when the more prominent avulsive style created a complex of rivers with lakes, swamps, internal flood basin deltas and floodplains (Latrubesse et al., 2010) that continued to support populations of M. maristellae, despite them already being in decline. In the northernmost reach of the wetlands system, in Venezuela, the decreasing abundance trend from early Miocene to

Journal Pre-proof Pliocene also exists (Fig. 8) but was not followed by a complete disappearance of the group in that region. The Venezuelan savannahs presently harbor some genera we identified as related (Fig. 7, Appendix Fig. 1 and 2). The origin of this savannah region is yet to be confirmed but most likely was between the late Miocene and Pliocene/early Pleistocene (Jaramillo and Quiroz,

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2012). It would have been related to climatic change (cooling and

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drying) and in synchronicity with the development of dry belts in

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central and southern South America (Simon et al., 2009; Palazzesi

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et al., 2014), as well as globally (Strömberg et al., 2011; Pound et al., 2012; Herbert et al., 2016). Moreover, during the Pliocene,

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extensive coastal plain settings developed in Venezuela (Lorente,

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1986), conducive to open vegetation structures. Pocknall et al. (2001) mentions ‘savannah grasses’ as important palynomorphs in

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the late Miocene to Pleistocene sections of eastern Venezuela.

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Both savannahs and coastal plains provided open habitats for the maintenance of the Malveae populations following their demise in western Amazonia. Later stages of the Neogene were more forested than the early and middle Miocene in western Amazonia due to geomorphological conditions, thus narrowing the ecological niche suitable for M. maristellae populations. Pliocene and early Pleistocene pollen records in Amazonia are almost non-existent; the few that exist point to vegetation types of the lowland

Journal Pre-proof Amazonian forests (Nogueira et al., 2013; D’Apolito et al., 2018). Given all of the above, the M. maristellae complex vanished from Amazonia in the late Neogene due to increasing humidity driven by the Andean orographic effect (Poulsen et al., 2010; Barnes et al., 2012) as well as forest structure densification, whereas in Colombia/Venezuela the fossil remained with the development of

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open and dry environments.

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4.2.1. An alternative hypothesis for the paleoecology of

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the Malvacipolloides maristellae complex In spite of strong support for the hypothesis above, an

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alternative idea has to be explored - that the populations of M.

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maristellae directly inhabited the Pebas aquatic settings (hypothesis 1, see Introduction). In favor of this idea, there are two

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main arguments.

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First, extant genera are palynologically silent to underrepresented in modern spectra even where they occur (Appendix Table 4), unlike Miocene localities where high abundance peaks are observed. Proximity to sedimentation environments leads to rapid transport, preservation and higher fossilization potential (Prentice, 1985; Sugita, 1994). Hence, the fossil populations could be specialized in shore habitats, belonging to the hydroseral community. Indeed, many extant species can be

Journal Pre-proof found thriving in waterlogged habitats (Table 3). Hoorn et al. (2019) showed that at many sites, M. maristellae can be found together with freshwater taxa, including high abundances of freshwater algae, and in open-water settings. Second, M. maristellae populations were destabilized by marine flooding episodes (Salamanca et al., 2016; Hoorn et al.,

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2019) that happened in northwestern South America during the

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early and middle Miocene (Hoorn, 1993; Boonstra et al., 2015;

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Salamanca et al., 2016; Jaramillo et al., 2017; Linhares et al.,

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2017). In fact, the Mariñame sequence in southern Colombia recorded the disappearance of abundant Malvacipolloides at the

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onset of estuarine conditions (Salamanca et al., 2016; Hoorn et al.,

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2019), which was interpreted as salinity intolerance. An interesting example in that regard was germination experiments with

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Sphaeralcea bonariensis, they showed intolerance to increasing

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salinity levels (Sobrero et al., 2014). If we assume M. maristellae occupied marginal habitats (marshes, lake margins and floodplains), a direct impact of higher base level can be expected, and in brackish inundation scenarios, large-scale mortality of these populations could explain the spatial and temporal decline in the paleodistribution (Fig. 8). In this scenario, the interpretation that M. maristellae populations directly inhabited aquatic settings could be advanced.

Journal Pre-proof In either scenario, drier peripheral areas or wetlands, light availability, soil use plasticity and disturbance tolerance would be primary drivers of the ecology of M. maristellae populations.

4.3. Insights into the historical biogeography of the Malvacipolloides maristellae complex and tribe

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Malveae in South America

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Hoorn et al. (2019) reconstructed the biogeography of M.

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maristellae using a combination of fossil record and molecular

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phylogenetics of Malvoideae. They found strong support for a monophyletic tribe Malveae and the two subtribes Malvinae and

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Abutilinae, but not for genera including Abutilon, Bakeridesia and

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Callianthe. The earliest inferred arrival of M. maristellae in South America, according to Hoorn et al. (2019), would range from 22.5

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to 6.8 Ma (and is centered around 14 Ma) in either the Abutilon or

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Callianthe clades. Three of the genera we obtained as matches with the fossil belong to the Abutilinae. Allosidastrum and Wissadula are in close alliance with Abutilon, thus any of them would be indicating similar age ranges as proposed by Hoorn et al. (2019). Malvella is more basal in the phylogeny and could potentially indicate Oligocene ages (~27 Ma) for the arrival. A second group belongs to subtribe Malvinae and includes Sphaeralcea and Monteiroa. The latter is associated with the

Journal Pre-proof Sphaeralcea alliance that also includes Tarasa (Tate et al., 2005). The Sphaeralcea alliance is more basal within Malveae (Tate et al., 2005; Donnell et al., 2012), with maximum split ages estimated from the middle Miocene (Hoorn et al., 2019) to the early Oligocene, ~32 Ma (Areces-Berazain and Ackerman, 2016). The fossil record of pollen similar to zonocolporate-spiny

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Malveae includes not only M. maristellae from ~17.7 Ma in

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northwestern South America (Jaramillo et al., 2011), but also many

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morphotypes from southern South America. M. comodoroensis

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Barreda, 1993 appears in the Chenque Formation (Argentina) with an estimated basal age around 19.7 Ma (Cuitiño et al., 2015). The

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fact that Malvacipolloides appears more or less synchronously in

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northern Colombia/Venezuela (Muller, 1981; Jaramillo et al., 2011) and southern Argentina (Barreda, 1993) during the early

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Miocene indicates a rapid dispersal and/or radiation of tribe

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Malveae in this period. This is in agreement with Mautino et al. (2004) who described a rich palynoflora assignable to tribe Malveae from the middle Miocene of Argentina. The affinities of this southern Malveae pollen include Bastardia and Wissadula (M. densiechinata in Anzótegui and Garralla, 1986), an unnamed fossil pollen of Sphaeralcea (Anzótegui and Garralla, 1986), and the record of Baumannipollis variaperturaus Barreda, 1993, related to Bastardia by Mautino et al. (2004). All these Malveae taxa belong

Journal Pre-proof to lineages arising in the Oligocene and particularly the Miocene (Areces-Berazain and Ackerman, 2016; Hoorn et al., 2019). Thus, evidence points to a Malveae group of relatable taxa from northern to southern South America arriving between the Oligocene and early Miocene and successfully diversifying from the middle Miocene. This diversification is attributed to Andean mountain-

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building and climatic cooling and drying (Hoorn et al. 2019),

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5. CONCLUSIONS

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which created habitats preferred by extant Malveae genera (Fig. 7).

The reconstructed biogeography of the Malvoideae fossil

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pollen Malvacipolloides maristellae in northwestern South

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America showed widespread populations from western Amazonia all the way to coastal Venezuela during the Miocene. An attempt to

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establish botanical affinities with extant Malvaceae yielded 14

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genera, with greatest similarity to Allosidastrum, Sphaeralcea, Monteiroa, Malvella, and Wissadula, all of which belong to the tribe Malveae (subtribes Abutilinae and Malvinae). These genera are extra-Amazonian, are mostly found in drier and colder settings like savannahs, dry forests, forest edges and open areas in full light, and tolerate soils with varied oligotrophic and hydric stress. Throughout their paleogeographical extension, the populations in the early Miocene recorded high abundances in many localities,

Journal Pre-proof which then dropped off significantly from the late Miocene/Pliocene. We linked this trend to two factors: the negative effects of brackish water inundations (Salamanca et al., 2016; Hoorn et al., 2019) and the gradual increase in humidity (Poulsen et al., 2010; Barnes et al., 2012). The higher humidity led to increased forest cover following the demise of the Pebas wetlands,

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which limited the open, light-demanding ecological niche

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exploited by the M. maristellae pollen group. In the Pliocene and

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Quaternary, there is a consistent absence of the fossil in western

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Amazonia, attesting to its final displacement outside the forest structure. In its northern extension in Venezuela and Colombia, the

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fossil survived for longer as a result of available open and dry

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environments that developed in the latest Neogene.

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ACKNOWLEDGEMENTS

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We sincerely thank Carina Hoorn and an anonymous reviewer for their valuable comments that improved the first version of our manuscript. We also thank Fátima Leite and Rogério Rubert for fruitful discussions and the staff of the UFMT, INPA and MBM herbaria for their help. The authors are grateful for funding from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT) [DCR grant

Journal Pre-proof number 568838/2017 to C.D.; and CNPq/476020/2013/1 to S.A.F.S.C and C.D].

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FIGURE CAPTIONS

Journal Pre-proof Figure 1 - Schematic model of the tricolporate and spiny pollen morphology of Malvacipolloides maristellae and extant tribe Malveae of the Malvaceae (adapted from Barth 1975). A) Grain in polar view. B) Detail of spine and aperture in cross section. C) Detail of spine showing columellae through tectum. D) Spine type 1 (acute end). E) Spine type 2 (rounded end). Edm_pv (equatorial

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diameter in polar view); Cpa (colpus aperture); Cpl (colpus

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length); Ed (spine density); Id (inter-spine distance); Ap

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(apocolpium side); Sl1 (length of longest spine); Sl2 (length of

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shorter spine); Sw1 (width of large base); Sw2 (width of short base); Cw (costa width); Cl (costa length); C1 (thickest columellae

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thickness); C2 (thinnest columellae thickness); Ne (nexine); Co

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(columellae); Te (tectum).

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Figure 2 - Principal Component Analyses (PCA) of morphometric

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data comparing fossil pollen Malvacipolloides maristellae and extant Malvaceae genera. A) PCA with raw data. B) PCA with logtransformed data. C) PCA with measurements divided by the equatorial diameter. Numbers in parentheses along axes 1 and 2 are proportion of explained variation. Arrows show variables: Edm_pv (equatorial diameter in polar view); Id (inter-spine distance); Sl1 (length of longest spine); Sl2 (length of shortest spine); Sw1 (width of large base); Sw2 (width of short base); C1

Journal Pre-proof (thickest columellae thickness); C2 (thinnest columellae thickness); Ne (nexine); Co (columellae).

Figure 3 - Boxplots with proportion of measurements relative to equatorial diameter for the fossil grains of Malvacipolloides maristellae and extant genera of Malvaceae (Table 1). Raw

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measurements can be found in Appendix Table 1. mm= M.

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maristellae; ab= Abutilon; al= Allosidastrum; bk= Bakeridesia;

-p

bs= Bastardiopsis; c= Callianthe; h= Herissantia; ma= Malvella;

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mo= Monteiroa; si= Sidastrum; sp= Sphaeralcea; w= Wissadula.

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Figure 4 - Proportion of aperture number and spine type (see Fig.

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1) for the fossil Malvacipolloides maristellae and genera analysed in this study. 3c3p = tricolporate, 4c4p = four-colporate, 5c5p =

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five-colporate.

Figure 5 - Elevation data for the extant genera studied (data from WorldClim; Fick and Hijmans, 2017). Dashed line is the mean value from western Amazonia sites. ab = Abutilon; al=Allosidastrum; bk= Bakeridesia; bs = Bastardiopsis; c=Callianthe; h= Herissantia; ma= Malvella; mo= Monteiroa; si=Sidastrum; sp=Sphaeralcea; t=Tarasa; w=Wissadula.

Journal Pre-proof Figure 6 - Bioclimatic data for the extant genera studied here (data from WorldClim, Fick and Hijmans 2017). Dashed line is the mean value from western Amazonia sites. A) Annual precipitation (mm). B) Mean annual temperature (ºC). C) Temperature of the coldest month (ºC). D) Precipitation of the driest quarter (mm). ab = Abutilon; al=Allosidastrum; bk= Bakeridesia; bs = Bastardiopsis;

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c=Callianthe; h= Herissantia; ma= Malvella; mo= Monteiroa;

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si=Sidastrum; sp=Sphaeralcea; t=Tarasa; w=Wissadula

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Figure 7 - Modelled distribution for all extant genera of Malveae found as potential matches for Malvacipolloides maristellae (Table

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2). Models are overlapped (individual maps are in Appendix Fig.

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2). Color code shows probability of occurrence. Solid black line is outline of the Amazon biome based on WWF Ecoregions (Olson et

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al., 2001) and solid grey lines are savannah or other dry forests

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within Amazonia (adapted from Adeney et al., 2016).

Figure 8 - Maps showing the relative abundance of M. maristellae (open circles) and its absence (red crosses) in the NeogeneQuaternary of western South America. Light blue shaded area A), B) and C) is the approximate extension of the Pebas system adapted from Hoorn et al. (2010). All red crosses in map D) are from late Pleistocene-Holocene records (see also Appendix Table 4

Journal Pre-proof and Appendix Fig. 3), and open circles in coastal Venezuela are Pliocene localities.

PLATE I - (1,2) Malvacipolloides maristellae (3c3p) (1AS-105AM) (EF:Y33), (3,4) Malvacipolloides maristellae (4c4p) (1AS105-AM) (EF:V45-3/4), (5,6) Malvacipolloides maristellae (5c5p)

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(1AS-105-AM) (EF:S38), (7,8) Abutilon ramiflorum (PALMA

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586) (EF:H29-3), (9,10) Allosidastrum pyramidatum (PALMA

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999) (EF L17), (11,12) Bakeridesia esculetum (PALMA 588)

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(EF:N16), (13,14) Bastardiopsis densiflora (PALMA 588) (EF:F24-1), (15,16) Callianthe amoena (PALMA 986) (EF:P24),

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(17,18) Callianthe bedforniana (PALMA 897) (EF:U14-1),

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(19,20) Callianthe rufinerva (PALMA 897) (EF:G30-3).

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PLATE II - (1,2) Herissantia crispa (PALMA 596) (EF:L21-1),

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(3,4) Herissantia intermedia (PALMA 898) (EF:O14-3), (5,6) Herissantia nemoralis (PALMA 899) (EF:X18), (7,8) Herissantia tiubae (PALMA 597) (EF:M24-2), (9,10) Malvella lepidata (PALMA 967) (EF:P14-3), (11,12) Monteiroa bullata (PALMA 969) (EF:O14), (13,14) Monteiroa glomerata (PALMA 970) (EF:U33-4), (15,16) Monteiroa ptarmicifolia (PALMA 1071) (EF:L31-2), (17,18) Sidastrum multiflorum (PALMA 923)

Journal Pre-proof (EF:N26-2), (19,20) Sphaeralcea australis (PALMA 902) (EF:P15-3).

PLATE III - (1,2) Sphaeralcea bonariensis (INPA 94915) (EF:N33-2), (3,4) Sphaeralcea chenopodifolia (PALMA 900) (EF:K14), (5,6) Sphaeralcea crispa (PALMA 903) (EF:E22), (7,8)

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Sphaeralcea lacinata (PALMA 901) (EF:L19), (9,10) Sphaeralcea

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mendocina (PALMA 904) (EF:N15), (11,12) Wissadula decora

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(PALMA 906) (EF:O22-3), (13,14) Wissadula grandifolia

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(PALMA 908) (EF:N17-2), (18,16) Wissadula indivisa (PALMA 907) (EF:L7-1), (17,18) Wissadula paraguariensis (PALMA 617)

na

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(EF:M15), (19,20) Wissadula periplocifolia (INPA).

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APPENDIX FIGURES AND TABLE CAPTIONS

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Appendix Figure 1 – Distribution of extant genera from Table 2. Background map shows South American biomes after Olson et al., (2001).

Appendix Figure 2 – Distribution models of extant genera from Table 2. Color code is probability of occurrence. Outline is the Amazon biome based on WWF Ecoregions (Olson et al., 2001).

Journal Pre-proof Appendix Figure 3 – Pleistocene-Holocene records revised in search for Malveae genera (see main text). Background map shows South American biomes after Olson et al., (2001).

Appendix Table 1 – Raw morphometric data from Malvacipolloides maristellae and extant Malveae genera (see

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Table 1).

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Appendix Table 2 – Relative abundance of Malvacipolloides

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maristellae of all sites used in Fig. 8 (see Methods).

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Appendix Table 3 – Raw pollen counts of Malvacipolloides

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(2011).

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maristellae per section and their pollen zones after Jaramillo et al.

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Appendix Table 4 – Miocene to Quaternary sites revised from the literature where Malvacipollodies maristellae and extant Malveae genera (Table 2) are absent.

Journal Pre-proof Table 1. List of extant species and herbarium information of all species collected for pollen analyses and morphometric comparisons with fossil pollen of Malvacipolloides maristellae. Herbarium number

Accepted species name

12.973 204430

Abutilon ramiflorum Allosidastrum pyramidatum

MBM

29452

Bakeridesia esculenta

UFMT

37.775

Bastardiopsis densiflora

INPA

n.a.

Bastardiopsis densiflora

MBM

230513

MBM

49341

MBM

ro

-p

re

Callianthe amoena

lP

ur

87711

Callianthe bedfordiana

Callianthe rufinerva

6.787

Herissantia crispa

INPA

n.a.

Herissantia crispa

INPA

n.a.

Herissantia crispa

MBM

15069

Herissantia nemoralis

UFMT

6.788

Herissantia tiubae

MBM

262214

Herissantia intermedia

MBM

92945

Malvella lepidota

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UFMT

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UFMT MBM

na

Herbariu m

Taxonomi c authority A. St.-Hil. Krapov., Fryxell & D.M. Bates (A. St.Hil.) Monteiro (Hook. & Arn.) Hassl. (Hook. & Arn.) Hassl. (K. Schum.) Donnell (K. Schum.) Donnell (K. Schum.) Donnell (L.) Brizicky (L.) Brizicky (L.) Brizicky (A. St.Hil., Juss. & Cambess.) Brizicky (K. Schum.) Brizicky (Hassl.) Krapov. (A. Gray) Fryxell

Journal Pre-proof 788

Monteiroa bullata

MNRJ

30443

Monteiroa glomerata

MNRJ

198152

Monteiroa ptarmicifolia

MBM

58295

Sidastrum multiflorum

MBM INPA

172364 19379

Sphaeralcea australis Sphaeralcea bonariensis

MBM

45691

MBM

110956

Sphaeralcea chenopodifolia Sphaeralcea laciniata

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MBM

(Ekman) Krapov. (Hook. & Arn.) Krapov. (A. St.-Hil. & Naudin) Krapov. (Jacq.) Fryxell Speg. (Cav.) Griseb. Rodrigo

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ur

na

lP

re

-p

ro

(K. Schum.) Krapov. MBM 27767 Sphaeralcea crispa Hook. & Baker f. MBM 217595 Sphaeralcea mendocina Phil. MBM 196230 Wissadula decora S. Moore MBM 294097 Wissadula grandifolia Baker f. ex Rusby MBM 119582 Wissadula indivisa R.E. Fr. UFMT 15.761 Wissadula paraguariensis Chodat INPA n.a. Wissadula periplocifolia (L.) C. Presl ex Thwaites MBM 294097 Wissadula subpeltata (Kuntze) R.E. Fr. Herbaria codes: UFMT = Universidade Federal de Mato Grosso (CuiabáMT, Brazil); INPA = National Institute for Amazon Research (ManausAM, Brazil); MBM = Curitiba Botanical Gardens (Curitiba-PR, Brazil).

Journal Pre-proof Table 2. List of taxa with spiny-colporate morphologies similar to Malvacipolloides maristellae. Taxon

Taxonomic authority Mill.

Abutilon

Reference

type

Barth (1975) Atlas

Abutilon aff (Miq.) lanatum= (Callianthe Donnell lanata)

Barth (1975) Atlas

Abutilon angulatum

(Guill. & Perr.) Mast.

Christensen (1986)

Abutilon anodoides

A. St.-Hil. & Milla (2006) Naudin

Paper

Abutilon cf. schenckii (K. Schum.) = (Callianthe Donnell schenckii)

ro

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Dissertation Atlas

Abutilon fraseri

(Hook. f.) Walp.

Christensen (1986)

Paper

Abutilon hirtum

(Lam.) Sweet

Christensen (1986)

Paper

(A. St.-Hil.) Donnell

Barth (1975) Atlas

Planch.

Christensen (1986)

Abutilon mullerifriderici = (Calliathe mulleri-friderici)

(Gürke & K. Schum.) Donnell

Barth (1975) Atlas

Abutilon otocarpum

F. Muell.

Christensen (1986)

Paper

Abutilon pauciflorum (A. St.-Hil.) = (Callianthe Dorr pauciflora)

Saba (2007)

Dissertation

Abutilon peltatum

K. Schum.

Milla (2006)

Dissertation

Abutilon purpurascens

(Link) K. Schum.

Milla (2006)

Dissertation

Abutilon rufinerve = (Callianthe

(A. St.-Hil.) Donnell

Milla (2006)

Dissertation

-p

re

lP

na

Abutilon rufiverne = (Callianthe rufinerva)

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Abutilon insigne

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Lorente et al. (2017)

Paper

Journal Pre-proof rufinerva) Saba (2007)

Dissertation

Abutilon sp.

Mill.

Colinvaux et Atlas al. (1999)

Abutilon sp.

Mill.

SalgadoLabouriau (1973)

Atlas

Allowissadula holosericea

(Scheele) D.M. Bates

Milla (2006)

Dissertation

Bastardiopsis densiflora

(Hook. & Arn.) Hassl.

Barth (1975) Atlas

Bastardiopsis densiflora

(Hook. & Arn.) Hassl.

Bastardiopsis sp.

(Hook. & Arn.) Hassl.

ro

of

Abutilon scabridum = (K. Schum.) (Callianthe scabrida) Donnell

Paper

re

-p

Christensen (1986)

Barth (1989) Atlas Christensen (1986)

Paper

Dombeya wallichii

Bush and Weng (2007)

Data base

(K. Schum.) Brizicky

Oliveira and Santos (2014)

Atlas

Herissantia crispa

(L.) Brizicky

Bush and Weng (2007)

Data base

Herissantia tiubae

(K. Schum.) Brizicky

Silva et al. (2016)

Atlas

Kearnemalvastrum lacteum

(Aiton) D.M. Bates

Christensen (1986)

Paper

Malvella sherardiana

Jaub.

Christensen (1986)

Paper

Monteiroa bullata

(Ekman) Krapov.

Christensen (1986)

Paper

Monteiroa bullata

Monteiroa bullata

Roth and Lorscheitter

paper

lP

Bogenhardia crispa = (L.) Brizicky (Herissantia crispa)

na

(Lindl.) Baill.

Jo

ur

Herissantia tiubae

Journal Pre-proof 2008 (K. Schum.) Krapov.

Milla (2006)

Dissertation

Sidastrum paniculatum

(L.) Fryxell

Oliveira and Santos (2014)

Atlas

Sphaeralcea ambigua A. Gray

Christensen (1986)

Paper

Sphaeralcea emoryi

Torr. ex A. Gray

Christensen (1986)

Paper

Sphaeralcea laxa

Wooton & Standl.

Christensen (1986)

ro

of

Pseudabutilon aristulosum

Cuadrado and Boilini (2006)

Paper

(Gillies ex Hook. & Arn.) Krapov.

Cuadrado and Boilini (2006)

Paper

(Griseb.) Krapov.

Cuadrado and Boilini (2006)

Paper

(Link) R.E. Fr.

Lorente et al. (2017)

Atlas

(Link) R.E. Fr.

Milla (2006)

Dissertation

Wissadula decora

S. Moore

Cuadrado and Boilini (2006)

Paper

Wissadula densiflora

R.E. Fr.

Christensen (1986)

Paper

Wissadula densiflora

R.E. Fr.

Cuadrado and Boilini (2006)

Paper

Wissadula excelsior

(Cav.) C. Presl

Milla (2006)

Dissertation

Wissadula

(A. St.-Hil.)

Cuadrado and Boilini

Paper

-p

Tarasa alberti = Reiche (Malvastrum albertii)

Paper

lP

na

Tarasa trisecta

re

Tarasa humilis

ur

Wissadula contracta

Jo

Wissadula contracta

Journal Pre-proof R.E. Fr.

(2006)

Wissadula glechomifolia

(A. St.-Hil.) R.E. Fr.

Milla (2006)

Dissertation

Wissadula gymnanthemum

(Griseb.) K. Schum.

Cuadrado and Boilini (2006)

Paper

Wissadula paraguariensis

Chodat

Cuadrado and Boilini (2006)

Paper

Wissadula parviflora

(A. St.-Hil.) R.E. Fr.

Cuadrado and Boilini (2006)

Paper

Wissadula periplocifolia

(L.) C. Presl ex Thwaites

Milla (2006)

Wissadula setifera

Krapov.

Wissadula subpeltata

Dissertation

Cuadrado and Boilini (2006)

Paper

(Kuntze) R.E. Fr.

Christensen (1986)

Paper

(Kuntze) R.E. Fr.

Cuadrado and Boilini (2006)

Paper

(Kuntze) R.E. Fr.

Milla (2006)

Dissertation

Wissadula tucumanensis

R.E. Fr.

Cuadrado and Boilini (2006)

Paper

Wissadula wissadifolia

(Griseb.) Krapov.

Cuadrado and Boilini (2006)

Paper

re

lP

na

Wissadula subpeltata

Jo

ur

Wissadula subpeltata

-p

ro

of

glechomifolia

Names between parentheses represent updated species names using Tropicos.org

Journal Pre-proof Table 3. Habitat and other environmental information available for extant Malveae genera found as affinity candidates to Malvacipolloides maristellae. Data from GBIF records (see Methods). Genera

Habitat/environment from collection records

Abutilon

swamp, secondary vegetation, Atlantic forest,

of

dry tropical forest, forest edge, rocky outcrops in montane ombrophilous forest and

ro

Atlantic forests, various path edges, riverside,

-p

rocky and dry soils, wet savannahs, caatinga,

re

dense forest on red-clay, various types of

lP

disturbed forests, open grassy areas, dry river bed, dry deciduous forest, terra firme forest;

disturbed forest, along roads, forest edge,

ur

Bakeridesia

dry tropical forests;

na

Allosidastrum

Jo

inside forest, Campos rupestres (rocky and

Bastardiopsis

grassy grounds); scrubland, forests and degraded forests, semideciduous forests, riverside, edge of campos (open fields);

Briquetia

rocky savannahs, disturbed forests, in xerophytic vegetation, rocky outcrops and secondary forests, roadside and forest edges,

Journal Pre-proof wet savannahs, forest clearings, caatinga, lakeside; Callianthe

open land, ruderal; disturbed, secondary and gallery forest; sandstone summit/sandy soils, dry forest, moist forest with disturbed/burned areas, roadsides, clearings, montane forest,

of

floodable field, open savannah on rocky

ro

grounds, cloud forest with open-dry areas,

-p

diverse forest edges, hill tops, semi-

re

deciduous forest, dry valleys, hygrophilous forest, shrubby vegetation on outcrop, dense

lP

ombrophilous forest; various localities in caatinga forests, coastal

na

Herissantia

scrubland, montane forest, various forest and

ur

road edges, sandy, clayey and thin soils,

Jo

rocky soils, savannahs, dry creek, lakeside, campos rupestres, flooded areas, seasonally dry forests, dry scrub vegetation, xerophytic slopes and gallery forests;

Pseudabutilon

rocky grounds, secondary forests, xerophytics forests, scrub, Chaco forest, unshaded areas, Chiquitano forest, dry coastal areas, rocky floodplain, montane

Journal Pre-proof deciduous forest, dry tropical forest; Sidastrum

montane forests, various forest and path edges, secondary forests, dry forests, Atlantic forests, caatinga, sandy soils, various degraded forests, wet savannahs and swamps, Chaco forest, rocky outcrops, low scrub

herbs along roads, trails and other manmade

-p

pathways;

ro

Sphaeralcea

of

forest;

dry or grassy hillside, limestone hill, river

re

Wissadula

terrace, sandy terrains periodically flooded,

lP

steep-dry slopes, edge of clearings, forest

na

margins, secondary forests, near or in caatinga forests, gallery forest, roadside,

ur

rocky field, dry forest, lakeside marshes, in

Jo

coastal rainforest along clearings, savannah/cerrado vegetation on rocky grounds, floodable areas (e.g. wet savannah), scrub forest, semi-deciduous evergreen forests, oxbow/ponds of rivers, all types of pastures and grazed lands, clayey but mostly sandy soils.

Journal Pre-proof Highlights    

Jo

ur

na

lP

re

-p

ro

of



A Neogene malvoid pollen is studied from northern South America We compared fossil and extant morphologies and reviewed fossil occurrences Fourteen extant taxa from the Abutilinae and Malvinae subtribes were found The fossil spread quickly in the early Miocene and declined from middle Miocene to present We propose ecologies for the fossil and relate it to environments of the Pebas system

Figure 1

Figure 2

Figure 3A

Figure 3B

Figure 4

Figure 5

Figure 6

Figure 7

Figure 8