Paleobiology, 2020, pp. 1–25
DOI: 10.1017/pab.2020.45
Article
Cretaceous–Paleogene plant extinction and recovery in Patagonia
Elena Stiles
, Peter Wilf, Ari Iglesias, María A. Gandolfo, and N. Rubén Cúneo
Abstract.—The Cretaceous–Paleogene (K/Pg) extinction appears to have been geographically heterogeneous for some organismal groups. Southern Hemisphere K/Pg palynological records have shown
lower extinction and faster recovery than in the Northern Hemisphere, but no comparable, well-constrained Southern Hemisphere macrofloras spanning this interval had been available. Here, macrofloral
turnover patterns are addressed for the first time in the Southern Hemisphere, using more than 3500
dicot leaves from the latest Cretaceous (Maastrichtian) and the earliest Paleocene (Danian) of Argentine
Patagonia. A maximum ca. 90% macrofloral extinction and ca. 45% drop in rarefied species richness is estimated across the K/Pg, consistent with substantial species-level extinction and previously observed extirpation of host-specialized leaf mines. However, prior palynological and taxonomic studies indicate low
turnover of higher taxa and persistence of general floral composition in the same sections. High species
extinction, decreased species richness, and homogeneous Danian macrofloras across time and facies
resemble patterns often observed in North America, but there are several notable differences. When compared with boundary-spanning macrofloras at similar absolute paleolatitudes (ca. 50°S or 50°N) from the
Williston Basin (WB) in the Dakotas, both Maastrichtian and Danian Patagonian species richnesses are
higher, extending a history of elevated South American diversity into the Maastrichtian. Despite high species turnover, our analyses also reveal continuity and expansion of leaf morphospace, including an
increase in lobed and toothed species unlike the Danian WB. Thus, both Patagonian and WB K/Pg macrofloras support a significant extinction event, but they may also reflect geographically heterogeneous
diversity, extinction, and recovery patterns warranting future study.
Elena Stiles. *Department of Geosciences, Pennsylvania State University, University Park, Pennsylvania 16802,
U.S.A. E-mail: estiles@uw.edu. *Present address: Department of Biology, University of Washington,
Seattle, Washington 98105, U.S.A.
Peter Wilf. Department of Geosciences, Pennsylvania State University, University Park, Pennsylvania 16802,
U.S.A. E-mail: pwilf@psu.edu
Ari Iglesias. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)–Universidad Nacional del
Comahue INIBIOMA, San Carlos de Bariloche 8400, Río Negro, Argentina. E-mail: ari_iglesias@yahoo.com.ar
María Alejandra Gandolfo. L.H. Bailey Hortorium, Plant Biology Section, School of Integrative Plant Science,
Cornell University, Ithaca, New York 14853, U.S.A. E-mail: mag4@cornell.edu
N. Rubén Cúneo. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)–Museo Paleontológico
Egidio Feruglio, Avenida Fontana 140, Trelew 9100, Chubut, Argentina. E-mail: rcuneo@mef.org.ar
Accepted: 27 August 2020
Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.jsxksn071
Introduction
The devastating environmental consequences of the end-Cretaceous bolide impact
affected both marine and terrestrial organisms
(e.g., Alvarez et al. 1980; Prinn and Fegley
1987; Robertson et al. 2013; Vellekoop et al.
2014; Tyrrell et al. 2015; Artemieva and Morgan
2017; Brugger et al. 2017). Over 60% of Cretaceous species became extinct, making the
Cretaceous–Paleogene (K/Pg) event the most
recent of the “big five” mass extinctions (Raup
and Sepkoski 1982; Jablonski 2005; Schulte
et al. 2010). Although the K/Pg event affected
biotas globally, the severity of the extinction
and the pacing of the recovery were geographically heterogeneous for some groups of organisms (see next paragraph). Modern biodiversity
is shaped by the surviving lineages of the K/Pg
(e.g., Erwin 2002; Krug et al. 2017), establishing
today’s biogeographic patterns, in part, as the
legacy of a globally heterogeneous extinction
(e.g., Wolfe 1987).
Southern Hemisphere records of calcareous
nannoplankton, insect herbivory, and terrestrial palynomorphs indicate lower extinction
and/or faster recoveries than Northern
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2
ELENA STILES ET AL.
Hemisphere counterparts (Vajda et al. 2001;
Vajda and Raine 2003; Iglesias et al. 2007; Pole
and Vajda 2009; Jiang et al. 2010; Barreda
et al. 2012; Cantrill and Poole 2012; Schueth
et al. 2015; Donovan et al. 2016). Furthermore,
several plant and vertebrate groups that had
been known only from Mesozoic localities in
the Northern Hemisphere, have been reported
in Cenozoic Southern Hemisphere deposits
suggesting that they survived the K/Pg in
southern latitudes (Case and Woodburne
1986; Pascual et al. 1992; Bonaparte et al.
1993; Goin et al. 2006, 2012; McLoughlin et al.
2008, 2011; Gelfo et al. 2009; Sterli and de la
Fuente 2019). Proposed explanations for this
geographic heterogeneity (Jiang et al. 2010;
Donovan et al. 2016, 2018) have referenced
increased distance from the Mexican impact
site (Schulte et al. 2010), oceanic buffering of
impact winter temperatures in the Southern
Hemisphere (Bardeen et al. 2017; Tabor et al.
2020), and a bolide impact angle that would
have directed most ejecta and debris northward
(Schultz and D’Hondt 1996).
Because plants are the primary producers in
terrestrial ecosystems and one of the most biodiverse groups of organisms, the paleobotanical record is critical for understanding
extinction events on land (e.g., Nichols and
Johnson 2008). However, the vast majority of
plant-bearing K/Pg continental sites is concentrated in the western interior of North America
(NAM), which bears numerous examples of
stratigraphically and temporally well constrained boundary-spanning palynofloras
(e.g., Nichols et al. 1986; Nichols and Fleming
1990; Sweet et al. 1990, 1999; Sweet and Braman
2001; Nichols 2002; Bercovici et al. 2009) and
macrofloras (e.g., Wolfe and Upchurch 1986;
Johnson et al. 1989; Johnson and Hickey 1990;
Johnson 1992, 2002; Upchurch 1995; Barclay
et al. 2003; Nichols and Johnson 2008). Southern Hemisphere K/Pg-spanning paleofloras
are scarce and have been primarily limited to
palynological records (e.g., Vajda-Santivanez
1999; Vajda et al. 2001; Vajda and Raine 2003;
Pole and Vajda 2009; Barreda et al. 2012; Cantrill and Poole 2012; Scasso et al. 2020). Cretaceous–Paleogene macrofloras from New
Zealand revealed a dramatic floral turnover
(Pole and Vajda 2009) and a paleoclimatic
cooling trend consistent with global records
(Kennedy et al. 2002) across the K/Pg, but the
severity of the macrofloral extinction was not
estimated. Until now, no well-constrained and
well-sampled macrofloral Maastrichtian and
Danian sites from the same region have been
available in the Southern Hemisphere.
Recent studies of the latest Cretaceous (Maastrichtian) Lefipán and early Paleocene (Danian)
Salamanca and Peñas Coloradas Formations of
Chubut, Argentine Patagonia (Fig. 1; and see
“Materials” and “Analytical Methods”) showed
lower palynological extinction, faster recovery
of insect herbivory damage-type diversity, and
remarkably diverse Danian macrofloras compared with most NAM sections of the same
ages. Specifically, spore and pollen records
showed <10% extinction across the K/Pg compared with the 30%–40% extinction in NAM
palynofloras (Nichols and Fleming 1990;
Sweet and Braman 2001; Hotton 2002; Nichols
2002; Barreda et al. 2012). Notably, in early
Danian Patagonian pollen records, an abundance spike of the conifer Classopollis represents
the last record of a genus that is otherwise only
known until the Late Cretaceous worldwide
(Barreda et al. 2012). Insect feeding-damage
types on angiosperm leaves recovered to
pre-K/Pg diversity levels within about 4 Myr,
compared with the estimated ca. 9 Myr for
NAM (Donovan et al. 2016, 2018), and Danian
macrofloras of the Salamanca Formation are
much more diverse than most coeval NAM
counterparts, suggesting a faster-paced Patagonian recovery (Iglesias et al. 2007). However,
comparable Maastrichtian leaf floras from the
same Patagonian region have not yet been evaluated using similar methods.
Gymnosperm macrofossils of the Lefipán
and Salamanca Formations have been the subject of taxonomic studies (Zamuner et al.
2000; Brea et al. 2005; Quiroga et al. 2015;
Ruiz et al. 2017; Wilf et al. 2017; AndruchowColombo et al. 2018, 2019; Escapa et al. 2018),
indicating the survival of the Podocarpaceae
and Araucariaceae conifer families. The presence of several derived angiosperm groups
known from reproductive material in the Salamanca Formation suggests that they also
represent K/Pg survivor families (Iglesias
et al. 2007; Raigemborn et al. 2009; Jud et al.
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PATAGONIAN K/PG PLANT EXTINCTION
2017, 2018a,b; Supplementary Tables 1, 2).
Angiosperm leaf fossils have sourced the aforementioned work on K/Pg insect damage
(Donovan et al. 2016, 2018), yet the extensive
leaf collections on which the insect herbivory
was documented have not been rigorously
compared to quantify macrofloral species
extinction in Patagonia across the Cretaceous/
Paleogene transition.
Fossil dicot leaves from the Maastrichtian
and Danian of Patagonia (Fig. 1) together
offer insight into macrofloral K/Pg diversity,
and potential extinction and recovery patterns
with well-sampled, stratigraphically and temporally constrained collections for the first
time in the Southern Hemisphere (Iglesias
et al. 2007; Scasso et al. 2012; Clyde et al.
2014; Donovan et al. 2016, 2018). Through the
analysis of more than 3500 leaf fossils from
four localities, this study addresses terminal
Cretaceous and early Paleocene macrofloral
diversity in Patagonia, and the possible effects
of the K/Pg extinction event on the floras of
the region while considering the potential climatic, sampling, and ecological biases impacting the observations. Although the main goal
of this contribution is to document the first temporally constrained K/Pg-spanning macrofloral assemblages occurring within the same
region in the Southern Hemisphere, we compare our results with the well-sampled,
boundary-spanning K/Pg NAM macrofloras
from similar absolute paleolatitudes (ca. 50°N
or 50°S) in the Williston Basin (WB) in North
Dakota (Johnson 2002; Wilf and Johnson 2004)
to further explore potential biases in our observations and to examine potential geographic
heterogeneity in macrofloral patterns among
two widely separated regions.
Materials
The collections studied here are primarily the
same as those from Chubut, Argentina, used in
earlier work on Danian floral diversity (e.g.,
Iglesias 2007; Iglesias et al. 2007) and K/Pg
insect damage (Donovan et al. 2016, 2018),
plus some additional material previously not
cataloged (Supplementary Table 3). Iglesias
et al. (2007) documented Danian dicot-leaf
diversity by morphotyping and assigning
3
systematic affinities when possible (Iglesias
2007; Iglesias et al. 2007; more recent updates
shown in Supplementary Table 1). Donovan
et al. (2016, 2018) analyzed the insect feedingdamage diversity on the leaves from Maastrichtian and Danian collections and proposed a
preliminary morphotype classification for the
Maastrichtian leaves. The leaf collections from
the Lefipán (Maastrichtian) and Salamanca
and Peñas Coloradas (Danian) Formations
were compiled over a series of field trips
involving the four junior authors and others
since 2003, and they are curated in the Paleobotanical Collection of the Museo Paleontológico Egidio Feruglio (MEF; repository
acronym MPEF-Pb), Trelew, Argentina (Supplementary Table 3). All collections studied
are unbiased, complete census collections of
all identifiable material found, taken to the
lab at MEF, and vetted and tallied. Although
they are separated by ca. 400 km (Fig. 1), and
the K/Pg boundary horizon itself is not preserved in the Lefipán or Salamanca Formations,
these Maastrichtian and Danian collections
represent broadly similar, marginal marine
depositional settings and the only large, stratigraphically constrained leaf collections from
their time periods sourced from a single region
in the Southern Hemisphere. In addition to the
summary presentation and citations that follow, further detailed accounts of collecting
methods and sites and full descriptions of the
leaf morphotypes are in separate preparation.
Lefipán Formation.—The siliciclastic Lefipán
Formation conformably overlies the Campanian–Maastrichtian fluvio-estuarine Paso del
Sapo Formation, and it is unconformably overlain by the Eocene Barda Colorada Ignimbrite
(Spalletti 1996; Aragón and Mazzoni 1997;
Scasso et al. 2012; Aragón et al. 2018) and
other Paleogene volcanic units (Aragón et al.
2018). Deposited in the shallow, paleo-Atlantic
Paso del Sapo embayment (Fig. 1A,B), the
Lefipán Formation records the latest Cretaceous (?Campanian–Maastrichtian) to early
Paleocene (Danian) infilling of the Jurassic–
early Paleocene Cañadón Asfalto Basin
(Fig. 1A) (Spalletti 1996; Scasso et al. 2012;
Figari et al. 2015). Leaf cuticular pCO2 estimates
(Martínez et al. 2018), TEX86 proxy records
(Scasso et al. 2012; Vellekoop et al. 2017), and
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ELENA STILES ET AL.
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PATAGONIAN K/PG PLANT EXTINCTION
paleobotanical evidence (Baldoni 1992; Baldoni
et al. 1993; Barreda et al. 2012; Wilf et al. 2017)
indicate that the upper Maastrichtian Lefipán
Formation was deposited in mesothermal (or
warmer), frost-free climates (Fig. 1A) along a
coastline fringed by patchy woodlands and
mangroves; macrofossil evidence suggests
areas of rain forest as well (Wilf et al. 2017;
Escapa et al. 2018).
The San Ramón Section (SRS; Fig. 1B,D)
studied here is the most complete of the Lefipán
Formation (Scasso et al. 2012), comprising marginal, tidal-flat deposits to fully marine sediments within a tidally dominated deltaic
setting that ranges from ?Campanian–
Maastrichtian to Danian in age (Legarreta and
Uliana 1994; Spalletti 1996; Barreda et al.
2012; Scasso et al. 2012; Vellekoop et al. 2017;
Butler et al. 2019). The K/Pg impact layer
recognized at other sites around the world
(e.g., Alvarez et al. 1980, 1990; Orth et al.
1981; Brooks et al. 1986; Lerbekmo and
St. Louis 1986; Schulte et al. 2010) is not preserved in the SRS, probably due to bioturbation
or erosion at that particular level (Scasso et al.
2012). However, the K/Pg in the Lefipán Formation is constrained to about 4 m of section
based on biostratigraphic data, including the
marker Turritella malaspina lag bed as the first
Danian deposit (Fig. 1D) (Medina and Camacho 1990; Scasso et al. 2012), dinoflagellate
index taxa (Barreda et al. 2012; Vellekoop
et al. 2017), age-diagnostic continental palynomorphs (Barreda et al. 2012), and a sudden
and significant turnover of invertebrate faunas
(Aberhan and Kiessling 2014) and microfloras
5
with the extinction of ca. 10% of total and
50% of angiosperm palynotaxa (Fig. 1D) (Barreda et al. 2012).
Lefipán Formation specimens analyzed here
were collected in the SRS (Fig. 1A,C,D) in sandstone–mudstone tidal-flat deposits (Scasso
et al. 2012). Localities LefW, LefE, and LefL,
as detailed in Donovan et al. (2016, 2018) and
Wilf et al. (2017), yielded a total of 1062
dicot-leaf specimens from unbiased collections
biostratigraphically constrained to the 67–66
Ma range and most likely in the 66.5–66.0
range based on dinoflagellate markers
(Fig. 1D) (Barreda et al. 2012; Scasso et al.
2012; Vellekoop et al. 2017). All identifiable
material was collected at these sites and taken
back to the MEF, where it was vetted and censused (no identifiable fossils were discarded
in the field). The LefW macrofloral site corresponds to the same plant-bearing beds discussed in Scasso et al. (2012) and Vellekoop
et al. (2017). The LefW collection (Supplementary Table 3) includes 278 dicot-leaf specimens
spanning about 20 m of stratigraphic section
from four collecting horizons, the youngest of
which is located 5 m below the Danian Turritella marker bed (Scasso et al. 2012; Donovan
et al. 2016; Vellekoop et al. 2017). Approximately 1000 m map distance east of LefW is
the single fossiliferous horizon yielding the
macrofloras of the LefE and LefL collections.
Locality LefE, 21.5 m below the Turritella
marker bed, is closest to LefW. The LefE quarry
extends about 40 m along the horizon (Wilf
et al. 2017), from where 614 dicot-leaf fossils
were collected. LefL is located approximately
FIGURE 1. Setting of paleobotanical localities. A, Paleogeographic reconstruction of Patagonia at K/Pg time, redrawn from
Scasso et al. (2012). Light blue diagonal pattern: shallow platform; yellow horizontal pattern: coastal lowlands; dashed line:
approximate boundary between paleoclimatic belts as inferred by Scasso et al. (2012). Locations of panels B and C marked.
B, Location of Scasso et al.’s (2012) San Ramón section (within star) of the Lefipán Fm., containing Maastrichtian macrofloras and Maastrichtian and Danian palynofloras. Modified after Barreda et al. (2012). C, Locations of Danian paleobotanical sites: Palacio de los Loros (PL), Salamanca Fm.; Las Flores (LF), Peñas Coloradas Fm.; and Bosque Petrificado José
Ormachea (OR, Salamanca Fm., used here for pollen data only). Modified after Clyde et al. (2014) and Comer et al.
(2015). D, Summary stratigraphy showing chronostratigraphic and absolute age constraints, placement of palynological
(tick marks) and macrofloral sampling sites (black stars; compiled from Iglesias 2007; Barreda et al. 2012; Clyde et al.
2014; Comer et al. 2015; Donovan et al. 2016, 2018). Summary of absolute ages of the fossil sites (see text for details): Lefipán
floras, 67–66 Ma, most likely 66.5–66.0 Ma; PL1 flora, 66.4–65.7 Ma (C29n); PL2 flora, 64.7–63.5 Ma (C28n); LF flora, 62.5–
62.2 Ma (C27n). Range of stratigraphic section comprising approximate locations of LefW sampling horizons (as described
in Vellekoop et al. 2017) indicated by dashed line (see “Materials” for details). LefE, LefL, and LefW are shown on a single
column for simplicity but represent different locations (see text for details). LefE and LefL come from a single laterally
extensive horizon that varies in stratigraphic distance below the Turritella bed. The position shown is for LefL. BBF, Bajo
Barreal Fm. (Color online.)
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6
ELENA STILES ET AL.
500 m (map distance) east of LefE, in the same
bed, at 24 m locally below the Turritella bed
(Donovan et al. 2016) and yielded 170 dicot-leaf
specimens. The single fossiliferous horizon
containing LefE and LefL cannot be correlated
precisely to those in LefW due to cover and erosion in the intervening landscape, but their ages
are probably very similar based on stratigraphic position.
Salamanca and Peñas Coloradas Formations.—
The Danian Salamanca and Peñas Coloradas
Formations are the oldest Cenozoic sedimentary units in the north-central San Jorge Basin
(Fig. 1A) (Sylwan 2001; Clyde et al. 2014;
Comer et al. 2015). In our study area (Fig. 1A,
C), tidally influenced, marginal to estuarine
deposits of the early Danian Salamanca Formation (Legarreta and Uliana 1994; Iglesias 2007;
Comer et al. 2015) unconformably overlie fluvial and pyroclastic deposits of the Late Cretaceous (Campanian) Bajo Barreal Formation
or (where preserved) the Maastrichtian La
Angostura Basalt (Fig. 1D) (Iglesias 2007;
Clyde et al. 2014; Comer et al. 2015), and they
are unconformably overlain by the fluviovolcanic deposits of the late Danian Peñas Coloradas Formation of the continental Rio Chico
Group (Fig. 1C,D) (Iglesias 2007; Raigenborn
et al. 2010; Clyde et al. 2014; Comer et al.
2015; Krause et al. 2017). At the Las Flores
(LF; Fig 1C) Peñas Coloradas Formation locality, deposits overlie the Maastrichtian Colhué
Huapi Formation and La Angostura Basalt
(Casal et al. 2015; Comer et al. 2015).
Fossil occurrences from the Salamanca and
overlying Peñas Coloradas Formations are consistent with humid, mesothermal, frost-free climates (Bonaparte et al. 1993; Brea et al. 2005;
Iglesias et al. 2007; Palazzesi and Barreda
2007; Raigemborn et al. 2009; Futey et al.
2012; Clyde et al. 2014; Ruiz et al. 2017, 2020).
Palynofloras of the Salamanca Formation and
related strata over larger areas reflect a range
of environments, from mangrove swamps to
lowland and upland forests (Petriella and Archangelsky 1975; Zamaloa and Andreis 1995; Volkheimer et al. 2007). In the study area (Fig. 1C,
D), local pollen records show diverse,
angiosperm-dominated lowland forests (Petriella and Archangelsky 1975; Clyde et al.
2014).
The unbiased, lab-vetted (the same collecting
and tallying methods used as for the Lefipán
floras) early Paleocene leaf collections analyzed
in this study came from two early Danian Salamanca Formation localities in the Palacio de los
Loros sampling area (PL1 and PL2) and one late
Danian locality in the Peñas Coloradas Formation, the LF plant-fossil site (Fig. 1B) (Iglesias
2007; Iglesias et al. 2007; Clyde et al. 2014). Biostratigraphic data from foraminifera, dinoflagellates, and calcareous nannoplankton
indicate the early Danian age for the local Salamanca Formation, with a maximum absolute
age of 67.31 ± 0.55 Ma from 40Ar/39Ar dating
of the La Angostura Basalt flow underlying
the formation in the easternmost exposures of
the study area (Fig. 1D) (Clyde et al. 2014).
The U-Pb age of a tuff layer in the Peñas Coloradas Formation at Palacio de los Loros is 61.984
± 0.041 Ma, placing it in the late Danian
(Fig. 1D) (Clyde et al. 2014). Combined analysis
of paleomagnetic stratigraphy, biostratigraphy,
and U-Pb and 40Ar-39Ar ages place the paleobotanical sites PL1, PL2, and LF within geomagnetic polarity chrons C29n (65.58–64.88
Ma), C28n (64.67–63.49 Ma), and C27n (62.52–
62.22 Ma), respectively (Fig. 1D) (Clyde et al.
2014; Comer et al. 2015), using the 2012 Geologic Time Scale (Gradstein et al. 2012).
Between the early Danian Salamanca and
late Danian Peñas Coloradas Formations,
there is a sharp change in the depositional
environment. The strata at PL1 and PL2 were
deposited in marginal estuarine settings,
whereas LF was deposited in a nearly fully terrestrial fluvio-volcanic environment (Comer
et al. 2015). Locality PL1 (Fig. 1A,C,D) produced 1089 dicot-leaf specimens, preserved in
sand–siltstone sediments interpreted as lateral
accretion beds of abandoned tidal channel fill
(facies Sab in Comer et al. 2015). The younger
locality PL2 yielded 1132 dicot-leaf specimens,
collected from silty claystones interpreted as
the transitional facies of tidal flats prograding
over a coastal plain (facies SCt in Comer et al.
2015). Sediments in locality LF are the coarsestgrained of the Danian macrofloral sites, from
where 564 dicot-leaf specimens were recovered
from poorly sorted litharenites interpreted as
channel fills (facies LF1 in Comer et al. 2015).
Based on sedimentology and preservational
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PATAGONIAN K/PG PLANT EXTINCTION
quality, the potential order of transport distances for fossil leaves is ranked highest to lowest as LF, PL1, and PL2. Donovan et al. (2018)
noted that preservation quality in Salamanca
Formation locality PL1 is similar to that of the
Lefipán Formation, indicating minimal preservation bias between the oldest Paleogene locality and the Maastrichtian collections in this
study.
Analytical Methods
Macrofloral turnover across the K/Pg transition was addressed through analyses of (1)
change in species composition, (2) morphospace shifts among assemblages, and (3) the
potential biasing effect of the ca. 400 km separation between the Cretaceous and Paleogene
collection sites using crosschecks from local
pollen records in both formations (Fig. 1D). Preliminary Lefipán Formation morphotypes
(Donovan et al. 2016) were significantly revised
and updated based on leaf architectural characters (Ellis et al. 2009). Danian morphotypes of
the Salamanca and Peñas Coloradas Formations are based on the morphotype set of the
PL1, PL2, and LF macrofloral localities (Iglesias
2007; Iglesias et al. 2007) and an additional set
published in the supplementary information
of Donovan et al. (2016; Supplementary
Table 4). A total of 58 Maastrichtian and 43
Danian morphotypes were established and
used in the subsequent analyses (Supplementary Table 4). Each morphotype is here interpreted as likely to have been produced by a
single species with morphologically distinct
leaves and will be referred to as a species
throughout this study. An updated specimenlevel collections inventory of all leaf morphotypes as used here is archived in Supplementary Table 3.
Extinction and Turnover.—All Maastrichtian
and Danian collections were grouped into
two respective assemblages for macrofloral
extinction estimates and morphospace analyses
due to their self-similar floral compositions and
morphospace occupation, based on preliminary analyses. Each of the Maastrichtian morphotypes was compared with the Danian
morphotypes in search of K/Pg survivor pairs
based on a detailed comparison of their leaf
7
architecture (per Johnson et al. 1989; Ash
et al. 1999; Ellis et al. 2009). Maastrichtian and
Danian morphotypes that shared all morphological characters or that fell within each
other’s ranges of variation were considered
survivor pairs.
Once the survivor pairs were established,
they were each considered as a single species,
along with all the other leaf species, in a principal components analysis (PCA) applied to a
matrix of species abundances per sample,
with the objective of testing compositional heterogeneity among the considered Maastrichtian and Danian macrofloral collections. In
this analysis, Maastrichtian collections LefW
and LefE+LefL were considered as two samples, because LefW was collected along several
horizons within the same small canyon (see
“Materials”), and LefE and LefL were collected
along the same fossiliferous horizon.
For rarefied (Tipper 1979) species richness
analysis across the K/Pg, the Maastrichtian
LefE and LefL sites were grouped into a single
sample, from which LefW was excluded
because it includes specimens from multiple
horizons with uncertain stratigraphic relationships to horizon LefE+LefL. The Salamanca
(PL1 and PL2) and Peñas Coloradas (LF) localities (Fig. 1A,C,D) (Iglesias 2007; Iglesias et al.
2007) were considered for rarefaction individually because they span three Danian time intervals (Fig. 1D) (see “Materials”; Clyde et al. 2014;
Comer et al. 2015). Each rarefaction curve was
plotted with a 95% confidence interval using
the R package iNext (Hsieh et al. 2016).
As a baseline for comparison of rarefied species richness between Patagonian and North
American K/Pg assemblages, three representative dicot-leaf samples surpassing 350 specimens each (per Burnham 1993) from
meter-binned collections of the Maastrichtian
Hell Creek and Danian Fort Union Formations
in the WB of southwestern North Dakota were
selected from the dataset of Wilf and Johnson
(2004; see also Johnson 2002). The Dean
Street level found 15 m below the K/Pg boundary (Wilf and Johnson 2004) represents the
most diverse, latest Maastrichtian HCIII zone
(Johnson 2002). Two representative Fort
Union Formation collection horizons were
based on specimen counts >350 and
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8
ELENA STILES ET AL.
magnetostratigraphic constraints. Horizon +7
m is the most specimen-rich representative of
early Danian Fort Union Formation fossil horizons, corresponding to geomagnetic polarity
chron C29r (which is unrecorded in Patagonia).
The +38 m horizon is constrained to chron C29n
(Hicks et al. 2002; Johnson 2002), serving as a
temporal analog to the PL1 locality in Patagonia (Fig. 1D) (Clyde et al. 2014). While acknowledging work on diverse Paleocene floras from
the more southerly Denver and San Juan basins
(Johnson and Ellis 2002; Flynn and Peppe 2019;
Lyson et al. 2019), we focus on the floras of the
WB for comparison, because they come from
similar absolute paleolatitudes to our samples
(i.e., ca. 51.3°S for the Danian Patagonian floras,
ca. 48.4°S for the Cretaceous Lefipán floras, and
ca. 49.4°N for the WB floras, versus ca. 42.5°N
for the Denver Basin, following Iglesias et al.
2007: fig. 3), contain both Cretaceous and Paleocene floras that are well sampled in a single
area, and remain the best-sampled and
described boundary-spanning K/Pg macrofloras of NAM.
Morphospace Analysis.—Species richness and
morphological diversity are not always
coupled, and this disconnection may be driven
by underlying selective pressures (Foote 1993;
Roy and Foote 1997). Morphospace analysis is
here used as a quantitative tool to measure
morphological diversity and phenotypic relationships among angiosperm leaf species and
their change through time, by summarizing
morphological characters in a mathematical
space where phenotypic dissimilarities are
observed as graphical distances (Mitteroecker
and Huttegger 2009). Leaf architecture is
related both to systematic affinities and environmental parameters (e.g., Wolfe 1995; Wilf
1997; Little et al. 2010; Givnish and Kriebel
2017), making leaves ideal candidates to simultaneously test species and morphological turnover across the K/Pg. Through morphospace
analysis, the multivariate relationships among
characters can shed light on selective morphological extinction patterns, if present, and the
relationships between morphological disparity
and species richness.
Based on the Manual of Leaf Architecture (Ellis
et al. 2009), forty-six discrete shape, size, margin, and venation characters (Supplementary
Table 5) were scored for each of the Maastrichtian and Danian morphotypes (Supplementary
Table 7). Features that were not preserved (or
observable) in at least three-fourths of the specimens, such as fourth- and higher-order venation, were excluded to reduce noise in the
dataset. After observation of all available
material, character states for each morphotype
were usually based on one or two (if a single
specimen did not preserve all morphological
characters) selected exemplar specimens. If a
morphotype showed significant variation in
one or more characters after observation of all
available samples, end members were separated in the morphological matrix designated
by letters following the morphotype name
(e.g., SA9A, SA9B; Supplementary Table 7) to
ensure that all morphological diversity was
captured in the subsequent ordination. Maximum size was based on the largest specimen
of each species in the collection. Missing characters were coded as “NA.”
The morphological matrix (Supplementary
Table 7) was ordinated using principal coordinates analysis (PCoA) with the R Package ape
(Paradis and Schliep 2018). Because it compares
each morphotype on a character-by-character
basis, PCoA is considered the best-performing
method for datasets with uneven preservation
and missing characters (Foote 1994; Roy and
Foote 1997). The percentages of missing data
for each character and each morphotype are
reported in Supplementary Table 8. To understand how species are distributed in space
and to explore possible character-related patterns, the same scores obtained in the PCoA
ordination were analyzed by graphically superimposing character states on plotted scores
including axes PCoA 1–PCoA 3. The process
was repeated for each character.
To obtain a quantitative measure of morphospace occupation for Maastrichtian and Danian
assemblages and to verify consistency in the
results, four disparity measures were calculated separately for each Maastrichtian (LefW,
LefE, and LefL) and Danian (PL1, PL2, and
LF) leaf assemblage and for grouped Maastrichtian (LefW+LefE+LefL) and Danian (PL1
+PL2+LF) assemblages. Based on the first
four axes of the PCoA, (1) a hypercuboid volume and (2) a sum of ranges were estimated
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PATAGONIAN K/PG PLANT EXTINCTION
(Foote 1994; Wills et al. 1994). Based on the
Euclidean pairwise distance matrices, the (3)
average pairwise distance and (4) maximum
pairwise distance were extracted. The hypercuboid volume was estimated by multiplying the
ranges of the first four axes (Wills et al. 1994).
Following Gerber’s (2019) proposed measures
of disparity for discrete character spaces, the
(3) average and (4) maximum pairwise distances of the Euclidean distance matrix are
reported here (Supplementary Table 6) for
each local assemblage and the grouped Maastrichtian and Danian assemblages.
Pollen Analysis and Regional Floral Heterogeneity.—Palynological records from the same formations and sections offer the closest possible
points of comparison to macrofloras, and they
provide, for the most part with taxonomic resolution above the species level, information
about changes in regional floral composition
(Behrensmeyer et al. 2000; Nichols and Johnson
2008). To evaluate the effects of the approximately 400 km distance separating the Maastrichtian and Danian localities (Fig. 1A) as a
spatial bias affecting macrofloral composition,
published palynological records for the same
two sampling areas and stratigraphic framework (Fig. 1D) (Barreda et al. 2012; Clyde
et al. 2014) were compared at taxon-by-taxon
and whole-assemblage levels. The Lefipán
Formation palynological records from the
SRS span the boundary (Fig. 1D) (unlike the
Lefipán macrofloras; Barreda et al. 2012);
thus, both their Maastrichtian and Danian
components were compared with the exclusively Danian records of the Salamanca Formation at Palacio de los Loros and adjacent
areas sampled at high stratigraphic resolution
(Clyde et al. 2014). We note that several other
palynological studies exist of both formations
based on other sections (e.g., Archangelsky
1973; Petriella and Archangelsky 1975;
Medina and Camacho 1990; Baldoni et al.
1993; Casal et al. 2015), but our goal is to compare palynological data from the same wellconstrained sections as the macrofloras
addressed here. The fine temporal correlations
between the Lefipán and Salamanca Formations are not yet established.
V. Barreda (Museo Argentino de Ciencias
Naturales, Buenos Aires) kindly reviewed the
9
illustrations and species lists in Clyde et al.
(2014) to establish equivalencies between palynotaxa (e.g., “Proteaceae sp. A” and “Proteaceae sp. B”) among the Lefipán and
Salamanca sections, and her vetted species
data were used in subsequent analyses (Supplementary Table 2). Sample-level compositional
comparisons were based on a presence–
absence matrix of palynomorph species and
morphotypes (Supplementary Table 2) and
processed in the R vegan package (Oksanen
et al. 2017).
The presence–absence matrix of palynomorph data was transformed using the Beals
smoothing method (McCune 1994; Münzbergová and Herben 2004), which accounts for
unevenness in ecological sampling by replacing
species’ presence data with a probability of
occurrence based on co-occurrences in the
sample pool. This method was used to reduce
the underlying compositional heterogeneity
caused by the inherent sampling bias of the fossil record. The samples were then clustered
based on their Bray-Curtis pairwise dissimilarity matrix calculated from the Beals-smoothed
dataset and linked using Ward’s method algorithm (Oksanen et al. 2017).
Results
Extinction and Turnover.—We recognize only
five Maastrichtian leaf species as having a corresponding survivor in any Danian assemblage
(Figs. 2, 3), indicating a raw dicot macrofloral
extinction of 92.2%. Using only the oldest
Danian assemblage (PL1 locality) yields a
93.3% extinction. Excluding species represented by a single specimen (singletons)
reduces the extinction slightly, to 90.6%. The
K/Pg survivor pairs based on Maastrichtian
(prefix LEF) and Danian (prefix SA) morphotypes (Supplementary Tables 1,2) are referred
to as Survivor Pair (SP) 1 (LEF57-SA20;
Fig. 2A–E), SP2 (LEF64-SA35; Fig. 2F–I), SP3
(LEF6-SA19; Fig. 3A–C), SP4 (LEF18-SA08;
Fig. 3D–G), and SP5 (LEF55-SA78; Fig. 3H–J).
We interpret SP1 (Fig. 2A–E) to have a botanical affinity with the family Cunoniaceae based
on its architectural characters including compound leaves (Fig. 2), supported by the welldocumented presence (and earliest global
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ELENA STILES ET AL.
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PATAGONIAN K/PG PLANT EXTINCTION
macrofossil occurrence) of this family from
abundant co-occurring Lacinipetalum spectabilis
flowers with in situ pollen (schizomerioid
Cunoniaceae; Jud et al. 2018) from PL2 and
other Salamanca Formation localities and fossil
wood in the Peñas Coloradas Formation (Raigemborn et al. 2009). The affinities of SP2
(Fig. 2F–I) and SP5 (Fig. 3H–J) remain
unknown. Following Iglesias et al. (2007), SP3
(Fig. 3A–C) is equivalent to some specimens
designated as “Sterculia” acuminataloba Berry
1937 of the family Malvaceae, and SP4
(Fig. 3D–G) belongs to the family Rosaceae
based on diagnostic characters including serrated margins with compound teeth and craspedodromous secondary venation. The
survivorship of the family Rosaceae is a new
contribution of this study, along with Cretaceous macrofloral evidence to support the
K/Pg survival of Malvaceae and Cunoniaceae,
previously known from pollen records in these
sections (Barreda et al. 2012; Jud et al. 2018a,b).
Laurophyll morphotypes observed in this
study provide evidence for the K/Pg survival
of the Lauraceae in Patagonia, although we
cannot assign any Maastrichtian laurophyll to
a definite Danian species-level equivalent
because they lack cuticular preservation for further analysis (e.g., Carpenter et al. 2018). Based
on a conservative “lumping” approach, we
established four Maastrichtian laurophyll morphotypes based on their having typical lauraceous leaf architectural features (after Hickey
and Wolfe 1975). Lefipán Formation morphotypes LEF08, LEF24, LEF26, and LEF32 (Supplementary Table 3), coupled with Danian
Laurophyllum piatnitzkyi Berry and Laurophyllum chubutensis Berry of the Salamanca and
Peñas Coloradas Formations (Iglesias et al.
2007), add Lauraceae to the list of Patagonian
K/Pg macrofloral survivor families. Laurophyllum piatnitzkyi is notable as the most abundant
11
species in the Danian assemblages, accounting
for ca. 17% of total leaf specimens (Iglesias et al.
2007).
The loss of common taxa followed by the
emergence of previously rare taxa is a commonly observed pattern across mass extinction
intervals (e.g., Erwin 2002; Johnson 2002;
Jablonski 2005). A comparable pattern occurs
in our survivor pairs (Fig. 4). SP1 of the Cunoniaceae (Fig. 2A–E) is a major component of
Maastrichtian floras, but its abundance is
greatly reduced at earliest Danian PL1 before
partially recovering in PL2 (Fig. 4). In contrast,
Malvaceae SP3 (Fig. 3A–C) and Rosaceae SP4
(Fig. 3D–G), both minor components in Maastrichtian assemblages, surpass 5% of assemblage composition at early Danian PL1 and
are reduced back to minor components at PL2
and LF (Fig. 4). Leaf morphotypes SP2 and
SP5, of unknown affinities, remain minor components throughout.
Rarefied dicot-leaf richness dropped in Patagonia by almost 40% across the K/Pg and
remained comparably low from the early to
late Danian (Fig. 5). Patagonian Danian floras
are remarkably homogeneous across time and
facies, from early to late Danian and from marginal marine to pyroclastic–fluvial environments, in comparison with the relatively more
heterogeneous Lefipán floras deposited in similar facies and spanning a narrower time interval (Fig. 6). A sharp drop in rarefied species
richness was also observed in the North American K/Pg floras of the WB in North Dakota
(e.g., Johnson 2002; Wilf and Johnson 2004).
However, our rarefaction also shows that Patagonian floras are significantly more diverse
than the North Dakota floras not only during
the early Danian (Iglesias et al. 2007) but also
the Maastrichtian (Fig. 5).
Morphospace Analysis.—Pre- and post-K/Pg
leaf assemblages significantly overlap in
FIGURE 2. K/Pg survivor pairs (SPs) from the Maastrichtian Lefipán (blue circles) and Danian (unmarked) Salamanca and
Peñas Coloradas Formations (see also Fig. 3). A–E, SP1, Cunoniaceae, including articulated compound leaf. Note ovate and
asymmetrical blades of variable leaflets, curved primary vein, craspedodromous secondary venation, mixed percurrent tertiaries perpendicular to secondaries, and small triangular teeth with long-rounded sinuses. A, MPEF-Pb-4416 from locality
LefE; B, MPEF-Pb-4349, LefE; C, MPEF-Pb-9154 from locality PL2; D, MPEF-Pb-3691, PL1; E, MPEF-Pb-3694, PL1. F–I, SP2.
Note well-developed palmate lobing, toothed margin, straight secondaries with opposite insertion, compound agrophic
veins, and alternate percurrent tertiaries. F, MPEF-Pb-3701a, LefL; G, MPEF-Pb-2031, PL1; H, MPEF-Pb-3701b detail of
alternate percurrent venation; I, MPEF-Pb-2031 (also H) detail of alternate percurrent venation. (Color online.)
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12
ELENA STILES ET AL.
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PATAGONIAN K/PG PLANT EXTINCTION
13
FIGURE 3. K/Pg survivor pairs (SPs; continued from Fig. 2) from the Maastrichtian Lefipán (blue circles) and Danian
(unmarked) Salamanca and Peñas Coloradas Fms. A–C, SP3, “Sterculia” acuminataloba. Note the palmately lobed form
with entire margins, three strong primary veins, central primary deflected by strong basal secondaries, interior secondaries,
intersecondary veins, agrophic veins, irregularly branching brochidodromous secondaries with spacing decreasing apically, and percurrent tertiaries nearly perpendicular to the primary vein. A, MPEF-Pb-4662a from locality LefW; B,
MPEF-Pb-3692, PL1; C, MPEF-Pb-3695, PL2. D–G, SP4, Rosaceae similar to Crataegus spp. Note ovate shape, craspedodromous secondaries, pinnate lobing with toothed lobes, large triangular teeth, opposite to subopposite secondaries. D,
MPEF-Pb-4487, LefE; E, MPEF-Pb-4482, LefE; F, MPEF-Pb-3693, PL1; G, MPEF-Pb-4030, PL1. H–J, SP5. Note ovate-elliptic
leaf shape, opposite to subopposite concave-upward brochidodromous secondaries, intersecondary veins perpendicular to
primary, widely spaced irregularly angled tertiaries ranging from opposite to alternate percurrent, and fimbrial vein running along entire margin. H, MPEF-Pb-4870, LefL; I, MPEF-Pb-4835, LefE; J, MPEF-Pb-3019, LF. (Color online.)
morphospace, but there is an increase in morphospace occupation between the terminal
Cretaceous and early Paleogene (Fig. 7). This
result shows no significant loss of characters
and higher morphological disparity in postcompared with pre-K/Pg assemblages, despite
lower species richness in the Danian. Morphospace occupation across the K/Pg is characterized by three notable shifts. First,
morphospace volume expands, driven by
Danian lobed species displaying blade incision
characters absent in the Maastrichtian. Examples include lobed species with toothed margins such as SA35 (see circled groups in
Fig. 8A). Second, within the morphospace
area shared by Maastrichtian–Danian assemblages (Fig. 8), more Danian species have
lobed blades, toothed margins, and craspedodromous venation.
FIGURE 4. Relative abundance of each survivor pair (SP; see
Figs. 2, 3) in total leaf counts from Maastrichtian and
Danian floral assemblages.
Third, extremes in morphological variation,
seen as end members along the PCoA axes,
are all represented by Danian species, signaling
higher morphological disparity in post-K/Pg
assemblages (Fig. 8). For example, with the
lowest score along axis PCoA 1, Danian species
SA35 (Fig. 8A, lower left) is lobed with craspedodromous secondary veins and toothed margins, whereas SA50 (Fig. 8B, upper right),
with the highest score for axis PCoA 1, is
unlobed
with
entire
margins
and
FIGURE 5. Rarefied leaf species richness with 95% confidence intervals for Patagonian sites (solid lines, this
study) and Williston Basin, North Dakota (dashed lines,
denoted with meters below or above K/Pg impact layer;
data from Wilf and Johnson 2004). Data include all Maastrichtian (black) and Danian (gray) dicot-leaf samples,
including singleton species (see “Methods” for details).
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14
ELENA STILES ET AL.
FIGURE 6. Compositional differences between Maastrichtian (K) and Danian (Pg) assemblages based on a species
by abundances principal components analysis (PCA),
showing increased similarity of floral composition from
the Maastrichtian (Lef) to the Danian (PL, LF) macrofloras,
even though the Danian assemblages represent a longer
time interval and a much greater array of facies types.
PCA 1 variance explained = 72.7%, PCA 2 variance
explained = 11.5%.
brochidodromous venation. Intermediate morphotypes along PCoA 1 display combinations
of entire and toothed-margined characters
and additional, less common venation types.
Maastrichtian morphotypes cluster toward
the higher scores of PCoA 1 and most share
morphological characteristics with SA50, such
as entire margins, no lobes, and brochidodromous secondaries (Fig. 8).
When we analyzed morphospace occupation
by character states (Supplementary Table 5),
the most significant observable variation was
found in characters of maximum blade size,
lobation, and margin types. Maximum leaf
size ranges from nanophyll to megaphyll,
with representatives of both Maastrichtian
and Danian species in each size class. The
representation of both Maastrichtian and
Danian leaves within the same size class
range could indicate isotaphonomic leaf assemblages. However, for purposes of morphospace
analysis, leaves in the smallest (nanophyll) and
largest (macrophyll and megaphyll) size
classes were excluded, because they included
too few specimens to produce an interpretable
morphospace occupation pattern. Individually
plotting the ordination scores by maximum leaf
size classes of each species (Fig. 9), we found
that shifts in morphospace occupation across
the K/Pg become more significant as maximum leaf size increases (Figs. 7, 9).
Within each size class, there appear to be distinct morphological trends (Fig. 9). In the
FIGURE 7. Percentage increase in leaf morphospace occupation from Maastrichtian to Danian in Patagonia based on four
measures of disparity (see “Methods” for details). A, Morphospace volume increase based on all Maastrichtian and Danian
species. B, Morphospace area change partitioned by most common leaf size classes.
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PATAGONIAN K/PG PLANT EXTINCTION
15
FIGURE 8. Morphospace occupation of Maastrichtian and Danian assemblages from principal coordinates analysis
(PCoA). The expanded Danian morphospace (see Fig. 7) indicates higher morphological diversity in post-K/Pg floras despite lower species richness. A, Axis 2 vs. axis 1. Characteristically lobed outliers driving Danian morphospace expansion
are recognized as two groups as circled; labeled exemplar species are: 1, SA35; 2, SA39; 3, SA55; 4, SA19A; 5, SA19B. B, Axis
3 vs. axis 1. Morphological end members along PCoA 1, both Danian, labeled: 1, SA35; 2, SA50.
smallest size classes, microphylls and notophylls, Maastrichtian leaves occupy a larger
morphospace than Danian species, as shown
by the four end members along axes 1 and 2
(Fig. 9A, labeled 1–4; Fig. 9B, labeled 1, 2, and
4). This result is supported by a reduction in
morphospace volume (Fig. 7B), indicating that
leaves in these size classes are more morphologically diverse in Maastrichtian assemblages.
In contrast, the larger mesophyll-sized leaves
(Fig. 9C) expand in morphospace occupation
after the K/Pg (Fig. 7B). Danian mesophylls
span a wide range of morphologically diverse
lobed, unlobed, entire-margined, and toothed
morphotypes. Mesophyll Maastrichtian morphotypes are generally entire-margined and
share self-similar secondary venation patterns
(e.g., labels 5 and 6, Fig. 9C).
We found distinct morphospaces occupied by
lobed versus unlobed species, whether we
included all species (Fig. 10A), Maastrichtianonly (Fig. 10B), or Danian-only (Fig. 10C) assemblages. Lobed leaves are consistently more morphologically disparate than unlobed types
(Fig. 10B,C), a notable result considering that
presence of lobes is only one of the more than
40 characters weighted equally in the ordination. Lobation in Danian species is generally
associated with non-entire margins and
craspedodromous venation, a relatively uncommon combination in Maastrichtian assemblages.
Regarding margin characters, in both Maastrichtian and Danian assemblages, toothed
and entire-margined morphotypes occupy distinct morphospaces (Fig. 10D), presumably in
large part a result of the numerous characters
in the matrix that pertain to toothed margins
that are coded as zeroes for entire-margined
morphotypes. However, there is some overlap
among toothed and entire-margined types in
Maastrichtian assemblages, characterized by
species with margins scored as crenate and a
few entire-margined examples (Fig. 10E). Interestingly, there is no such overlap in Danian
assemblages (Fig. 10F), graphically showing
the loss of crenate margins from pre- to
post-K/Pg assemblages and indicating one of
the few morphological losses.
Pollen Analysis and Floral Heterogeneity among
Sections.—Comparison of published pollen
records from the same sections as the macrofloral localities (Fig. 1D) shows that the Maastrichtian–Danian Lefipán and Danian-only
Salamanca Formation samples (Fig. 1A) share
most of the same pollen species and thus the
same higher taxa (families and possibly
genera), whether or not the Maastrichtian
pollen data are included. First, in the closest
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16
ELENA STILES ET AL.
(Supplementary Table 2). Second, the Salamanca Formation also shares about 75% of
palynospecies with the Danian strata of the
Lefipán (Barreda et al. 2012; Supplementary
Table 2). Thus, the same higher plant taxa are
inferred to be present in the Danian microfloras
of both formations (Fig. 1), despite the high
species-level turnover indicated by leaves.
Third, the percentage of shared palynotaxa
among the Maastrichtian Lefipán and the
Danian Salamanca (i.e., the pollen analog to
the macrofloras studied here; Fig. 1) is similar
to that among Maastrichtian and Danian Lefipán Formation samples within the SRS.
These palynological results all suggest that
geographic separation does not significantly
influence the composition of higher taxa
between the two localities, supporting the comparability of the Maastrichtian and Danian
macrofloras undertaken here. Considering all
the Danian palynotaxa (Lefipán and Salamanca), 80% are Cretaceous–Paleogene survivors based on the Cretaceous Lefipán as the
source of survivors for both formations, demonstrating the persistence of taxa including
the gymnosperm families Podocarpaceae and
Classopollis sp. (Cheirolepidiaceae) and the
angiosperm families Arecaceae, Liliaceae, Proteaceae, Symplocaceae, and Gunneraceae, as
well as various bryophytes and ferns (Supplementary Tables 1, 2). Cluster analysis of the
Beals smoothed compositional matrix (Fig. 11)
shows that despite the high percentage of palynomorph species shared between the two formations, compositional differences associated
with age and formation can be recognized.
Discussion
FIGURE 9. Morphospace occupation (axis 2 vs. axis 1) partitioned by maximum leaf size per species using the same
PCoA scores for each species shown in Fig. 8. Microphyll
is the smallest size class present; mesophyll is the largest.
A, Microphylls, selected end-member morphotypes with
icons are 1, LEF16; 2, LEF20; 3, LEF46; 4, LEF34. B, Notophylls, examples are 1, LEF64; 2, LEF01; 3, SA50; 4,
LEF05. C, Mesophylls, examples are 1, SA35; 2, SA74; 3,
LEF12; 4, SA73; 5, LEF07; 6, LEF26; 7, SA55.
stratigraphic comparison with the leaf data,
approximately 60% of palynospecies in the
Danian Salamanca Formation are shared with
the Maastrichtian part of the Lefipán Formation
A high angiosperm macrofloral extinction
percentage, drop in rarefied species richness,
depauperate and homogeneous early Paleocene floras (Fig. 6) despite spanning a range
of continental to marginal facies (e.g., Comer
et al. 2015), and significant extinction of specialized plant–insect associations in Patagonia
(Donovan et al. 2016) all provide evidence of
a significant K/Pg floral extinction event as
seen in NAM (Fig. 5) (Wolfe and Upchurch
1986; Johnson and Hickey 1990; Johnson 2002;
Wilf and Johnson 2004). Our results support a
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PATAGONIAN K/PG PLANT EXTINCTION
17
FIGURE 10. Principal coordinates analysis (PCoA axis 2 vs. axis 1) coded by time period, lobed vs. unlobed species (A–C),
and toothed vs. entire-margined species (D–F). Species ordination scores are the same as and extracted from the analysis
shown in Fig. 8. A–C, Lobed species lead the morphospace increase from Maastrichtian to Danian assemblages. D–F,
Toothed and entire-margined species occupy distinct areas of morphospace in all assemblages and increase in separation
in Danian assemblages, indicating a loss of intermediate morphospace across the extinction interval. First column shows
morphospace occupation by all species, colored by respective character. Second column shows morphospace distribution
of Maastrichtian species only. Exemplars in B, 1, LEF64; 2, LEF66; 3, LEF46; 4, LEF05; and E, 1, LEF64; 2, LEF53; 3, LEF7; 4,
LEF46. Third column shows morphospace distribution of Danian species only. Exemplars in C, 1, SA35; 2, SA48; 3, SA50; 4,
SA39; and F, 1, SA35; 2, SA50.
disruption in plant communities of global
extent across the K/Pg (Vajda et al. 2001;
Nichols and Johnson 2008; Barreda et al. 2012;
Cantrill and Poole 2012; Vajda and Bercovici
2014; Donovan et al. 2016).
Lauraceae have recently been proposed as
the principal component of K/Pg recovery
macrofloras alongside the classic fern spike in
the North American Ratón Basin (Berry 2019),
although Lauraceae are not reported from the
well-sampled early Danian localities in North
Dakota (Johnson 2002). The dominance of
L. piatnitzkyi in early Paleocene Patagonian
macrofloras, and of several other leaf morphotypes assigned to the family (Iglesias 2007; Iglesias et al. 2007) would be consistent with the
presence of Lauraceae-dominated K/Pg recovery floras in regions of both North and South
America.
Despite the similarities between Patagonian
and North American records, the subtle differences between them suggest that extinction
could have been heterogeneous between the
two regions. Morphological turnover shows
interesting differences between the WB and
Patagonia, even though the WB floras have not
been analyzed in morphospace. Maastrichtian
assemblages of North Dakota are characterized
by the abundance of leaves with a “Cretaceous
look” or unusual lobation (Johnson 2002:
p. 371), a feature that is drastically reduced in
the early Paleocene (Johnson and Hickey 1990;
Johnson 2002). In contrast, the increase in proportion of lobed and toothed species in the
early Paleocene of Patagonia (Fig. 8) (Iglesias
et al. 2007) leads to an expansion in morphospace occupation by post-K/Pg assemblages.
Despite our estimate of almost complete
species-level macrofloral turnover in Patagonia,
the continuity and expansion of leaf morphologies (Fig. 8) and, presumably, their underlying
ecological and phylogenetic diversity across
the K/Pg could, in part, reflect low turnover at
higher taxonomic levels observed in both the
microfloral and macrofloral records of Patagonia (Barreda et al. 2012; Supplementary Table 1).
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18
ELENA STILES ET AL.
FIGURE 11. Cluster analyses of palynospecies occurrences
with Beals smoothing (see “Methods” and Fig. 1) from the
Maastrichtian (samples M1–3) and Danian (D1–11) Lefipán
Fm. (Barreda et al. 2012) and Danian-only Salamanca Fm.
(remaining samples; Fig. 1) (Clyde et al. 2014). A, All species.
B, Gymnosperms and angiosperms only. C, Angiosperms only.
Both WB and Patagonian species richness
suffer a sharp drop between Maastrichtian
and Danian assemblages (Fig. 5). The K/Pg
drop in rarefied species richness, though severe
in both areas, is much sharper in the WB
(ca. 75%) than in Patagonia (ca. 45%; Fig. 5).
Rarefaction highlights another important
contrast between the WB and Patagonian
records; not only Danian (Iglesias et al. 2007)
but also Maastrichtian assemblages in Patagonia are significantly more diverse than coeval
macrofloras in the WB. The Lefipán floras are
approximately 40% richer than the most
diverse Maastrichtian Hell Creek (HCIII)
NAM zone assemblage (Fig. 5). Thus, whereas
previous studies of the Danian Salamanca Formation (Iglesias 2007; Iglesias et al. 2007) and
Eocene macrofloras of Patagonia (Wilf et al.
2003a, 2005) provided evidence for an ancient
history of high South American Cenozoic floral
diversity, our results (Fig. 5) extend that history
into the Late Cretaceous.
The high species richness of Patagonian
Paleocene and Eocene assemblages compared
with NAM equivalents has been hypothesized
in part to be the legacy of low K/Pg floral
extinction as observed in the palynological
record (Barreda et al. 2012). Our results suggest
that the rich Cenozoic macrofloras of Patagonia
also carry a legacy of rich Cretaceous floras, as
well as significantly earlier recovery of Paleocene species richness resulting from the persistence of most higher taxonomic levels
(Supplementary Tables 1, 2). Nonetheless, an
emerging body of research shows that floral
diversity in the early Paleocene of the Denver
and San Juan Basins can be higher relative to
the more northerly WB (Johnson and Ellis
2002; Flynn and Peppe 2019; Lyson et al.
2019). These studies show heterogeneity in
NAM floral richness during the early Paleocene, a pattern warranting further intensive
study.
Insect damage-type data on the same leaf
collections studied here showed a similar pattern of high extinction and robust early recovery compared with NAM (Donovan et al.
2016, 2018). Donovan et al. (2016, 2018) posed
the disappearance of plant hosts across the K/
Pg as a potential driving mechanism for the
severe insect herbivore extinction observed in
Patagonia; host-specialized insects such as leaf
miners would have been severely affected by
an elevated species-level floral extinction (as
in NAM: Labandeira et al. 2002; Donovan
et al. 2014). Our results confirm this interpretation and suggest that despite the low K/Pg
turnover of major clades observed in floras of
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PATAGONIAN K/PG PLANT EXTINCTION
Patagonia and elsewhere (see Sauquet and
Magallón 2018), high plant-species turnover
resulted in devastating consequences for terrestrial faunas.
The empirical species-extinction percentage
of >90% in Patagonia in all likelihood is positively biased by several factors, including
coarser stratigraphic sampling than in WB
macrofloras, geographic variation, and climatic
effects, and that is why we present it as a maximum estimate. Regarding sampling, the
uncertain temporal placement of the Lefipán
Formation macrofloras within the last ca. million years before the K/Pg boundary (Barreda
et al. 2012; Vellekoop et al. 2017) and the lack
of earliest Danian (chron 29r) sediments preserved in the Salamanca Formation probably
bias against finding a higher number of survivor pairs (Fig. 1). The limited stratigraphic
coverage of macrofloras in the upper Lefipán
Formation is analogous to considering only a
small interval of the Hell Creek Formation
(Johnson et al. 1989; Johnson 2002; Wilf and
Johnson 2004), where there is a general trend
of lower percentages of observed survivor
dicot-leaf species in a simple experiment
where the distance of sample windows below
the boundary layer increases (Fig. 12). Furthermore, observed extinction may exceed 90%
even for some intervals relatively close to the
boundary, as can be seen in the 20–30 m and
40–50 m bins of the Hell Creek Formation
(Fig. 12). Although there are macrofloral collections from lower Lefipán Formation strata
(Andruchow-Colombo et al. 2018; Martínez
et al. 2018), their precise age is not known,
and the preserved diversity of dicot leaves is
not nearly so extensive as in the upper Lefipán
studied here. Therefore, observations across a
wide stratigraphic range in the Lefipán Formation are not possible at this time.
Addressing the geographic separation
between the Maastrichtian and Danian macrofloras (Fig. 1), the cluster results showing differences between the Lefipán and Salamanca
sections’ microfloral assemblages (Fig. 11) provide evidence for some geographical heterogeneity of higher-taxa associations, which would
accentuate species-level contrasts observed in
the respective macrofloras (Behrensmeyer et al.
2000; Nichols and Johnson 2008). Different
19
FIGURE 12. Simulated percentage of K/Pg-surviving Cretaceous dicot-leaf species in the Williston Basin of North
Dakota by 10 m bin window below the K/Pg impact horizon (data from Wilf and Johnson [2004], including singletons; see “Discussion” for details). The Lefipán leaf floras
studied here, with a 91% observed extinction, could correlate temporally to any one of these stratigraphic bins.
underlying palynospecies associations suggest
that the 400 km spatial separation of Maastrichtian and Danian assemblages plays some role
in the likely overestimation of Patagonian macrofloral extinction by imparting a geographical bias
(Fig. 11). On the other hand, geographic effects
could not have been severe, because the number
of shared palynospecies in the same strata as the
leaf floras was very high (see “Results”).
With regard to climate, marine and continental proxy records show a global relatively shortlived climatic warming within the last ca. 500
kyr of the Maastrichtian, followed by cooling
during the final ca. 100 kyr of the Maastrichtian
persisting into the early Paleocene (Stott et al.
1990; Huber and Watkins 1992; Wilf et al.
2003b; Bowman et al. 2014; Vellekoop et al.
2017; Woelders et al. 2017; Huber et al. 2018;
Hull et al. 2020). The increase in toothed and
lobed leaf morphotypes across the K/Pg in
Patagonia (39.7% to 60.5% and 12% to 27.9%,
respectively), both of which are observed drivers of morphospace expansion in Paleogene
floras, would correlate to a ca. 5°C drop in
mean annual temperature, with standard
caveats for paleoclimatic inference on this
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20
ELENA STILES ET AL.
basis (Wolfe 1971; Greenwood et al. 2004; Little
et al. 2010). The uncertain age within the last
million years of the Maastrichtian of the Lefipán
Formation macrofloras studied here, however,
introduces an important potential climatic bias
on observed extinction that would compound
the sampling bias mentioned earlier.
In the Hell Creek Formation, peak richness of
floral diversity (HCIII zone flora) correlates
with the highest temperature estimates of the
late Maastrichtian, followed by a decline in species richness during rapid cooling in the terminal Maastrichtian (Wilf et al. 2003b). If a
comparison were to be made solely between a
collection of Maastrichtian HCIII floras from
the peak of diversity of warmth and those of
the Fort Union, an overestimation of extinction
percentages would result. For example, if we
only compare the −15 m (HCIII) and +38 m
(in C29N like the PL1 flora) horizons in North
Dakota (Wilf et al. 2003b; Wilf and Johnson
2004), the observed dicot-leaf extinction is
99%. Although it is not possible to state the
age of the Maastrichtian Lefipán Formation
floras at this precision, their high species richness, dinoflagellate markers indicative of the
last 0.5 Myr of the Cretaceous, and associated
warm proxy temperatures (Barreda et al. 2012;
Scasso et al. 2012; Vellekoop et al. 2017) suggest
that they could correlate to the terminal Cretaceous warming event and thus HCIII, possibly
translating into an overestimation of macrofloral extinction in this study on the assumption
that temperature correlates with plant
diversity.
Conclusions
We report the first K/Pg macrofloral investigation in the Southern Hemisphere that is
based on large, stratigraphically constrained
collections. Our 92% observed macrofloral
extinction is best viewed as a maximum
because of likely geographic, stratigraphic,
and paleoclimatic biases. Nonetheless, our estimate clearly reflects underlying high
species-level turnover in Patagonia. High
macrofloral turnover and associated insect
herbivore extinction, compositionally homogeneous Danian floras, and a sharp drop in rarefied floral species richness in Patagonia
reveal extinction and recovery patterns broadly
resembling those observed in NAM and support a geographically widespread extinction
event. However, Patagonian and North American turnover show contrasts.
Compared with NAM floras of the WB in
North Dakota, Patagonian floras are much
more diverse in both Maastrichtian (Fig. 5)
and Danian (Iglesias et al. 2007) assemblages.
Richer Maastrichtian floras in Patagonia may
have contributed to the less severe drop in overall species richness and significantly faster
Danian recovery than observed in the WB or
other northern Great Plains floras. Insect herbivory observations on the same collections
(Donovan et al. 2016, 2018) follow patterns
similar to North American records, indicating
that the macrofloral species extinction in Patagonia had catastrophic effects on herbivorous
insect communities. However, like their host
macrofloras, specialized insect damage types
in Patagonia recover much faster than those in
NAM, despite high turnover in both regions.
This study reports speciose Maastrichtian
macrofloras in Patagonia for the first time,
extending the history of elevated floral diversity in South America into the terminal Cretaceous. The limited palynological extinction
and continuity of most higher taxa (families
and genera) across time and space indicate persistence of major plant clades even as significant extinction took place at the species level.
Leaves with lauraceous affinity are characteristically dominant in the Patagonian macrofloral
assemblages, as in the NAM Ratón Basin,
drawing an interesting parallel between the
two regions. In addition to Lauraceae, we provide macrofloral evidence to support the survival of the families Cunoniaceae, Malvaceae,
and Rosaceae in Patagonia.
Morphospace analysis of Maastrichtian–
Danian Patagonian macrofloras shows minimal
character loss from the K/Pg extinction and
that Danian macrofloras are morphologically
more diverse than Maastrichtian assemblages.
Danian floras rich in lobed and toothed species
appear to be a notable Patagonian characteristic
that contrasts with North American macrofloras of the WB, where lobed forms largely disappear across the K/Pg. Increased diversity of
toothed species in Danian Patagonian
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PATAGONIAN K/PG PLANT EXTINCTION
assemblages is probably related to a general climatic cooling, potentially aligning with global
temperature records.
Extinction and recovery in Patagonian macrofloras parallel North American WB assemblages
in the K/Pg drop of rarefied species richness,
low-diversity homogeneous Paleocene floras,
and dramatic loss of specialized insect herbivores, indicating that terrestrial ecosystems in
both areas were severely disrupted. Contrasts
between Patagonian and North American
macrofloras emerge in a faster Patagonian recovery, comparably much higher floral diversity
throughout the Cretaceous–Paleogene time interval, and differences in morphological turnover.
Acknowledgments
We thank the technical staff of the Museo
Paleontológico Egidio Feruglio (MEF), including
P. Puerta, M. Caffa, E. Ruigomez, L. Reiner, and
L. Canessa, as well as K. Johnson, R. Scasso,
M. Donovan, and many others for their
field and laboratory assistance over several expeditions and collections visits. We thank
V. Barreda for her assistance reviewing palynological records and M. Patzkowsky and
T. Bralower for valuable advice during the development of this project. We thank the editors,
K. Boyce and C. Looy, and V. Vajda and three
anonymous reviewers for providing constructive
feedback that helped us improve this article.
Funding was provided to E.S. by Geological
Society of America Student Research grant
no.12008-18, a Mid-American Paleontological
Society (MAPS) Outstanding Research Award,
the Penn State Geosciences Charles E. Knopf,
Sr., Memorial Scholarship, and two Penn State
Geosciences Paul D. Krynine Scholarships, as
well as contributions from National Science
Foundation grants DEB-15556666/1556136,
EAR-1925755/1925552, DEB-0919071/0918932,
and DEB-0345750 that benefited all authors.
This work partially fulfilled the M.Sc. in Geosciences degree requirements of E.S. at Penn
State University.
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FIRST SOUTH AMERICAN AGATHIS (ARAUCARIACEAE),
EOCENE OF PATAGONIA1
PETER WILF2,7, IGNACIO H. ESCAPA3, N. RUBÉN CÚNEO3, ROBERT M. KOOYMAN4,
KIRK R. JOHNSON5, AND ARI IGLESIAS6
2Department
of Geosciences, Pennsylvania State University, University Park, Pennsylvania 16802 USA; 3Museo Paleontológico
Egidio Feruglio, Consejo Nacional de Investigaciones Científicas y Técnicas, Trelew 9100, Chubut, Argentina; 4National
Herbarium of New South Wales, Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney 2000, New South
Wales, Australia; 5National Museum of Natural History, Smithsonian Institution, Box 37012 MRC 106, Washington, D.C. 20013
USA; and 6División Paleontología, Universidad Nacional del Comahue, Instituto de Investigaciones en Biodiversidad y
Ambiente–Consejo Nacional de Investigaciones Científicas y Técnicas, San Carlos de Bariloche 8400, Río Negro, Argentina.
• Premise of the study: Agathis is an iconic genus of large, ecologically important, and economically valuable conifers that range
over lowland to upper montane rainforests from New Zealand to Sumatra. Exploitation of its timber and copal has greatly
reduced the genus’s numbers. The early fossil record of Agathis comes entirely from Australia, often presumed to be its area of
origin. Agathis has no previous record from South America.
• Methods: We describe abundant macrofossils of Agathis vegetative and reproductive organs, from early and middle Eocene
rainforest paleofloras of Patagonia, Argentina. The leaves were formerly assigned to the New World cycad genus Zamia.
• Key results: Agathis zamunerae sp. nov. is the first South American occurrence and the most complete representation of
Agathis in the fossil record. Its morphological features are fully consistent with the living genus. The most similar living species
is A. lenticula, endemic to lower montane rainforests of northern Borneo.
• Conclusions: Agathis zamunerae sp. nov. demonstrates the presence of modern-aspect Agathis by 52.2 mya and vastly increases the early range and possible areas of origin of the genus. The revision from Zamia breaks another link between the
Eocene and living floras of South America. Agathis was a dominant, keystone element of the Patagonian Eocene floras, alongside numerous other plant taxa that still associate with it in Australasia and Southeast Asia. Agathis extinction in South America
was an integral part of the transformation of Patagonian biomes over millions of years, but the living species are disappearing
from their ranges at a far greater rate.
Key words:
Río Pichileufú.
Agathis; Araucariaceae; Argentina; Borneo; conifers; Eocene; extinction; Laguna del Hunco; rainforests;
Agathis R. A. Salisbury (Araucariaceae; kauri, dammar) is
one of the most impressive and valuable tree genera in the
world, but little is known about its evolutionary and biogeographic history. Several recent molecular-clock studies have
given a wide range of estimates of its age (Knapp et al., 2007;
Biffin et al., 2010; Crisp and Cook, 2011; Leslie et al., 2012).
We begin with a brief introduction to living Agathis, followed
by an overview of its limited fossil record, which was, until
now, entirely from Australia and New Zealand.
Living Agathis—Agathis has ca. 17 species distributed across
lowland to upper montane rainforests in Australasia and Southeast
Asia (Table 1). Agathis has broad leaves, outlives most competing
canopy angiosperms, and characteristically emerges above them at
giant size (several species reach 50–65 m height). The genus is a
backbone element of forest architecture and element cycling, supports diverse epiphytes and fungi, and is an important source of
animal food, shade, roosting space, and shelter (Dumbleton, 1952;
Mirams, 1957; Wise, 1962; Ripley, 1964; Gorman, 1975; Towns,
1981; Ecroyd, 1982; Enright and Ogden, 1987; Bishop, 1992;
Greene, 1998; Silvester and Orchard, 1999; Jongkind et al., 2007;
Verkaik and Braakhekke, 2007; Wyse, 2012). Most areas where
Agathis grows are rainforests with many rare or endemic species of
plants and animals (e.g., Enright, 1995; Wong and Phillipps, 1996;
Morrogh-Bernard et al., 2003; Balete et al., 2009; Wilcove et al.,
2013). Agathis can be an important component of tropical peatlands (Yii, 1995), whose organic carbon flux has increased ca. 32%
since 1990 in Southeast Asia as a result of disturbance (Moore et
al., 2013). Thus, Agathis removal and related disturbance on a
large scale are likely to have significant detrimental effects on carbon balance, biodiversity, and ecosystem structure and function.
Human impacts on Agathis populations are indeed enormous
(Whitmore, 1977, 1980a; Bowen and Whitmore, 1980a, 1980b;
1 Manuscript received 9 September 2013; revision accepted 21 November
2013.
The authors thank M. Caffa, L. Canessa, B. Cariglino, M. Carvalho, M.
Gandolfo, C. González, R. Horwitt, M. Gandolfo, E. Hermsen, K.
Kitayama, S. Little, H. Mujih, P. Puerta, L. Reiner, E. Ruigómez, and S.
Wing for their extraordinary assistance in the field and laboratory and/or
helpful and timely comments; the staff at CANB (B. Lepschi and C.
Cargill), NSW (L. L. Lee and L. Murray), US (A. Clark, I. Lin, K. Rankin,
and R. Russell), and USNM (J. Wingerath) for expediting specimen access
and loans; and the Nahueltripay family and Instituto de Investigaciones
Aplicadas for land access. This work received primary support from
National Science Foundation grants DEB-0919071, DEB-0918932, and
DEB-0345750 and from the David and Lucile Packard Foundation, as well
as early support from National Geographic Society grant 7337-02, the
University of Pennsylvania Research Foundation, and the Andrew W.
Mellon Foundation.
7 Author for correspondence (e-mail: pwilf@psu.edu)
doi:10.3732/ajb.1300327
American Journal of Botany 101(1): 156–179, 2014; http://www.amjbot.org/ © 2014 Botanical Society of America
156
January 2014]
TABLE 1.
Agathis zamunerae sp. nov., general features compared with the 17 living Agathis species.
Leaves
Species, range
bract
pairs
bracts,
i or s
Cone scale
Seed body
Larger seed wing
length
ms
arr
ms
height
ms
width
shape
length
length
width
length
width
length
width
e, l
24–132
2.2–7.3
3
i
23–56
i
1.5–2.1
1.3–2.0
19–26
21–36
11.8
ca. 7
13.4
8.1
e, l
30–80
2–3
4–5
i
9–16
i
0.5–0.7
0.6–0.8
16–23
23–30
7–9
4–5
12–15
8
l, o
23–70
5–15
3
i
30–50
i
2.1–2.7
1.8–2.5
~20
~30
8–10
5
12
8
e, l, o
25–140
1–8
2
s
20–90
i
5–6
4–8
~35
35–45
12–15
7–8
20
13
l, o, o–e
25–140
0–5
2–4
s
10–40
i
1–1.5
2–2.5
~35
35–45
12–15
7–8
20
13
l–o, o
o, ob, o–l
20–80
20–90
2–15
2–5
2
2–3
s
s
10–40
10–30
i
i
1.5
1.2–1.6
2
1.6–1.8
~30
~30
~40
40–45
11–13
11–13
7–8
7–8
15
15–20
10
10–12
e, l, l–o
50–140
2–10
4
i, s
22–30
t
0.7–1.0
1–1.5
~30
35–40
12
7
20
15
l
60–130
4–5
4
s
20–25
t
0.5–1.8
<1.6
~25
30–35
12–15
7
20
13
e, l, len, o–e
l, o–l, ob
50–110
25–170
2–10
0–7
2–3
4
i
i
10–40
20–45
i
i
1.5–2
1.8–2.2
2–2.5
1.4–2.2
25–30
~35
30–35
35–45
10
12–15
6
7–8
15
20–25
8
10–15
e, l
30–90
0–1
4–5
i
10–16
t
0.5–0.7
0.5
25–35
33–45
10–12
6–8
20–25
10–13
o, o–len
55–110
~0
5–8
i
40–70
i
2.2–2.5
2.0–2.6
~30
~30
6–8
5
n/a
n/a
e, l, o–e
45–200
1–12
4–8
i
25–50
i
0.8–2
1–3
30–40
30–40
15–20
8–10
20–30
15–20
l, o, ~orb
20–70
2–3
2–3
s
6–15
i
1
1.2–1.5
~20
~30
10
6
12
6
ob–tr, ob–tr, ~orb
40–85
4–20
4–5
i
30–50
i
1.8–4.5
2–4.5
16–20
22–26
9–11
7–8
15–20
9–12
e, l, obl
50–140
2–18
4–5
i, s
40–70
i/t
0.7–1.5
1–2
~30
35–42
12–14
7–8
20–25
12–15
l, o
40–120
0–6
2–3
~i
35–60
i/t
2.1–2.5
1.8–2.5
~35
40–50
12–15
7–8
20–25
13–17
WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
Agathis zamunerae Wilf,
sp. nov., Patagonia
A. atropurpurea B. Hyland,
Austr.
A. australis (D. Don) Lindl.,
New Zealand
A. borneensis Warb.,
Borneo to Sumatra
A. dammara (Lamb.)
Rich. & A. Rich., Malesia
A. flavescens Ridl., Malaysia
A. kinabaluensis de Laub.,
Borneo
A. labillardierei Warb.,
New Guinea
A. lanceolata (Sébert
& Pancher) Warb., New Cal.
A. lenticula de Laub., Borneo
A. macrophylla (Lindl.)
Mast., Fiji, Vanuatu,
Solomons
A. microstachya J. F. Bailey
& C. T. White, Austr.
A. montana de Laub.,
New Cal.
A. moorei (Lindl.) Mast.,
New Cal.
A. orbicula de Laub.,
Borneo
A. ovata (C. Moore ex
Vieill.) Warb., New Cal.
A. robusta (C. Moore ex
F. Muell.) F. M. Bailey,
Austr., New Guinea
A. silbae de Laub., Vanuatu
Pollen cones
ped
length
Notes: Extant species data from Farjon (2010). All measurements in millimeters. Abbreviations: arr, arrangement; Austr., Australia; br, bract; e, elliptic; i, imbricate; l, lanceolate; len, lensshaped; ms, microsporophyll; New Cal., New Caledonia; o, ovate; ob, obovate; obl, oblanceolate; orb, orbicular; ped, peduncle; s, spreading; t, tessellate; tr, truncate.
157
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Figs. 1–7. Agathis zamunerae sp. nov., leafy twigs. Figs. 1 and 2, Río Pichileufú. Figs. 3–7, Laguna del Hunco. 1, 2. Specimens figured as “Zamia
tertiaria” by Berry (1938: pl. 9, USNM 40378h, and pl. 8, fig. 5, USNM 40378d part, respectively). Fig. 1 arrows: lower arrow indicates point expanded
January 2014]
WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
Soerianegara et al., 1993; Farjon et al., 1993; Farjon, 2010).
The economically prized genus has been dramatically reduced
from most of its lowland ranges, and many large forests that it
once dominated no longer exist. Many species are still declining and are under conservation threat, in all likelihood still losing significant genetic diversity (Kitamura and Abdul Rahman,
1992). The timber is an extremely versatile, odorless softwood
(Kirk, 1889; Whitmore, 1977). Exports of Agathis logs from
Indonesia alone reached 760 000 m3 in a single year (1973), and
a 30 000-ha forest in Kalimantan, dominated by Agathis with
ca. 200 m3 timber ha–1, was completely logged out by the 1960s
(Whitmore, 1977; Soerianegara et al., 1993; Farjon, 2010). The
New Zealand species, A. australis, was cleared from an estimated 1.2 million ha to ca. 7500 ha coverage (>99% loss) in
only ca. 50 yr (Whitmore, 1977; Farjon, 2010). Agathis microstachya (Australia) lost about half its population, and A. dammara (Malesia) has been reduced by ≥30% (Farjon, 2010). In
New Caledonia, nickel mining impacts have greatly reduced
Agathis populations, as well as logging (Farjon, 2010; Jaffré
et al., 2010). In addition, Agathis is especially resiniferous
(Salisbury, 1807), and its Manila copal was extensively tapped
and dug from underground deposits (“gum-digging”) for diverse industrial uses (Kirk, 1889; Soerianegara et al., 1993;
Mabberley, 2002). The remaining populations of several species have limited protection in nature reserves, but many of
these are vulnerable to poaching, degazetting, clearing of surrounding buffer areas, and climate change. As adjacent lowlands
are cleared and pressures from marginal tropical agriculture
move upslope, the montane populations of Agathis are increasingly threatened.
Agathis reproductive organs and adult foliage are notoriously difficult to sample without felling or shooting (Howcroft, 1987). They are mostly borne above long trunks that
are dangerous to climb because of copious slippery resin and
abscision of the lower branches. Many species are endemic
to very remote or steep montane areas. Also, the large, globose seed cones shatter at maturity. Even when well sampled, there is little morphological variation among the
species, such that minute technical characters of pollen cones
found in the litter are usually needed to identify a giant tree
(Meijer Drees, 1940; Whitmore, 1980b). As a result, detailed
knowledge of morphological and genetic variation—and,
thus, a solid systematic framework—have not yet been established for Agathis. Even the two most recent treatments
differ substantially in species delimitations (Eckenwalder,
2009; Farjon, 2010).
Fossil Agathis— The evolutionary and biogeographic history of Agathis remains poorly known from the fossil record, in
sharp contrast to the outstanding, global Mesozoic and Southern Hemisphere Cenozoic fossil record of its familial relative
Araucaria. There is a long history of uncertain or dubious identifications of Mesozoic and Cenozoic material to Agathis, as
discussed elsewhere (Seward and Ford, 1906; Florin, 1940a;
159
Stockey, 1982; Hill, 1994; Brodribb and Hill, 1999; Hill et al.,
2008; Pole, 2008).
According to the most recent reviews (Hill et al., 2008; Pole,
2008), the only reliable fossil Agathis occurrences are Cenozoic
and from the limited area of southern Australia, late Paleocene
to early Miocene, and New Zealand, late Oligocene–Miocene.
While clearly suggesting a Gondwanan origin for what is now
mostly a tropical genus, nearly all these fossil occurrences are
of leaf fragments with in situ cuticle or of dispersed cuticles,
and several of the interpretations are contentious. Agathis tasmanica R. S. Hill and Bigwood (1987), early Oligocene of Little Rapid River and Cethana, Tasmania, is one of the few
examples that convincingly preserves the complete leaf form.
This includes the typical Agathis short petiole (“false petiole,”
sensu Offler, 1984), the basal constriction of the blade that is
not found in the other living Araucariaceae, Araucaria Juss.
and Wollemia W. G. Jones et al., nor in the extinct Araucarioides Bigwood and R. Hill, which co-occurs with Agathis and
Araucaria in Cenozoic sediments of Tasmania (Bigwood and
Hill, 1985; Hill et al., 2008). Pole (2008) disputed some of the
other Australian examples as potentially belonging to other
genera. In New Zealand, abundant but isolated leaves from
Newvale Mine (Oligocene–Miocene) were first assigned to Agathis sp. aff. A. australis (Lee et al., 2007) and later to Agathis
sp. (Jordan et al., 2011); these were stated to lack petioles (although no leaf base was shown), which is unusual for Agathis
but does occur on adult leaves of A. australis (Kirk, 1889), and
to have a sharply acute apex, a feature found in few living Agathis species and not in A. australis (Offler, 1984; see also Hill
et al., 2008). Moreover, Pole (2008) found the cuticular characters of the Newvale Mine fossils inconclusive. The possibility
remains that the Newvale Mine fossils represent a species of
Araucariaceae outside of Agathis.
Regarding reproductive organs, Cookson and Duigan (1951)
reported two seed cones and one pollen cone containing araucariaceous pollen, both associated with Agathis yallournensis
Cookson and Duigan leaves (Oligocene–Miocene, Victoria),
that they considered to be reproductive organs of A. yallournensis. Although the pollen cone did not preserve basal bracts, the
remaining features are consistent with Agathis and distinct (as
discussed by Cookson and Duigan) from Araucaria pollen
cones also found at the site with associated Araucaria lignitici
leaves. Otherwise, Agathis pollen cones have no fossil record
prior to the present study, although they are the principal organs
that show variation reliably at the species level (Whitmore,
1980b; Farjon, 2010) and, thus, are essential for any refined
interpretation of fossils. The oldest previously illustrated fossil
of a likely bract-scale unit (here, “cone scale” as widely used)
dispersed from an Agathis seed cone is from the early Oligocene Cethana flora of Tasmania (Carpenter et al., 1994),
although Agathis cone scales have been mentioned without
illustration from the late Eocene Vegetable Creek flora, New
South Wales (Hill, 1995). In New Zealand, a late Miocene cone
scale and leaf base from the Oruawharo locality (Pole, 2008)
←
in the inset, showing an attached leaf base with obliquely raised, darkened abscision zone; upper arrow expands to Fig. 10. 3. Spray with three abscision
scars on one side of twig opposite the attached leaves, small terminal bud, and insect-feeding damage. MPEF-Pb 6303b, from quarry LH6. 4. Spray showing opposite branching, prominent grooves on twigs, numerous abscision scars with supporting tissues decurrent on the twig, well-preserved leaf bases with
twisted petioles, and large, scaly terminal bud subtended by a prominent growth-increment scar. MPEF-Pb 6319, from LH25. 5. Spray showing opposite
branching, two terminal buds (arrows), copious amber preserved as white, longitudinal stripes in twigs and leaves (note long distal leaf). MPEF-Pb 6313,
from LH13. 6. Spray with terminal bud, weathered white. MPEF-Pb 6304b, from LH6. 7. Spray portion showing twisted leaf bases and large, scaly terminal
bud. MPEF-Pb 6321a, from LH27 (also Fig. 8).
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AMERICAN JOURNAL OF BOTANY
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Figs. 8–15. Agathis zamunerae sp. nov., twig features, from Laguna del Hunco except Fig. 10, from Río Pichileufú. Arrows with same orientations indicate corresponding points. 8. Detail of terminal bud shown in Fig. 7, under partial epifluorescence, showing overlapping, closely adpressed bud scales and
remnant surface relief. 9. Spray portion showing small terminal bud and subtending pair of opposite leaves. Note abundant amber (white). MPEF-Pb 6312,
from LH13. 10. Detail of twig at a leaf attachment point (corresponding to upper arrow in Fig. 1), showing grooved twig and leaf divergences typical for Agathis
in a historical specimen. 11. Well-preserved twig with one remaining attached leaf, strong longitudinal grooves, several (sub)opposite, decussate abscision
scars, swellings, and breakage scars. MPEF-Pb 6305a (left), b (right and Figs. 12–14), from LH6. 12. Detail, well-developed grooves and ridges and blanketing
mesh of tiny, quadrangular epidermal cells of the former green twig. 13. Detail, grooves and epidermal cells. 14. Detail of dark, raised abscision scar supported
by woody supply tissues extending from the twig. 15. Composite image (9 panels) of a grooved twig, apical direction to right, with several opposite decussate
pairs of abscision scars and one attached leaf at right (three others attached to this twig are outside of frame). MPEF-Pb 6320b, from LH27.
provide a more convincing, though younger example of fossil
Agathis than the Newvale Mine fossils mentioned above.
Given the sparse, fragmentary record, the fossils so far assigned to Agathis may or may not represent plants that had
abundant features of the living genus. Based on the known fossil record exclusive to Australia and New Zealand, it has long
been suggested that Agathis probably evolved in those areas
(Florin, 1963:181; Gilmore and Hill, 1997; Hill and Scriven,
1998; Kunzmann, 2007). Likewise, no fossil or native living
Agathis has previously been recorded from South America.
The Eocene fossil sites of Patagonia are producing a large
number of extant conifer, fern, and angiosperm genera that
show trans-Antarctic connections to fossil and extant Australasian floras (see Materials and Methods). These occurrences
January 2014]
WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
161
Figs. 16–24. Agathis zamunerae sp. nov., leaves. Note dark abscision scars with elliptical cross sections, well-defined petioles, blunt apices, range of
aspect ratios, and parallel, straight venation. Figs. 17 and 23, Río Pichileufú (arrows show corresponding points), others from Laguna del Hunco. 16. Leaf
with abundant coalified mesophyll. MPEF-Pb 6365, from LH13. 17. Specimen figured as “Zamia tertiaria” by Berry (1938: pl. 8, fig. 4, USNM 40378f
counterpart). Note typical Agathis features listed above, plus abundant, longitudinal amber casts of the resin ducts (also Fig. 23). 18. MPEF-Pb 6363, from
LH13. 19. MPEF-Pb 6374, from LH27 (also Figs. 26, 27, and 30). 20. MPEF-Pb 6359a, from LH13 (also Figs. 21 and 22). 21, 22. Details at and near base
of MPEF-Pb 6359a (Fig. 20), showing constricted petiole and bifurcating veins. 23. Detail, left-margin of leaf in Fig. 17, showing resin ducts (white amber
casts) alternating with veins (dark, coalified). 24. Petiole detail, showing elliptical cross section. MPEF-Pb 6334, from LH6.
notably include evidence for the other two extant genera of
Araucariaceae: Wollemia-type pollen (Dilwynites) has recently
been discovered in the early middle Eocene Ligorio Márquez
Formation in Santa Cruz Province, Argentina, although some
living species of Agathis can produce similar pollen (Macphail
et al., 2013; Macphail and Carpenter, 2013), and Araucaria
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AMERICAN JOURNAL OF BOTANY
[Vol. 101
Figs. 25–31. Agathis zamunerae sp. nov., fine leaf-surface features, all with long axis of leaf vertical and apex upward, Laguna del Hunco. All under
epifluorescence except Fig. 27. 25. Set of parallel veins, no stomata preserved. MPEF-Pb 6386, from LH27. 26, 27. Veins with intervening rows of numerous,
coalified, randomly oriented Florin rings, from leaf shown in Fig. 19 (also Fig. 30). Same approximate leaf area under epifluorescence (Fig. 26) and under
reflected light to show visual cues as under a hand lens (Fig. 27), corresponding Florin rings circled. 28. As in Fig. 26, different leaf, with resin duct remains
(white amber cast) and coalified mesophyll. MPEF-Pb 6322b, from LH27 (also Figs. 29 and 31). 29. Detail from leaf shown in Fig. 28 (also Fig. 31). 30. Guard
cell casts preserved within coalified Florin rings, from leaf shown in Figs. 19, 26, and 27. 31. Guard cell cast, from leaf shown in Figs. 28 and 29.
macrofossils have long been known from many Patagonian
sites (Panti et al., 2012), including those studied here (Berry,
1938; Wilf et al., 2005).
In his classic monograph on the middle Eocene Río Pichileufú flora of Río Negro Province, Argentina, Berry (1938) illustrated a number of foliar specimens, several attached to axes
(Figs. 1 and 2), that he assigned to the putative cycad “Zamia”
tertiaria Engelhardt (1891), a name based on a fragmentary leaf
fossil from Eocene deposits in Chile. Zamia L. is an entirely
New World genus. We have recovered numerous new specimens of “Zamia tertiaria” sensu Berry 1938 at Río Pichileufú
and, especially, from the early Eocene Laguna del Hunco flora,
where it is the seventh most abundant leaf type among >150
overall, and by far the most common gymnosperm leaf type
(Wilf et al., 2005: fig. 3). The leaves also preserve a notable
richness of insect-feeding damage, under separate study (C. C.
Labandeira et al., unpublished data). A priori, this high relative
abundance of broad fossil leaves, indicating very significant
biomass (e.g., Burnham et al., 1992) and a large component
community, seemed very unlikely for a presumably small cycad
species within a forest of tall rainforest trees (e.g., Wilf, 2012), and
it became clear from a number of features, especially the bumpy
January 2014]
WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
163
Figs. 32–36. Agathis zamunerae sp. nov., (presumed) immature seed cone from Laguna del Hunco, terminal on a thickened branch, with large, transverse growth increment scar (rightward arrows). Numerous imbricate, upturned cone-scale apices are preserved across the cone base as impressions with
very low but visible relief, their distal margins coalified, forming a pattern of numerous, darkened, concave-downward arcs (the margins) capping slight
bulges in the matrix (the apex impressions). MPEF-Pb 6391b, from LH27. Arrows with same orientations indicate corresponding points. Fig. 35 equals Fig.
34 with colors reversed. 32. Whole specimen. 33. Detail of the area preserving cone-scale impressions/margin compressions, subtended by the growth increment scar, composite image under low-angle light. 34–36. Details of surface.
twigs with well-defined terminal buds and decussate phyllotaxy,
that “Z. tertiaria” sensu Berry 1938 is a conifer with simple
leaves, not a compound-leaved cycad.
Here, we show that “Z. tertiaria” leafy branches and isolated leaves from Eocene Patagonia (Figs. 1–31), and a suite
of newly discovered, associated female and male reproductive
organs (Figs. 32–72), can all be assigned to a new fossil species of Agathis. Agathis is revealed as the dominant conifer of
Eocene Patagonian rainforests, where it presumably towered
over many of the same taxa that it associates with today in
Australasia and Southeast Asia and had equally great ecological importance.
MATERIALS AND METHODS
Laguna del Hunco and Río Pichileufú—The early Eocene Laguna del
Hunco flora (LH, ca. 52.2 mya) and the early middle Eocene Río Pichileufú flora
(RP, ca. 47.7 mya) come from northwestern Chubut and western Río Negro provinces, respectively, in northwestern Patagonia, Argentina. Locality information,
maps, and stratigraphic and geochronologic data have been given in several recent papers (e.g., Wilf et al., 2003; Wilf, 2012). These classic sites were first reported in the 1920s and 1930s (Berry, 1925, 1935a, b, c, 1938) and preserve
fossiliferous caldera-lake deposits within a regional volcanic province (Aragón
and Romero, 1984; Aragón and Mazzoni, 1997). Paleontological and geological
investigations at Laguna del Hunco and Río Pichileufú have increased greatly
over the past decade. As recently reviewed (Wilf et al., 2009; Wilf, 2012): the
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AMERICAN JOURNAL OF BOTANY
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Figs. 37–39. Agathis zamunerae sp. nov., cone scale with in situ seed, Laguna del Hunco. MPEF-Pb 6398, from LH13. The seed is preserved mostly
as a very thin sediment cast, with some dark organic material remaining in the seed body. The rounded, larger wing (extending to distal left in this view) is
broken near its apex. The rudimentary wing is clearly visible, extending to distal right (in this view) from the seed body. 37, 38. Standard image and
grayscale-inverted duplicate. 39. Composite of 84 images in 44 panels, each taken with very low-angle, unidirectional lighting to show fine-scale relief
features. In addition to the seed remains, note typical Agathis cone-scale features as detailed in next plate.
ages are well onstrained from recent 40Ar-39Ar analyses and supplemented at Laguna del Hunco by paleomagnetic data from a 170-m stratigraphic section; the
paleoenvironments were similar to those of Australasian subtropical and montane
tropical rainforests; the fossil compression floras and their insect damage are
among the most diverse known in the world; and a large number of novel insect
taxa are present, along with fish and other vertebrate fossils.
A striking biogeographic pattern emerging from recent systematic studies is
the Gondwanan signature from the numerous plant taxa that are found at Laguna del Hunco, or from both Laguna del Hunco and Río Pichileufú, that are
extant in Australasian rainforests and often extinct in South America. In addition, many of these elements are commonly associated with each other, and
with Agathis, in their extant ranges. The long and growing list of “southern
connection” examples from one or both of these floras, many of which constitute the only fossil occurrences of the respective taxon in South America, requires updating here.
Ferns include Todea (Osmundaceae; extant in New Zealand, Australia, New
Guinea, and southern Africa; Carvalho et al., 2013) and Dicksonia (Dicksoniaceae; Malesia, Australia, New Caledonia, New Zealand, South and Central
America; Berry, 1938; Carvalho et al., 2013). Broadleaved conifers, which collectively provide the most significant evidence for a rainforest environment
with a tall canopy, include Papuacedrus (Cupressaceae; New Guinea and Moluccas; Wilf et al., 2009); Araucaria section Eutacta (Australasia; Berry, 1938)
and Agathis reported here; and in the Podocarpaceae, Podocarpus (global, primarily Southern Hemisphere; Berry, 1938), Dacrycarpus (Australasia and
Southeast Asia; Florin, 1940a; Wilf, 2012), Acmopyle (Fiji and New Caledonia;
Florin, 1940b; Wilf, 2012), and an undescribed species of Retrophyllum (Fiji,
New Caledonia, Moluccas, Neotropics; Wilf, 2012). Basal (noneudicot) angiosperms include leaves of the primarily Gondwanan families Atherospermataceae and Monimiaceae that are most similar to the living Australian genera
Daphnandra and Wilkiea, respectively (Berry, 1935c; Knight and Wilf, 2013).
Eudicots include the iconically Australian Eucalyptus (Myrtaceae; Gandolfo
et al., 2011; Hermsen et al., 2012), thought to represent colonization of volcanically deforested areas adjacent to standing rainforest; Akania (Akaniaceae,
Australia; Romero and Hickey, 1976; Gandolfo et al., 1988); three species of
Gymnostoma (Casuarinaceae; Malesia, Australia, Southeast Asia; Zamaloa
et al., 2006); several Cunoniaceae, including fruits likely to represent Weinmannia (Andes, New Zealand, Malesia, Madagascar) and Ceratopetalum (Australia
and New Guinea; Gandolfo and Hermsen, 2012); and diverse Proteaceae, including Orites (Australia, South America; González et al., 2007). It is noteworthy that no genus currently endemic to the Americas has so far been verified at
Laguna del Hunco or Río Pichileufú. Several historical examples of endemics
have turned out, after systematic revision, to represent taxa now extinct in
South America (e.g., Austrocedrus/Libocedrus to Papuacedrus, Fitzroya to
Dacrycarpus, and here Zamia to Agathis).
Provenance and repositories—Material reported here mostly includes collections made during expeditions from Museo Paleontologico Egidio Feruglio
(MEF, Trelew, Chubut, Argentina): to Laguna del Hunco in 1999, 2002, 2004,
2006, and 2009, from quarries LH2, LH4, LH6, LH10, LH13, LH15, LH22,
LH23, LH25, and LH27, from float rocks, and from quarry AL-1, located 5 km
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WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
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Figs. 40–51. Agathis zamunerae sp. nov., additional cone scales. Note typical Agathis features: basal scallops, large seed-depressions, concave-upward, asymmetrical seed-detachment scars, rounded upper corners, and thickened to recurved distal margins. All from Laguna del Hunco except Figs. 50
and 51, from Río Pichileufú. 40, 41. Specimens showing prominent seed depressions, detachment scars, and recurved apices. MPEF-Pb 6393 and MPEFPb 6392b, respectively, both from LH6. 42, 43. Details of seed-detachment scars for specimens shown in Figs. 40 and 41, respectively. Note preserved
relief, admedially curving architecture below scar, and exmedially curving architecture above. 44. Detail of hooked left basal scallop of specimen shown
in Fig. 41. 45. Specimen with deep seed depression and adjacent-ovule impression at basal right (arrow). MPEF-Pb 6397, from LH15. 46, 47. Specimen
showing shallow left-basal kink and deep right-basal scallop (hooked tip broken). MPEF-Pb 6396, from LH13. 48. Specimen with deep seed depression.
MPEF-Pb 6394a, from LH13. 49. Small scale, presumably from near the base or apex of its cone. MPEF-Pb 6395b, from LH13. 50, 51. BAR 4752 and
BAR 4751, respectively, both from RP3.
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Figs. 52–61. Agathis zamunerae sp. nov., pollen cones. Note typical Agathis features: variably short to long peduncles, cluster of rounded, spoonshaped basal bracts, and peltate microsporophylls with thick stalks and rounded distal margins. Microsporophylls preserved in both external and lateral
view, often on the same cone (e.g., Fig. 54). 52, 53. Holotype of A. zamunerae, part and counterpart, MPEF-Pb 6399a and 6399b, respectively, from LH6
(also Figs. 62 and 70–72). Note quadrangular cross section of the long peduncle (Fig. 53) and one basal bract pulled down, showing its inner surface (also
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WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
south of the main section; and to Río Pichileufú in 2002 and 2005, from quarry
RP3 and near quarry RP1, all as described in earlier studies (Wilf et al., 2003,
2005, 2009; Gandolfo et al., 2011; Wilf, 2012). The Laguna del Hunco collections from these field seasons are curated at MEF (repository prefix MPEF-Pb),
and the Río Pichileufú specimens are curated at Museo de Paleontología de
Bariloche (BAR), San Carlos de Bariloche, Río Negro, Argentina; letter suffixes (a, b) indicate parts and counterparts. A few additional specimens from
Río Pichileufú were found in older collections at BAR. Also, we examined the
historical collections of “Zamia tertiaria” from Río Pichileufú (Berry, 1938)
that were collected and sent to Berry by J. R. Guiñazu, exact quarry sites unknown. This included previously uncited and unfigured cohort material as well
as the figured specimens, all housed at the National Museum of Natural History, Smithsonian Institution (USNM). The small type and cohort collections
from Laguna del Hunco (Berry, 1925), also located at USNM, consist entirely
of angiosperm remains and, thus, are not relevant to the present study. The total
collection presented here as protologue for a new species contains 154 elements: 1 twig, 36 leafy twigs, 86 isolated leaves, 1 immature seed cone, 10
seed-cone scales (1 of these with an in situ seed), and 20 pollen cones. Nearly
all the fertile material is from Laguna del Hunco, which has much better preservation, but we also found three cone scales at Río Pichileufú. The new species
is most common in the uppermost well-sampled level at LH (quarries LH6, 22,
25, and 27; 47% of total specimens).
Fossil preparation and imaging—Techniques, software, locations, and
equipment for fossil preparation, macro- and microphotography, epifluorescence microphotography, and image compositing and processing at MEF
and the Penn State University Paleobotany Laboratory are the same as those
reported in the recent, preceding paper on fossil conifers from these sites (Wilf,
2012), with the following minor technical notes. First, in addition to the PaleoAro and Micro-Jack #2 air scribes listed previously (Wilf, 2012), we also used
the more powerful ME-9100 for fossil preparation when needed (all from Paleotools, Brigham City, Utah, USA). Second, very low-angle, unidirectional light
was often used to bring out fine surface features, especially for pollen cones and
cone scales; image contrast was usually set high, and some image colors were
inverted (Figs. 35 and 38) to make important fine features of the fossils more
visible. Third, for some epifluorescence imaging of specimens that showed low
excitation response and required long exposures, a small amount of normal reflected light was sometimes allowed to mix into the exposure along with the
fluorescence, with good results that better showed surface textures in combination with the dimly fluorescing features (e.g., Fig. 8, “partial epifluorescence”).
All photographs are by P.W., except Figures 49–51 (I.H.E.). Field photographs in Borneo were taken on a Sony DSC-RX100 compact camera. Cuticle was usually coalified, with remnants of epidermal cells sometimes
visible under epifluorescence. Only two leaf specimens preserved traces of
stomatal apparati preserved as coalified Florin rings, some with guard-cell
casts (e.g., Figs. 30 and 31).
Extant material and characters—Herbarium collections of Agathis, comprising most of the living species, were examined by P.W. at the U.S. National
Herbarium, Smithsonian Institution, Washington, D.C. (US); the Australian
National Herbarium, Canberra (CANB); the National Herbarium of New South
Wales, Royal Botanic Gardens, Sydney (NSW); and Royal Botanic Gardens,
Kew (K). In addition, P.W. and R.M.K. examined wild Agathis trees extensively in the field, in the Atherton Tablelands region of Queensland, Australia,
in August 2010 (A. atropurpurea, A. microstachya, and A. robusta), and on and
around Mount Kinabalu in northern Borneo, Sabah, Malaysia, in September
2012 (A. borneensis, A. kinabaluensis, and A. lenticula). Collectively, the
authors have examined all living species of Araucariaceae in herbaria, in the
field, and/or in cultivation.
Although it is an easily recognized genus, the species-level taxonomy of Agathis remains contentious, as seen in the large number of disagreements among
the principal modern treatments (de Laubenfels, 1972, 1988; Whitmore, 1980b;
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Eckenwalder, 2009; Farjon, 2010). Moreover, even agreed-upon names can incorporate varying sets of synonymized taxa and reference specimens and, thus,
are not consistent in practical use. Here, we use Farjon’s (2010) treatment because of its relatively detailed coverage of reproductive morphology; unless otherwise noted, Farjon (2010) is the source of all nomenclature and measurements
of extant conifer species mentioned below. However, all descriptions and comments made in the principal treatments cited above were tabulated and also used
in the comparisons, if it was possible to adjust for synonymies. A general comparative summary of principal measurements and character states for the new
fossil species, and for the extant species as described by Farjon (2010), is given in
Table 1 (for additional comparisons, see Description and Discussion).
As would be expected from the unsettled species-level taxonomy and
generally poor genetic sampling of Agathis, there is no robust systematic
framework of all the species into which to place the fossils, and no phylogenetic analysis was attempted here. Numerous recent papers have produced
variable results for relationships within Agathis (e.g., Gilmore and Hill,
1997; Setoguchi et al., 1998; Stefanović et al., 1998; Conran et al., 2000;
Quinn et al., 2002; Stöckler et al., 2002; Rai et al., 2008; Liu et al., 2009;
Biffin et al., 2010; Leslie et al., 2012; Escapa and Catalano, 2013). Critically,
the living species that we found to have greatest morphological similarity to
the fossils (A. lenticula; see Discussion) has never been analyzed in a phylogenetic context with either morphological or molecular data. Thirteen (the
maximum to date) Agathis species were included in a recent molecular analysis as part of a large-scale study of all conifer groups (Leslie et al., 2012).
This showed Wollemia as sister to Agathis, Agathis australis of New Zealand
as sister to all other sampled Agathis species, a clade containing the New
Caledonian species, and a clade containing the three Australian species (A.
atropurpurea, A. microstachya, and A. robusta; Hyland, 1977) that is sister
to the remaining West Pacific-Asian tropical species. The distinct position of
A. australis and the consistency of the New Caledonian clade appear to be
robust in other studies (e.g., Escapa and Catalano, 2013), and the status of
Wollemia as sister to Agathis, and of both together as sister to Araucaria, is
the prevailing result from many molecular analyses (Gilmore and Hill, 1997;
Stefanović et al., 1998; Conran et al., 2000; Quinn et al., 2002; Rai et al.,
2008; Liu et al., 2009; Biffin et al., 2010; Escapa and Catalano, 2013). To
evaluate the phylogenetic position of this and other fossil species of Agathis,
the previously developed morphological matrix of Escapa and Catalano
(2013) needs to be expanded to include additional living species and detailed
characters of microsporophyll morphology.
SYSTEMATICS AND RESULTS
Family— Araucariaceae J. B. Henkel & W. Hochstetter, Synopsis der Nadelhölzer: xvii (1865), nom. cons.
Genus— Agathis R. A. Salisbury, Transactions of the Linnean Society of London 8: 311 (1807), nom. cons.
Species— Agathis zamunerae Wilf, sp. nov.
Coniferales, morphotypes TY010 “Zamia” tertiaria, “TY012
“Araucariaceae pollen cone” (part), and TY014 “Araucaria
wide cone scale” (Wilf et al., 2005: A6).
Zamia tertiaria Engelhardt, Geological Society of America
Special Paper 12: 57 (1938), cited Río Pichileufú material only.
Etymology— In memory of the life and work of Dra. Alba B.
Zamuner, 1959–2012, paleobotanist and valued colleague (see
Iglesias, 2013).
←
Fig. 62). Fig. 52 arrows: thin arrow corresponds to same in Figs. 70 and 71; thick arrow corresponds to same in Fig. 72. 54. Specimen with short peduncle
and exposed cone axis. MPEF-Pb 6403a, from LH13 (also Fig. 66). 55. Specimen with long peduncle and well-preserved bract cluster. MPEF-Pb 6402,
from LH13 (also Figs. 63–65). 56. MPEF-Pb 6409a, from LH25. 57. Specimen exhibiting cone axis and numerous individual microsporophylls in lateral
view, showing thick, reflexed stalks and peltate heads. MPEF-Pb 6405a, from LH15. 58. Specimen with short peduncle and exposed cone axis. MPEF-Pb
6408b, from LH25. 59. Specimen with tightly adpressed basal bracts and exposed cone axis. MPEF-Pb 6401b, from LH13. 60. Specimen with compressed
microsporophylls (dark, coaly areas) and underlying impressions exposed at right. MPEF-Pb 6406a, from LH25. 61. Elongate specimen with short peduncle and exposed cone axis. MPEF-Pb 6404, from LH15 (also Fig. 67).
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Figs. 62–72. Agathis zamunerae sp. nov., fine features of pollen cones and microsporophylls. Figs. 62–66, 68, 69, and 72 under epifluorescence. 62.
Base of the holotype (Fig. 52; also Figs. 70–72), showing resin ducts in peduncle, basal bract cluster with rightmost bract pulled down, and basal microsporophylls in lateral view. 63–65. Details of cone shown in Fig. 55. Fig. 63, basal bract cluster. Figs. 64 and 65, microsporophyll heads in external view;
note obscuration of the bases by neighboring heads and convexity, rounded apices, and lack of marginal denticulations. 66, 67. Cone axes in longitudinal
view. Fig. 66, set of closely spaced, longitudinally elongate depressions where microsporophyll stalks detached. Counterpart of cone shown in Fig. 54. Fig.
67, basal remnants on the axis where stalks broke near the base and did not detach cleanly, and departing attached stalks to left, from cone shown in Fig.
61. 68, 69. Cone (naturally) broken obliquely, showing microsporophyll stalks and heads in oblique-dorsal view, MPEF-Pb 6313, from LH13. Note large
resin ducts, thick stalks that expand distally, and (especially in Fig. 69) markedly convex, apically and basally recurved heads. 70–72. Details of microsporophylls and pollen sacs preserved in lateral view on right margin of the holotype (Figs. 52 and 62). Thin arrows indicate corresponding points in
Figs. 52, 70, and 71. Thick arrow in Fig. 72 corresponds to same in Fig. 52, in same relative orientation (image here rotated counterclockwise to fit the
layout). Fig. 70, set of sporophylls with light brown pollen sac clusters preserved abaxial to each stalk. Fig. 71, detail of expanding stalk termination with
adaxial ridge, striated surface, and abrupt insertion into the peltate head. Fig. 72, detail, set of elongate pollen sacs, abaxial and subparallel to the dark stalk
vertical at frame left. Note curving tip of the sac at lower right; the tip is lying free on the rock surface. Composite of 68 images in 9 panels.
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WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
Holotype— MPEF-Pb 6399 (Figs. 52, 53, 70–72), a pollen
cone part and counterpart from Laguna del Hunco, Tufolitas
Laguna del Hunco, early Eocene, Chubut Province, Argentina,
quarry LH6 of Wilf et al. (2003).
Paratypes— Laguna del Hunco, Tufolitas Laguna del Hunco,
early Eocene, Chubut Province, Argentina. Twig: MPEF-Pb
6301 (quarry LH13). Leafy twigs: MPEF-Pb 6302 (LH2);
6303–6306 (LH6); 6307 (LH10); 6308–6315 (LH13; 6313 also
with unattached pollen cone); 6316–6318 (LH22); 6319, 6422
(LH25); 6320–6323, 6423 (LH27); 6324 (float). Leaves (isolated): MPEF-Pb 6325 (AL1); 6326, 6327 (LH2); 6328–6330
(LH4); 6331 (level of LH4); 3160, 6332–6342, 6344–6348
(LH6); 6349 (LH10); 6350–6367 (LH13); 6368 (LH23); 6369–
6373 (LH25); 6374–6388, 6420, 6421 (LH27); 6389, 6390
(float). Seed cone: MPEF-Pb 6391 (LH27). Cone scales: MPEFPb 6392, 6393 (LH6); 6394–6396 (LH13); 6397 (LH15). Cone
scale with attached seed: MPEF-Pb 6398 (LH13). Pollen cones:
MPEF-Pb 6313 (LH13, on block with leafy twigs per above);
6400 (LH6); 6401–6403 (LH13); 6404, 6405 (LH15); 6406–
6409 (LH25); 6410–6417 (LH27).
Río Pichileufú, La Huitrera Formation, early middle Eocene,
Río Negro Province, Argentina. 1. Original, historical collection,
exact quarry sites unknown, figured material referred to “Zamia” tertiaria Engelhardt by Berry (1938). Leafy twigs: USNM
40378c, 40378d, 40378h (Berry 1938: pls. 8.2, 8.5, and 9, respectively). Leaves (isolated): USNM 40378e, 40378f, 40378g
(Berry 1938: pls. 8.1, 8.4, and 8.3, respectively). 2. Additional
cohort material from the historical collection, not previously
reported, identified as “Zamia tertiaria” on Berry’s handwritten
tags. Leafy twig(s): USNM 545227, 545230, 545235. Leaves
(isolated): USNM 545223–545226, 545228, 545229, 545231–
545234, 545236–545238. 3. Older BAR collections. Leafy
twig(s): BAR 288-20, 1214-20, 5002-20. Leaves (isolated):
BAR 1211-20, 1214-20. 4. Recent collections for current project. Leafy twigs: BAR 4748 (near RP1), 4749 (RP3). Leaf (isolated): BAR 4750. Cone scales: BAR 4751–4753.
Specific diagnosis—Leaves with consistently elliptic to lanceolate shape; long length (to ≥132 mm); and a generally high
length:width ratio (observed 3.9–11.5:1). Seed body ca. 12 ×
7 mm, and larger seed wing ca. 13 × 8 mm. Pollen cones with stout,
short to long peduncle (to ≥7.3 mm); relatively few basal bract
pairs (3 pairs observed), arranged in a tightly imbricate cluster with
width less than that of the cone body (sporophyll-bearing region)
and no elongated bracts; cylindrical to slightly convex cone body
with long length (to ≥56 mm); and imbricate microsporophylls
with head width ≤2 mm and entire distal head margins.
Description—Resin, preserved as amber, abundant in all organs. Twigs (Figs. 1–15) opposite, strongly grooved longitudinally, with quadrangular epidermal cells sometimes present (on
presumed green twigs in life) and obliquely exserted leaf-abscision
scars subtended by woody supply tissues that are long-decurrent
on the axis. Terminal bud conspicuously globose, with many
tightly imbricate bud scales. Leaves (Figs. 1–7, 9–11, and 15–31)
well separated along the twig, opposite to subopposite decussate,
deployed distichously via basal twisting of the narrow petiole.
Petioles elliptical in cross section (e.g., Fig. 24), width at base
1.2–4.2 mm (mean ± 1 SD = 2.3 ± 0.8 mm; N = 51), darkened in
distinct abscision zone. Blades symmetrical, elliptical to lanceolate, the widest portion occurring at 35–63% of the total blade
length (48 ± 6%, N = 52), the base and apex acute, the apex
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slightly rounded or blunted, never sharp-pointed, not acuminate
or falcate. Blade length 24.3–132.4 mm (66.7 ± 17.1 mm, N =
59), width 5.7–18.5 mm (10.6 ± 2.7 mm, N = 94), length:width
ratio 3.9–11.5:1 (6.6 ± 1.7, N = 53). Blade dimensions vary continuously among samples, such that no clear recognition of juvenile versus adult foliage is possible. Veins parallel, midvein
absent, course nearly straight and little influenced by margin curvature, and numerous, via dichotomies from the petiolar veins
(Fig. 22). Resin ducts alternate with the veins (Fig. 23; see Kausik,
1976). Stomata (Figs. 25–31) rarely preserved but numerous and
densely packed wherever observed, usually in two rows per vein,
randomly oriented (oblique, perpendicular, or parallel to the
veins), preserved as casts of guard cells and/or as coalifed Florin
ring compressions of maximum long-axis length ca. 65 μm. Amphistomy, variation in stomatal distribution or size along the leaf
length, and variation in the length or continuity of stomatal strips
(Kausik, 1976) could not be confidently discerned.
Immature seed cone (one specimen, Figs. 32–36) ovate,
length 34 mm, width 33 mm, terminal on a thickened branch
(width 21 mm) that has a prominent growth-increment scar.
Cone scales (ovuliferous bract-scales) helically arranged in the
cone, their apices upturned in smooth arcs, without spiny distal
projections. When preserved separately (Figs. 37–51), presumably as mature, dispersed units, cone scales as wide as or wider
than long, length 18.6–26.1 mm (22.9 ± 2.2 mm, N = 9), width
21.4–35.7 mm (27.7 ± 4.9 mm, N = 9), distal margins thickened
and upturned or recurved, the apex broad and slightly expanded,
with either an attached seed (Figs. 37–39) or with a narrow, elliptical seed depression and an asymmetrically curved, distally
concave seed-detachment scar (Figs. 40–43). An impression of
the adjacent ovule in the cone may be present (Fig. 45). Longitudinal architecture (fibers, resin ducts, vasculature) within the
seed depression area oriented more linearly than outside, converging slightly admedially into the detachment scar, then curving exmedially in the area distal to the scar (Figs. 42 and 43).
Cone-scale base scalloped (auriculate) on both sides where preserved, usually hooked to a sharp point on at least one side,
sometimes reduced to a kink on other side, the scallops incised
1.1–5.2 mm from the base and without frilly projections. Cone
scale upper corners rounded, the distal margin smooth, straight
to rounded, thickened to recurved, and with a slight, broad distal expansion in the center. Pollen tubes not preserved (see Kaur
and Bhatnagar, 1986). Seed (one specimen, Figs. 37–39) at center of the cone scale base, single, inverted, and ovoid, length ca.
11.8 mm, width ca. 7 mm, its long axis aligned to that of the
scale, its body protruding slightly below the scale basal margin,
with two opposite wings: one large and well-rounded apically,
directed at ca. 40° in relation to the left basal margin (in adaxial
view as preserved and shown), length ca. 13.4 mm, and one small,
rudimentary, length ca. 3 mm, with an acute, pointed apex.
Pollen cones (Figs. 52–72) cylindrical to slightly convexsided, inserted on a stout peduncle, with subtending bract
clusters, apex smoothly curved. Peduncles short to long,
straight-sided to semiconical, rounded to quadrangular (Fig.
53) in cross section, expanding distally to the approximate
width of the cone bracts, distally concave upward. Peduncle
length 2.2–7.3 mm (4.3 ± 1.6 mm, N = 7), minimum width 1.0–
3.5 mm (2.8 ± 0.8 mm, N = 8), maximum width 4.1–6.8 mm
(5.6 ± 0.8 mm, N = 13). Cone length, including bracts but not peduncle, 23–56 mm (40.0 ± 9.5 mm, N = 10), diameter 6.6–10.8
mm (7.7 ± 1.2 mm, N = 16). Bracts tightly imbricate, apparently
consistently in three pairs, ovate, apices rounded, forming a
cluster 4.7–8.4 mm wide (6.1 ± 1.0 mm, N = 13) that is 68–97%
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Figs. 73–81. Extant Agathis, selected features of dried material for comparison to fossils. All except Fig. 77 are litter samples of a cultivated A. robusta, Myocum, New South Wales, Australia. Figs. 76 and 80 under epifluorescence. 73. Twigs with terminal buds of varying sizes. Note marked longitudinal striations, prominently and obliquely raised abscision scars with decurrent supporting tissue, and scaly, rounded buds. Compare Figs. 1–15. 74. Detail
of a large terminal bud, showing numerous overlapping scales and crowded, subtending abscision scars. Compare Fig. 8. 75, 76. Twig closeup showing
longitudinal ridges and grooves and quadrangular epidermal cells. Compare Figs. 12 and 13. 77. Seed-cone base, Agathis macrophylla (Aneityum Island,
Vanuatu, S.F. Kajewski 760, US Fruit Collection 325). Note thickened fertile branch and large growth-increment scar subtending the cone, and imbricate,
upturned scale tips with rounded, convex-upward margins. Compare Figs. 32–36. 78. Distal left corner (in adaxial view) of seed-abscision area of a cone
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WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
the width of the sporophyll-bearing region of the cone (80.3 ±
9.3%, N = 12) and is fully constrained below the first microsporophylls, with no elongate or leaflike basal bracts present. Bract length 2.4–4.7 mm (3.5 ± 0.5 mm, N = 8), width
2.3–3.5 mm (2.8 ± 0.5 mm, N = 7). Microsporophylls (Figs.
67–72) imbricate, peltate, numerous (ca. 250–500 cone–1), helically arranged. Stalks striated and with an adaxial median ridge,
reflexed basally to accommodate mass of the head and pollen sacs,
where detached leaving irregular pits (if cleanly detached, Fig. 66)
or basal remnants (Fig. 67) on the cone axis. Stalk length 1.9–2.9
mm (2.4 ± 0.4 mm, largest values from 11 cones), stalk plus head
total length 2.4–3.7 mm (3.0 ± 0.5, from 11 cones). Stalk and its
median ridge expand distally (Figs. 69–71), before their peltate
insertion into most of the microsporophyll head. Heads (Figs. 64,
65, and 68–71) abruptly angled from the stalks, then strongly recurved apically and deeply basally, outwardly markedly convex,
the shape ovate, the margin and apex smoothly rounded and without angled tips, notches, serrations, or denticulations. In external
view (e.g., Figs. 64 and 65), the basal margins of the heads are
obscured by imbrication. Head height in external view 1.5–2.1 mm
(1.7 ± 0.2 mm, from 12 cones), width 1.3–2.0 mm (1.6 ± 0.3 mm,
from 13 cones). Pollen sacs (Figs. 70 and 72) apparently immature
where observed, attached to the inner abaxial portion of the microsporophyll head, preserved as light brown patches, each containing several narrow, elongate sacs, the sac outlines subparallel
to the microsporophyll stalks; number of sacs could not be determined with confidence; pollen not preserved.
Remarks— We designate a pollen cone as the holotype for
the new species because it is well recognized that pollen cones
are the only organs of the genus Agathis that have relatively
abundant and distinctive characters at species level, once the
generic diagnosis is made from all available material (e.g.,
Whitmore, 1980b; Farjon, 2010). The holotype was collected 6
December 2002 (by P.W., K.R.J., and crew). We refer all the
cited fossil-plant organs to a single species because there is no
evidence that more than one taxon is definably present. There
are also no differences yet apparent among samples from the
two sites (L.H. and R.P.), despite intensive sampling of their
bulk floras. Moreover, each organ type recovered is independently assignable to Agathis using most of the standard botanical characters for the genus (see Familial and generic affinities)
and exhibits a self-consistent set of features and dimensions,
and the various organs are all found very closely associated on
single bedding surfaces. The certain attachments include the 36
specimens of twigs with attached leaves (e.g., Figs. 1–7) and
one seed in place on a cone scale (Figs. 37–39).
DISCUSSION
The Zamia tertiaria problem—“Zamia” tertiaria Engelhardt
(1891:646 and pl. 2 [Fig. 16]) is based on the single, holotype
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foliage specimen from the Eocene of Coronel, Chile, which is
now apparently lost, along with most other material from Engelhardt’s important 1891 monograph (Wilf, 2012). Engelhardt’s
drawing shows a parallel-veined leaf or leaflet with curved margins and no clear base or apex. Engelhardt further described this
foliage as pinnate, leathery, and sessile, without illustration of
these traits. Little can be said here to affirm or reject the identification to Zamia, especially with the holotype unavailable.
Thus, Engelhardt’s “Z.” tertiaria from Chile cannot be linked in
any meaningful way to the specimens described here from Argentina, nor to Agathis.
Much later, Berry (1922:120 and pl. 1 [Fig. 4], pl. 2 [Figs.
1–3]) assigned several Eocene foliar specimens that he collected from Arauco Mine, Curanilahue, Chile, to “Z.” tertiaria
Engelhardt. He also claimed that several specimens, including
one figured specimen (his pl. 1 [Fig. 4]), showed attachment to
a rachis “imbedded in the matrix.” Berry’s figured specimens
survive (USNM 320640–43, not shown), and on examination
they are somewhat different from his drawings and show typical monocot features, including at least two orders of parallel
veins (i.e., A and B veins sensu Hickey and Peterson (1978),
and distinct plications along the A veins, best seen in USNM
320643). There is no evidence of attachment to a rachis.
Berry (1922) also assigned to “Z. tertiaria” a second specimen from Engelhardt’s monograph that Engelhardt (1891: pl. 1
[Fig. 4]) had identified as a monocot leaf fossil (“Monokotyler
Blattrest”). On the basis of Engelhardt’s illustration, the only
information available, this specimen was quite different from
the “Z.” tertiaria holotype, and in fact very monocot-like, in
having many more parallel veins, numerous cross veins, and a
much more elongate, strap-shaped aspect. It is possible that Engelhardt’s “Monokotyler Blattrest” was indeed related to the
material from Arauco that Berry assigned to “Z. tertiaria,” but
not in the way Berry thought (all monocots, vs. all cycads per
Berry).
In any case, Berry’s (1922) “Zamia tertiaria” specimens
show no affinity to Engelhardt’s (1891) “Zamia” tertiaria, as
suggested long ago by Hollick (1932), nor to conifers. However, of historical note, Hollick (1932:177) explicitly noted a
general similarity of Berry’s (1922) specimens (probable monocots) to Agathis.
Subsequently, Berry (1938) referred specimens from Río
Pichileufú to “Zamia” tertiaria Engelhardt (e.g., Figs. 1, 2, and
17; see also Familial and generic affinities), and these, including Berry’s previously unreported cohort material, are the only
historical specimens of “Zamia” tertiaria that are reassigned
here to Agathis zamunerae. Berry’s Río Pichileufú material is
quite distinct from all the Chilean entities discussed above, excepting perhaps the lost, fragmentary holotype of “Z.” tertiaria.
Even if this specimen were found and determined to have features of Agathis, it would still lack the large suite of characters,
including those of leaf attachment and female and male reproductive organs, that is preserved in A. zamunerae. In summary,
←
scale. Note strong relief, incurved architecture immediately basal to the scar, and outwardly curved architecture immediately distal to the scar. Compare
Figs. 42 and 43. 79–81. Pollen cone with upward-facing microsporophylls removed manually, remaining microsporophylls in approximate lateral view as
in several of the fossils. Fig. 79 shows large pits on the cone axis where the enlarged microsporophyll bases had inserted and from which they detached
completely (cf. Fig. 66), as well as some remnants where the stalks broke off near the base (cf. Fig. 67). Epifluorescence in Fig. 80 clearly distinguishes
tissues of the stalks (note striations and adaxial ridges as in the fossils), the abaxial pollen sacs, and the peltate, convex, apically and deeply basally recurved
heads (cf. Figs. 69–72). Fig. 81, Single microsporophyll (compare Figs. 69–72). Note enlarged base, prominent, distally enlarged adaxial ridge, and the
distinct tissues of the head and the pollen sacs, which have dehisced, in contrast to those in the fossils (Fig. 72).
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[Vol. 101
Figs. 82–88. Agathis lenticula in Kinabalu National Park and environs, Sabah, Malaysian Borneo, September 2012. 82. Large emergent tree, lower
Mesilau Trail. 83. Young shoot, lower Mesilau Trail, showing typical Agathis features: green twig, opposite-decussate leaf attachment, distichous leaf deployment via basal twisting of petioles, parallel venation, and rounded terminal bud. Compare, e.g., Figs. 1–7. The lens-shaped juvenile leaves are typical
for this living species (and not the fossils). 84. Litter sample from below large tree, bank of Mesilau River. Note raised, opposite-decussate abscision scars
on twigs with decurrent supporting tissues (compare Figs. 11, 14, and 15), petioles with abscision scars on the leaves (compare Figs. 16–21 and 24), and
pollen cone fragments. 85. Litter sample of pollen cones, from large tree below Kiau View trailhead. Note numerous similarities to the fossils: tightly adpressed basal bracts with width less than that of the full cone, variably short to long and quadrangular (second from left) peduncles, cylindrical to convex
cone shape, and imbricate, convex microsporophyll heads (compare Figs. 52–72). Each small scale tick = 1 mm. 86, 87. Cone scales in litter below large
tree, Mempening Trail, with (Fig. 86) and without (Fig. 87) the seed still in place. Note typical Agathis features: hooked basal scallops, rounded apical
January 2014]
WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
“Zamia” tertiaria Engelhardt is an unsuitable basionym for the
Agathis fossils reported here, thus requiring the new species.
Of additional historical interest, Petersen (1946:49), referring to
Berry (1938), made the first record of “Zamia tertiaria” Engelhardt
at Laguna del Hunco as part of his outstanding geological survey
of the middle Chubut River region. Although Petersen’s collections are apparently lost, it is reasonable to infer that his identification (sensu Berry, 1938) was probably correct, and therefore that
Petersen was the first scientist known to collect what is here designated as Agathis zamunerae, at its type locality.
Familial and generic affinities— Each of the preserved organs of the new species displays a large number of distinctive
features that, in combination and often singly, are only found in
Agathis. These characters include most of those used by botanists to identify living Agathis and its species. Pending confirmation from a phylogenetic analysis, which would require
much more data from the extant species, we conclude from the
wealth of preserved morphological data that Agathis zamunerae
sp. nov. is, in all probability, closely related to the living species
of Agathis and belongs at least in the crown of the genus, and
perhaps in a derived position therein. A selection of comparative details from extant live, litter, and dried material is shown
in Figures 73–87.
Beginning with vegetative features: conspicuously grooved,
stout “green” twigs with globose, scaly terminal buds, bearing
opposite to subopposite, decussate, distichously deployed, simple, symmetrical, well-separated, multiveined, straight-veined
leaves with narrow petioles, a blunt apex, and randomly oriented stomata with Florin rings, are, collectively, firmly diagnostic of Agathis. Wollemia and some Araucaria species also
have multiveined leaves, but these are sessile (and decurrent in
Wollemia), overlap densely along the twig, lack conspicuous
Florin rings, and have more longitudinally oriented stomata in
most species (Florin, 1931; Cookson and Duigan, 1951; Stockey
and Taylor, 1981; Stockey, 1982; Bigwood and Hill, 1985;
Stockey and Atkinson, 1993; Chambers et al., 1998; Burrows
and Bullock, 1999; Hill et al., 2008; Pole, 2008; Escapa and
Catalano, 2013). Araucaria foliage is helically arranged, not
decussate nor distichously deployed, and nearly always with
a sharp apex; Wollemia leaves are distichous to four-ranked
and trimorphic. Araucaria pichileufensis Berry (1938) foliage,
which occurs abundantly at the same fossil localities at Laguna
del Hunco and Río Pichileufú, is easily recognized as distinct
from Agathis zamunerae in having the typically narrow, short,
single-veined, imbricate, helically deployed leaves of Araucaria Section Eutacta.
Outside Araucariaceae, the only living genus with vegetative
features similar to Agathis (including A. zamunerae), especially
in often having opposite–subopposite, elliptic, well-spaced,
petiolate, multiveined leaves, is Nageia (Podocarpaceae). However, this genus has a completely different, podocarpaceous-type,
173
acute terminal bud and veins that much more noticeably curve
with the margin and recurve toward the apex; both these features are used to distinguish living Nageia from Agathis where
they co-occur (Sterling, 1958; de Laubenfels, 1988; Beaman
and Beaman, 1993). In addition, Nageia, like most podocarps and
unlike A. zamunerae, has longitudinally oriented stomata (Florin,
1931; Hill and Pole, 1992). We note that broad, multiveined
conifer leaves that are generally similar to our vegetative fossils
are abundant throughout the Mesozoic and early Cenozoic and
attributed to various conifer lineages (e.g., Heidiphyllum, Nageiopsis, Podozamites, Araucarioides (see Axsmith et al., 1998;
Hill et al., 2008; Miller and Hickey, 2010), but the full combination of leaf and twig features preserved here is characteristic
only of Agathis.
Although the new material cited here from Río Pichileufú shows
abundant Agathis twig and leaf features and includes associated
cone scales (Figs. 50 and 51), it would be difficult to fully refute
Berry’s (1938) assignment of his original suite of vegetative specimens from that site, considered alone, to Zamia without the strong
corroboration from these new fossils. There are indeed many relevant similarities between some Zamia leaves and Agathis leafy
branches, including grooved twigs/rachises, petioles/narrow leaflet
bases, leaf(let) articulation and/or abscision, elongate and narrow
leaves/leaflets, and parallel venation. However, even Berry’s
specimens show features not found in Zamia, nor any cycads to
our knowledge: the twigs are notably bumpy and include expanded support tissue under the obliquely raised abscision zones
(e.g., Figs. 1, 2, and 10); leaf attachment is decussate (e.g., Fig. 2);
and the leaves have copious resin and thick abscision zones that
would be very unlikely in Zamia (Figs. 17 and 23).
The Zamia problem aside, special care must be taken when
identifying foliage with parallel venation at the two fossil sites,
because of the presence of monocots and because of two other
parallel-veined gymnosperm taxa, which, along with the conifers listed earlier (see Materials and Methods), complete the
gymnosperm flora so far known. First, Ginkgo patagonica
Berry (1935b) can quickly be distinguished from Agathis because it is palmately lobed and is usually preserved with thick,
abundant cuticle unlike any Agathis studied here; however, the
lobe tips can be confused with Agathis if found isolated and
without cuticle. Second, we have recently found fossils of a true
cycad at Laguna del Hunco (Wilf et al., 2003: fig. 1I). These
have petiolulate, long leaflets with parallel venation that are
much like Agathis, but the leaflets are toothed with decurrent
bases and lack articulations or abscision zones. Preliminary indications are that this cycad closely resembles the African genus Encephalartos (P. Wilf, unpublished data).
The female reproductive features described here are also stereotypical for Agathis. As in all Araucariaceae, the cone (Figs. 32–36),
though not well preserved, arises on a thickened branch, is large
and rounded (here subround due to presumed immaturity), and
has flattened, densely and helically arranged cone scales with
←
corners, and thickened, recurved, nonprojecting apex of the scale; large, ovoid seed body and corresponding depression in the scale; lateral impressions of
adjacent seed bodies; presence of one enlarged, broadly curved wing extending at an angle distally and to right (in this view) and one rudimentary wing to
left (individual cones may be “right-handed” or “left-handed;” this does not appear to have taxonomic significance), and corresponding impressions and
discoloration of the scale; and small, curved seed-abscision zone. Compare Figs. 37–51. 88. A large area east of the park’s Mesilau entrance that was recently degazetted, deforested, and planted for a cabbage monoculture, requiring intensive pesticide use. The cleared landscape is dense with large stumps.
Remaining intact, primary montane rainforest of the main body of the park, containing numerous, large Agathis lenticula and Dacrycarpus kinabaluensis
in this area, is in the background. The current park boundary is several tens of meters behind the forest line visible on the green slopes. Inset, stump of a
felled Agathis from this unprotected strip and its exuded copal.
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AMERICAN JOURNAL OF BOTANY
upturned tips. However, the large, prominently visible growthincrement scar subtending the fossil cone (see Fig. 77), the lack
of well-developed subtending foliage (or any foliage in this
case), and the lack of spinose or elongate cone-scale tips are
collectively typical for Agathis and not for Araucaria or Wollemia (de Laubenfels, 1972; Jones et al., 1995).
An important feature of Agathis cone scales that is easily
seen in the isolated fossil scales is the marked basal scallops
(e.g., Figs. 44, 47, 86, and 87), which function in life to provide
accommodation space for the seeds of adjacent scales within
the tightly packed seed cone. These are not present in Araucaria and, likewise, are not seen in the cone scales of the cooccurring A. pichileufensis. Wollemia cone scales have basal
embayments, but these are broader than in Agathis, and the
overall scale shape is markedly rhombic, unlike in Agathis and
the fossils. Further, as just mentioned, the cone scales of Araucaria, including A. pichileufensis, and Wollemia typically have
triangular to spinose, projecting tips (especially in Wollemia;
Jones et al., 1995) that comprise the ovuliferous scale portion
that is free of the bract, whereas in Agathis (excepting A. australis) and the fossils, there is consistently no apical projection,
or only a very broad, blunt expansion (e.g., Fig. 40), and the bract
and scale components appear to be fully fused. We also note
that Dettmann et al. (2012: table 2) reviewed the best-preserved
fossil seed-cone taxa of Araucariaceae, all of them Mesozoic,
and none of these has scalloped (“auriculate”) cone scale bases
as in Agathis, nor petiolate, opposite associated leaves.
All Araucariaceae have a single, inverted seed per cone scale,
as in the fossils. However, the seeds of Agathis and its sister
Wollemia are adpressed but attached to the scale only by a weak
stalk from which they are usually, though not always, shed,
leaving on the scale a characteristic, rhomboidal (Wollemia) or
asymmetrical curved (Agathis and fossils) abscision scar and a
marked, longitudinally grooved seed depression, as seen in the
fossils (e.g., Figs. 40–43, 45, 46, and 48; Owens et al., 1997;
Chambers et al., 1998; Dettmann et al., 2012). In Araucaria,
including A. pichileufensis from the same fossil localities, the
seed is embedded in the tissues of the cone scale. The fossil
seed in situ on its cone scale (Figs. 37–39), preserved extremely
fortuitously and mostly as a very thin sediment cast, clearly
shows typical Agathis positioning and morphology, including an ovoid body that projects slightly below the scale base,
a concave-upward detachment area, and two, strongly asymmetrical wings, this asymmetry being a recognized synapomorphy for the genus (Escapa and Catalano, 2013). Wollemia
has a single, relatively narrow wing that surrounds its seed
and does not resemble the fossil. We note for general interest
that DiMichele et al. (2001) reported an Early Permian gymnosperm seed with unequal wings that looks surprisingly
similar to Agathis, although the wing architecture is quite
different.
The fossil pollen cones exhibit several features that are distinctive for Agathis. Most notably, the peduncle is well defined
and can be elongate, and the basal bracts are broad, smoothly
rounded, and contained below the lowest microsporophylls
(e.g., Figs. 53–55, 62, 63, and 85). These features are typical for
living Agathis when present, although some species can have
sessile pollen cones (A. montana, and sometimes A. dammara,
A. macrophylla, A. microstachya, and A. silbae) or can produce
a single, extended, leaflike lower bract pair (A. australis and A.
kinabaluensis). In Araucaria, the pollen cones are usually sessile or have a very short, never elongate peduncle, and the basal
bracts, like the foliage leaves, are more numerous and much
[Vol. 101
more narrow and sharp-pointed, extending well above the lowest microsporophylls (Cookson and Duigan, 1951; de Laubenfels, 1972, 1988; Barrett, 1998; Hill, 1998; Farjon, 2010).
Araucaria pollen-cone size can also be much greater (≤25 cm
in length) than in Agathis (≤9 cm), and the fossils (≤5.6 cm).
Wollemia pollen cones are sessile and also range above Agathis
in size (≤12.5 cm in length); the basal bracts are small, triangular to semirounded, and sharp-pointed and extend onto the
basal microsporophylls (Hill, 1998; Eckenwalder, 2009; Farjon,
2010). Wollemia pollen cones are also shed without the bracts,
which therefore would not be seen in isolated fossil cones as
described here, and they easily disaggregate on drying (as also
observed in Araucaria bidwillii), such that the microsporophylls
break and leave the cone axis covered in their stubs (Chambers
et al., 1998). This situation is unlike that reported for Agathis
robusta (Chambers et al., 1998), whose microsporophylls remained intact when separated from the axis of the dried cone
axis and left behind “footprint” depressions that appear to be
similar to those in some of the fossils (Fig. 66). However, other
fossils show broken remnants of the stalk bases rather than pits
(Fig. 67). Likewise, when we tried this experiment, also on
dried pollen cones of A. robusta (Fig. 79), mostly pits but some
base remnants resulted, corresponding to intact (Fig. 81) and
“footless” detached microsporophylls, respectively.
Peltate microsporophylls, as seen in the fossils (Figs. 57 and
68–72), are typical for Araucariaceae (Gilmore and Hill, 1997).
Agathis microsporophylls (in species where these are imbricate;
Fig. 81), like those of the fossils, have rounded apices and a
thick, long stalk. Unlike the fossils, Araucaria microsporophylls tend to have more pointed, acute apices and a relatively
thin, weak, stalk, and Wollemia microsporophylls have very
short stalks and thickened, shield-shaped heads with large, angular surface projections (Cookson and Duigan, 1951; Jones et al.,
1995; Hill, 1998; Eckenwalder, 2009; Farjon, 2010). Epifluorescent imaging of an A. robusta pollen cone, with microsporophylls in lateral view (Fig. 80), very clearly distinguishes the
tissues of the stalk and its expanding median ridge, the apically
and deeply basally recurved head, and the abaxial pollen sacs
under the basal portion of the recurved head. The same distinctions can be seen in the fossils (Figs. 69–72).
Consistent with the observations above, a separate araucariaceous pollen cone morphotype from Laguna del Hunco (exemplar specimen LH13–1135 mentioned by Wilf et al., 2005),
under separate study, is larger than the fossils described here
and has a very short peduncle, numerous narrow, long, sharppointed, mucronate basal bracts that extend onto the basal microsporophylls, and large, triangular microsporophyll heads
with acute to acuminate apices. This morphotype is the probable pollen cone of the Araucaria pichileufensis plant.
Comparisons to extant species— Agathis zamunerae is the
first fossil Agathis to be so completely preserved as to allow
detailed comparisons to living species, using most of the typical
botanical characters (Table 1). The following combined character states of Agathis zamunerae, and those of the pollen cones
alone, are unlike any other Agathis species (also see Specific
diagnosis): leaves with consistently elliptic to lanceolate shape,
long length, and generally high length:width ratio; unique combination of seed and wing dimensions; and pollen cones with
cylindrical or slightly convex shape, long length, and stout,
long, peduncle, relatively few (3) basal bract pairs forming a
tightly imbricate cluster with width less than that of the cone
body and no elongate basal bracts, and imbricate microsporophylls
January 2014]
WILF ET AL.—EOCENE AGATHIS FROM SOUTH AMERICA
with head width ≤2 mm and entire head margins. Without a
phylogenetic context for the genus, it is problematic to evaluate
the importance and polarity of the various characters. However,
overall, and especially when considering pollen cone characters, Agathis lenticula (Figs. 82–88) emerges as the living species with the greatest morphological similarity to the fossils,
though with several differences (Table 1). This species has not
been considered in the limited phylogenetic analyses done so
far for Agathis, and correcting this omission would have obvious importance for evaluating the phylogenetic position of A.
zamunerae, as well as for the conservation of A. lenticula.
In A. lenticula, the pollen cones (Fig. 85) are somewhat
shorter than the longest fossil cones but otherwise broadly consistent in cylindrical shape (of mature cones), length and stoutness of the peduncle, number and imbrication of bracts, and
microsporophyll height, width, and imbrication. However, A.
lenticula microsporophylls are noticeably denticulate at the
apex, versus entire in the fossils. This difference could be preservational, but the denticulations we have observed in the living
species are large enough to be easily seen with a 10× hand lens,
and similar structures should be visible in our best-preserved
fossils (e.g., Figs. 65 and 71). The seed-cone scales of A. lenticula are consistent with the fossils in size and general shape.
The namesake lens-shaped juvenile leaves of A. lenticula (Figs.
83 and 84) were not seen in the fossils.
Agathis moorei shows some morphological overlap with the
fossils, but its pollen cones have important dissimilarities, and in
general its corresponding organs range much larger in size. Pollen cones of A. moorei are consistent with the fossils in cylindrical shape, peduncle length (although this can be significantly
longer than in the fossils), imbrication of bracts and microsporophylls, and height and width of microsporophyll heads, although
the width can be much greater. However, compared with the fossils, A. moorei pollen cones arise from more slender peduncles,
do not become so long, have 4–8 pairs of bracts (vs. three pairs in
the fossils), and have relatively flattened microsporophyll heads
with denticulate distal margins, compared to convex heads with
entire margins in the fossils. The seed-cone scales are also similar
to the fossils, but again they tend to be larger, especially in length.
Leaf shape is more variable than in the fossils, and leaf size can
be similar or much larger.
Agathis macrophylla pollen cones are comparable with the
fossils in cylindrical shape, peduncle stoutness and length, the
imbrication of basal bracts, and the imbrication, height, and
width of microsporophylls. However, in A. macrophylla, the
attachment of the microsporophyll stalk is not peltate but to the
abaxial edge of the head, and the microsporophyll apex is denticulate and can be notched. According to Farjon (2010; Table
1), there are four bract pairs, and the cone does not become so
long as in the fossils, whereas Eckenwalder (2009) reported
3–4 bract pairs and cone length that rarely reaches that of the
fossils. Seed-cone scales of A. macrophylla are generally larger
than in the fossils. Leaf shape is not usually elliptic in A. macrophylla and, consistent with the name, leaf length and width
can be significantly larger than in A. zamunerae.
Agathis robusta has pollen cones with several dissimilarities
from those of A. zamunerae, despite the similar long-cylindrical
aspect in both species, most notably: in A. robusta the peduncle can
be much longer, there are usually more bract pairs and these are
often distinctly less imbricate, and the microsporophylls are often
tessellate or only weakly imbricate. Also, cone scales of A. robusta
are usually larger than in the fossils. These living and fossil species
are most similar to each other in leaf size and shape.
175
Agathis australis of New Zealand, of general interest because
it emerges as the sister of all the remaining species in most molecular phylogenies, and because its history in New Zealand is
frequently debated (see General remarks), has many important
morphological differences from A. zamunerae. Many of these
are smaller dimensions of the organs (Table 1), but additional
differences from the fossils are that A. australis has: pollencone peduncles that can be much longer; pollen-cone bract
clusters loosely arranged and extending past the width of the
cone, often with subtending, leaflike, long bracts; microsporophyll heads wider; seed-cone scales with very distinct narrow,
triangular, mucronate apical projections; (adult) leaves often
with a truncate apex and longitudinally oriented stomata; and
seed-wings with a square shape. These numerous differences
from A. australis support the idea that A. zamunerae occupies a
derived position within the genus.
Agathis dammara resembles and is often considered conspecific with A. lenticula (Whitmore, 1980b; Eckenwalder, 2009).
In A. dammara, the basal bracts of pollen cones can be more
numerous (2–4 pairs) than in A. lenticula (2–3) and the fossils
(3) and are spreading rather than imbricate. Other differences
from the fossils are mostly dimensional (e.g., A. dammara has
shorter pollen cones and peduncles, and larger seed-cone
scales). The microsporophylls of A. dammara, A. lenticula, and
A. zamunerae are very similar, except that microsporophyll
height in A. dammara is distinctly lower than in the other two
species, and in both the living species the apical margins are
denticulate, versus entire in the fossils.
Finally, A. borneensis is another species with some general similarities to the fossils, mostly in the leaves, but its
pollen cones are very different. They are not strongly cylindrical and can be globose when immature, but most notably,
the pollen cones and microsporophylls become dramatically
larger than those of the fossils or of any other living Agathis
species.
Remarks on Agathis lenticula— Agathis lenticula (Figs.
82–88) may possess special evolutionary and biogeographic
importance for the genus, given its similarity to the fossil species A. zamunerae. Agathis lenticula is a large tree (≤45 m) that
is endemic to the lower montane forests of northern Borneo
(Malaysia; de Laubenfels, 1979; Yii, 1995). The Kinabalu Park
Headquarters Meteorological Station (1680 m), around which
A. lenticula is abundant, has a mean monthly temperature of ca.
20°C, with an annual range of 14.4–22.2°C, and annual precipitation of 2000–3800 mm, including drought years (Kitayama,
1992). Where it is still protected, we found the species to be
common and often dominant, for example along the lower
reaches of the Mesilau trail, in the eastern portion of Kinabalu
National Park (P. Wilf and R. M. Kooyman, personal observation). This species is considered Vulnerable and suffers ongoing losses within its limited range (Fig. 88) that are not well
documented because loggers do not discriminate it from A.
borneensis (Beaman and Beaman, 1993; Farjon et al., 1993;
Farjon, 2010; IUCN, 2013).
We note that Whitmore (1980b) and Eckenwalder (2009) did
not recognize A. lenticula as distinct from the more widespread
A. dammara, which if incorrect would be very likely to have
negative conservation effects on A. lenticula. In our experience,
the characters of A. lenticula are reliably distinct from A. dammara as originally proposed (de Laubenfels, 1979; Farjon,
2010), and we recommend that the species be managed in that
context.
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It is remarkable that Mt. Kinabalu alone has three species of Agathis (A. borneensis, A. lenticula, and A. kinabaluensis ) and that these form part of a diverse and entirely
Gondwanan conifer assemblage that also has six genera and
16 species of Podocarpaceae, along with their close relative Phyllocladus hypophyllus (Beaman and Beaman, 1993,
1998). Including A. orbicula, Borneo as a whole has four
species of Agathis, equal to New Caledonia (Table 1). Also
striking is that one of the tall podocarps that frequently cooccurs with Agathis lenticula, Dacrycarpus imbricatus, is
extremely similar to D. puertae from Laguna del Hunco and
Río Pichileufú (Wilf, 2012) at ca. 16 000 km modern distance, further illustrating the vast temporal and geographic
reach of a Gondwanan association surviving in an Asian
rainforest.
General comments— The evidence from Agathis zamunerae,
including the strong possibility that it represents a derived lineage, suggests that modern-aspect Agathis not only occupied a
vast land area by the early Eocene but was already well diversified. As for Eucalyptus and many other taxa (see Materials and
Methods), Eocene Agathis fossils from Patagonia show that
Australia can no longer be assumed to be the area of origin for
the genus. Agathis evolved in and became a dominant element
of the extensive southern rainforest biome of the Eocene, and in
all likelihood it once inhabited Antarctica, which had very
warm temperatures at this time (Pross et al., 2012), along with
Australia and South America. Agathis was probably restricted
primarily to rainforest environments throughout its history,
partly because it possesses accessory xylem tissues parallel to
the leaf veins (Kausik, 1976) that are likely to collapse during
drought (Brodribb and Holbrook, 2005; these run adjacent to
the veins and could not be distinguished in the compression
fossils).
There is a vigorous debate concerning the origins of Agathis
in New Zealand and, along with many other components of the
New Zealand biota, regarding its possible survival there through
a proposed interval of partial or complete submergence during
the Oligocene (Cooper and Millener, 1993; Stöckler et al.,
2002; Waters and Craw, 2006; Knapp et al., 2007; Lee et al.,
2007; Biffin et al., 2010; Crisp and Cook, 2011; Sharma and
Wheeler, 2013). Our results show, first, that modern-aspect Agathis was present long before the Oligocene, over a vast area of
Gondwana before its final breakup. Thus, putative survival in
situ was possible in that the genus had certainly evolved by that
time, but whether Agathis was really in New Zealand during the
Oligocene is not fully understood despite many possible fossils
(Pole, 2008). Second, the large past distribution of Agathis revealed here shows that many areas of Gondwana, not just Australia (as thought based on the previous fossil record), could
have been the source for New Zealand in a dispersal scenario.
This situation is similar to that of New Zealand’s endemic tuatara lizard (Sphenodon), for which there is a global record of
related fossil forms during the Jurassic, and now an especially
tuatara-like fossil is known from the Campanian–Maastrichtian
of Patagonia (Apesteguía and Jones, 2012). Third, A. zamunerae is the only fossil Agathis that can be well compared to
living species because of its preservation of a large suite of
characters from multiple organs, and in all probability it is not
closely related to A. australis (see Comparisons to extant species). Therefore, there is still no reliable fossil evidence, from
New Zealand or elsewhere, concerning the origins of the A.
australis lineage.
Agathis zamunerae is the oldest example of a modern-aspect
Agathis, but at the same time it is significantly younger than the
oldest Araucaria (Middle Jurassic), in line with the abundant
molecular data that show Araucaria to be sister to Agathis plus
Wollemia, and the relatively late (Turonian) appearance of Wollemia-type pollen (Dilwynites; Macphail et al., 1995; Macphail
and Carpenter, 2013). Early Paleocene vegetative and fertile
macrofossils from the San Jorge Basin in Chubut of a probable
stem taxon of Agathis, currently under study, corroborate the
idea of a Paleogene crown for Agathis and show an even older
ex-Australasian distribution for the Agathis lineage (I. H. Escapa
et al., unpublished data).
Conclusions— Agathis zamunerae sp. nov. shows a large
suite of character states that are all found in living Agathis and
demonstrates that the lineage was present by the early Eocene,
in turn helping to validate the Australian early Cenozoic record
of the genus. The presence of Agathis in both Australia and
Patagonia just prior to and during the middle Eocene terminal
breakup of Gondwana clearly indicates that its range during the
globally warm Eocene was vast and must have included Antarctica, as is true of other fossil taxa that were previously shown
to have had similar past distributions and that are also frequently
associated with Agathis today.
The new species was a dominant component of the ancient
Patagonian rainforest biome, as indicated by its relatively high
leaf abundance. Assuming that A. zamunerae of Patagonia was
similar to living Agathis in having large stature, long life span,
and keystone ecological roles, its extinction was an important
contributor to the ecosystem transformation process in Patagonia from the ancient, high-diversity rainforests, eventually leading to its modern-day, carbon-poor steppe and species-poor
temperate rainforest biomes. This natural process took many
millions of years, but in its present range, many thousands of
kilometers distant from Patagonia, the rapid loss of Agathis forest is having comparable impacts, several orders of magnitude
more rapidly. As in the past, the present loss of Agathis is correlated with massive ecosystem disturbances and may well portend a threshold event, whereas success in conserving the genus
seems likely to be correlated with many aspects of improved
ecosystem health and biodiversity.
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Int. J. Plant Sci. 182(3):000–000. 2021.
q 2021 by The University of Chicago. All rights reserved.
1058-5893/2021/18203-00XX$15.00 DOI: 10.1086/712427
FIRST SOUTH AMERICAN RECORD OF WINTEROXYLON, EOCENE OF LAGUNA DEL HUNCO
(CHUBUT, PATAGONIA, ARGENTINA): NEW LINK TO AUSTRALASIA AND MALESIA
Mariana Brea,1,*,† Ari Iglesias,‡ Peter Wilf,§ Eliana Moya,* and María A. Gandolfo∥
*Laboratorio de Paleobotánica, Centro de Investigación Científica y de Transferencia Tecnológica a la Producción, Consejo Nacional de Investigaciones Científicas y Técnicas and Facultad de Ciencia y Tecnología, Provincia de Entre Ríos, Universidad Autónoma de Entre Ríos,
España 149, E3105BWA Diamante, Entre Ríos, Argentina; †Cátedra de Paleobotánica, Facultad de Ciencias Naturales y Museo,
Universidad Nacional de La Plata, Calle 122 y 60 s/n, 1900 La Plata, Buenos Aires, Argentina; ‡Instituto de Investigaciones
en Biodiversidad y Medioambiente, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional del
Comahue, Quintral 1250, 8400 San Carlos de Bariloche, Río Negro, Argentina; §Department of Geosciences and
Earth and Environmental Systems Institute, Pennsylvania State University, University Park, Pennsylvania 16802,
USA; and ∥L. H. Bailey Hortorium, Plant Biology Section, School of Integrative Plant Science,
Cornell University, Ithaca, New York 14850, USA
Editor: Alexandru M.F. Tomescu
Premise of research. Winteraceae, a family within the Canellales, is composed of tropical trees and shrubs
broadly distributed in the Southern Hemisphere. The family is found today in eastern Australia, New Zealand,
Malesia, Oceania, Madagascar, and the Neotropics across a range of dry to wet tropical to temperate climate regions. The fossil record of woods related to the Winteraceae in the Southern Hemisphere is limited to the Late Cretaceous of the Antarctic Peninsula. Here, we present a detailed anatomical description of the secondary xylem of a
well-preserved trunk from the early Eocene Laguna del Hunco site, Huitrera Formation, Patagonia (Chubut Province, Argentina), that is referable to a new species of the genus Winteroxylon (Gottwald) Poole and Francis.
Methodology. The wood is preserved as a siliceous permineralization; it was sectioned using standard petrographic techniques and observed under both light and scanning electron microscopy. The anatomy was compared
with that of extant and fossil species of Winteraceae.
Pivotal results. The diagnostic anatomical features of Winteraceae preserved in the fossil include an absence of
growth rings, a lack of vessels, tracheids that are rectangular in cross section with circular bordered pits, diffuse
axial parenchyma, rays showing two distinct size ranges (uniseriate-biseriate or multiseriate, 3–15 cells wide),
and the presence of heterocellular rays containing sclerotic nests, cells with dark contents, and oil cells. The new
fossil species most resembles extant genera within the Zygogynum s.l. clade from Australasian and Malesian rain
forests; its anatomy is very similar to that of the extant genus Bubbia. The new Patagonian Winteraceae fossil wood
is characterized by the presence of sclerotic nests and oil cells in the rays, which differ from those of previously described species of Winteroxylon.
Conclusions. On the basis of the distinctive characters preserved, we erect Winteroxylon oleiferum sp. nov. The
new fossil is the first reliable macrofossil record of Winteraceae from South America, supporting the abundant palynological record of the family from the continent, and it is the oldest record of the Zygogynum s.l. clade, adding to
the long list of southern biogeographic connections between South America and Australasia via Antarctica during
the warm early Cenozoic.
Keywords: wood anatomy, early Eocene, Huitrera Formation, Winteraceae, Winteroxylon, Zygogynum s.l. clade.
teraceae is strongly supported in several molecular analyses (Suh
et al. 1993; Qiu et al. 1999, 2005; Zanis et al. 2003; Soltis and
Soltis 2004; Marquínez et al. 2009; Massoni et al. 2015a,
2015b; Müller et al. 2015; APG IV 2016). Both families are
made up of aromatic woody shrubs and small trees with disjunct
distributions in the Southern Hemisphere (Marquínez et al.
2009; Thomas et al. 2014).
Today, the Winteraceae include ca. 60–90 species of evergreen trees, shrubs, and, rarely, epiphytes. Vink (1985) and
Marquínez et al. (2009) recognized five extant genera within
Winteraceae: Drimys J.R. Forst. & G. Forst, Pseudowintera
Introduction
The early-diverging angiosperm clade Magnoliidae comprises
four orders: Magnoliales, Laurales, Canellales, and Piperales
(Massoni et al. 2014, 2015a, 2015b; APG IV 2016). Canellales
is the smallest magnoliid order and includes only the Canellaceae
and Winteraceae. The sister relationship of Canellaceae and Win1
Author for correspondence; email: cidmbrea@gmail.com.
Manuscript received August 2020; revised manuscript received October 2020;
electronically published February 8, 2021.
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Dandy, Tasmannia R. Br. ex DC., Takhtajania Baranova & J.
Leroy, and Zygogynum Baill. Vink (1988) later recognized four
genera within Zygogynum s.l.: Bubbia Tiegh., Belliolum Tiegh.,
Exospermum Tiegh., and Zygogynum. Thomas et al. (2014)
also recognized those four genera as a monophyletic group.
Winteraceae and Canellaceae are each monophyletic (Massoni et al. 2014 and references cited therein), and several phylogenetic analyses agree that within the Winteraceae, Takhtajania
is the earliest-diverging lineage (Marquínez et al. 2009; Massoni
et al. 2014; Thomas et al. 2014; Müller et al. 2015; Grímsson
et al. 2018), followed by Tasmannia and Drimys. All the preceding are collectively sister to a clade comprising Pseudowintera as
sister to Zygogynum s.l. (including Belliolum, Bubbia, Exospermum, and Zygogynum s.s.; as proposed earlier by Vink 1988).
The relationships within Zygogynum s.l. are not fully resolved
(Grímsson et al. 2018). Marquínez et al. (2009) estimated the divergence of Takhtajania from the rest of the family to be at
ca. 91.5 (120–74) Ma and indicated that Tasmannia may have
diverged from other Winteraceae at ca. 69.9 (74.8–66.9) Ma.
The living Winteraceae species are restricted to Australasia,
Malesia, Oceania, Madagascar, and South and Central America, primarily in rain forest environments but also in a diverse
range of dry to wet tropical to temperate climatic regions (Lindley 1836; Vink 1988, 1993; APG IV 2016). On the basis of its
fossil record, the early history of Winteraceae can be traced back
to the Cretaceous to Eocene of both hemispheres, after which the
range contracted southward (Doyle 2000; Grímsson et al. 2018).
Several molecular phylogenetic hypotheses based on nuclear and
plastid sequence data are generally consistent, indicating that the
Winteraceae had a long and complex biogeographic history that
is explained by a combination of vicariance, long-distance dis-
persal, and extinction events (Marquínez et al. 2009; Thomas et al.
2014). The living genera are considered typical members of the austral flora (Thomas et al. 2014) and have disjunct distributions
in Australasia and Malesia (Tasmannia, Pseudowintera, Zygogynum, Exospermum, Bubbia, Belliolum), Madagascar (Takhtajania), and the Neotropics (Drimys; Grímsson et al. 2018).
This article reports a new fossil of Winteraceae from South
America consisting of a large stump sampled at the early Eocene
Laguna del Hunco (LH) fossil site in the Huitrera Formation,
Chubut Province, Argentina (fig. 1). The LH biota was first studied by Berry (1925) and was sporadically investigated over the
ensuing decades (e.g., Frenguelli 1943; Romero et al. 1988). Extensive research during the past 20 years has yielded extremely
diverse flora and fauna from the fossil caldera lake beds (for summaries, see, e.g., Wilf et al. 2013; Barreda et al. 2020; RossettoHarris et al. 2020), which are highly informative for understanding past and current biogeographical patterns in the Southern
Hemisphere. The extensive biogeographic links of the LH flora
include, via ancient Gondwana, living rain forests of Australasia
and Malesia, where the largest number of “survivor” genera are
found in Australian and New Guinean lower montane rain forest
floras (e.g., Zamaloa et al. 2006; Wilf et al. 2009; Gandolfo et al.
2011; Carvalho et al. 2013; Gandolfo and Hermsen 2017;
Andruchow-Colombo et al. 2019).
Nearly all reported plant fossils from LH are compressions
(but see Barreda et al. 2020 for a diverse palynoflora), although
decades ago, Petersen (1946) found fossilized trunks at the top
of the main lake bed sequence that were not further studied.
Permineralizations, including a silicified trunk of the fern Todea
Willd. ex Bernh. (Osmundaceae) with in situ liverworts, fungi,
and coprolites from the same source unit (Tufolitas LH) south
Fig. 1 Distribution of extant (dark gray) and fossil (light gray, Cretaceous; black, Cenozoic; star, pollen; circle, wood; rectangle, leaf )
Winteraceae. Fossil wood records are labeled as follows: Winteroxylon mundlosi (late Eocene; Helmstedt Formation, Lower Saxony, Germany),
Winteroxylon jamesrossi (early Campanian; Santa Marta Formation, James Ross Island, Antarctica), Winteroxylon? (Maastrichtian; Great Valley
Sequence, California), Winteroxylon oleiferum sp. nov. (arrow; early Eocene; Laguna del Hunco, Huitrera Formation, Chubut Province, Argentina). Modified from Grímsson et al. (2018). References: Doyle (2000); Barreda and Archangelsky (2006); Marquínez et al. (2009); Grímsson et al.
(2018); Liang et al. (2018); and others cited therein.
BREA ET AL.—FIRST SOUTH AMERICAN RECORD OF WINTEROXYLON
of the main LH exposures (Bippus et al. 2019; Bomfleur and
Escapa 2019), have only recently been described from the area.
Pujana et al. (2020) described a podocarp-dominated conifer
wood assemblage from LH that included Protophyllocladoxylon
francisiae Pujana, Santillana & Marenssi, Phyllocladoxylon antarcticum Gothan, and cf. Cupressinoxylon sp. 1 and sp. 2.
In this article, we describe the first fossil angiosperm wood from
LH, a new species of Winteraceae, based on anatomical study of a
silicified stump. On the basis of anatomical comparisons with extant and fossil specimens, we describe and interpret the significance of the new species with regard to the wood evolution, fossil
record, and biogeography of Winteraceae.
Material and Methods
The sample studied here was collected at LH, Huitrera Formation, by A. Iglesias and P. Wilf during the November 2009
field season at lat. 42727036.2600S, long. 7072017.8600W, elevation 1109 m (fig. 1). The stump was found lying in a horizontal
position on a steep east-facing slope exposure of the fossiliferous
LH caldera lake beds (Tufolitas LH; fig. 2) at a position above
the highest productive levels for compression fossils (i.e., quarry
LH6; Wilf et al. 2003). The Tufolitas LH are well dated from
40
Ar/39Ar analyses of minerals in three different tuffs, all of them
below the resting level of the trunk, and the presence of two paleomagnetic reversals (Wilf et al. 2003, 2005). A maximum
sanidine 40Ar/39Ar age of 52:22 5 0:22 Ma for one tuff is considered most reliable (M. Smith in Wilf 2012) and provides a min-
000
imum age for the wood specimen. In addition, the youngest beds
of the underlying local unit, the Ignimbrita Barda Colorada, have
recently been 40Ar/39Ar dated as 52:54 5 0:17 Ma (Gosses et al.
2020). The Tufolitas LH, containing the new fossil, are overlain
by the hill-capping (and completely unfossiliferous) Andesitas
Huancache unit (Aragón and Mazzoni 1997). The Andesitas Huancache have not been dated locally using modern techniques,
but potentially correlative strata in the southern caldera exposures have recently been 40Ar/39Ar dated to 49:19 5 0:24 Ma,
providing a likely minimum age for the fossil lake beds (Gosses
et al. 2020). Thus, the age of the wood specimen is early Eocene,
with a possible age range of ca. 52.2–49.2 Ma. We prefer the
older end of this range because of the provenance of the specimen
in the Tufolitas LH (ca. 52.2 Ma radiometric age).
The sampled stump is 150 cm in preserved length and 50 cm
in diameter, increasing to 124 cm toward the base, with several
woody roots of 4–15 cm in diameter that mostly have an axial
orientation (fig. 2B), although some broad roots are perpendicular to the main stem (fig. 2B). Secondary wood from the distal
part of the base of the main stem (fig. 2C) was sampled, leaving
the bulk of the specimen intact at the site. The silicified trunk has
well-preserved secondary xylem. Thin sections were made using
standard petrographic techniques (transverse, tangential longitudinal, and radial longitudinal). The anatomical terms used
in this article follow the International Association of Wood
Anatomists’ “List of Microscopic Features for Hardwood Identification” (IAWA Committee 1989). The taxonomic assignment,
descriptions, and comparisons with extant and fossil species were
Fig. 2 A, Panoramic view of Eocene strata at Laguna del Hunco (LH), looking southwest from the LH4 fossil locality and showing the positions of selected fossil plant localities. Location of the Winteraceae fossil stump sampled here (1) and fossil locality LH4 (2; Wilf et al. 2003).
B, Fossil stump in basal view, showing roots at the base of the stump (the black arrow indicates roots disposed perpendicular to the main stem;
the white arrow indicates roots disposed in an axial orientation). C, Lateral view of the stump, clearly showing the two regions: the stump with
roots (left) and the base of the main stem (right). D, View from the apical part of the preserved stem, showing the variation in the stump’s diameter
toward the base. Pick for scale p 30 cm.
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performed following the InsideWood website (InsideWood 2004–;
Wheeler 2011) and previous descriptions by Bailey and Thompson (1918), Bailey (1944), Bailey and Swamy (1948), Metcalfe
and Chalk (1950), Swamy and Bailey (1950), Tortorelli (1956),
Patel (1974), Carlquist (1981, 1982, 1983a, 1983b, 1987, 1988,
1989, 2000, 2001), Scott and Wheeler (1982), Rancusi et al.
(1987), Poole and Francis (2000), Carlquist and Schneider (2001),
and Schweingruber et al. (2011).
The specimen was studied with a Nikon Eclipse E200 light microscope, and photomicrographs were taken with an attached
Nikon Coolpix S4 digital camera. The values in the anatomical
description are averages of 25 measurements. In all cases, the average value is cited first, followed by the minimum and maximum
values, which are given in parentheses. We prepared the specimen
for scanning electron microscopy (SEM) by cutting 1-cm3 blocks
of fossil wood, mounting them on SEM stubs, and coating them
with platinum/palladium; observation and photographs were
done using an FEI Nova NanoSEM 230 microscope at the Laboratorio de Microscopía, Caracterización de Materiales, Centro
Atómico Bariloche, Argentina. The macrofossil specimens and
slides are deposited at the Museo Paleontológico Egidio Feruglio
paleobotanical collection (MPEF-Pb) in Trelew, Argentina.
Results
Systematic Paleobotany
Order—Canellales
Family—Winteraceae
Genus—Winteroxylon (Gottwald) emend.
Poole & Francis 2000
Fig. 3 Winteroxylon oleiferum sp. nov., MPEF-Pb 3997. A, General view in transverse section, showing uniseriate rays (arrows) and tracheids.
B, C, General view in transverse section, showing uniseriate rays (white arrows), multiseriate rays (black arrows), and tracheids. D, General view in
tangential longitudinal section, showing uniseriate and multiseriate rays (white arrow) composed of procumbent and upright cells and probable
sheath cells (black arrows). E, F, General view in tangential longitudinal section, showing oil cavities (arrows) surrounded by parenchymatic cells
inside the multiseriate rays. G, General view in tangential longitudinal section, showing sclerotic nests (white arrow) and dark amorphous contents
(black arrow) in a multiseriate ray. H, I, General view in radial longitudinal section, showing heterocellular rays composed of procumbent and
upright cells (arrows). Scale bars p 400 mm.
BREA ET AL.—FIRST SOUTH AMERICAN RECORD OF WINTEROXYLON
Type Species—Winteroxylon mundlosi Gottwald 1992
Species—Winteroxylon oleiferum Brea, Iglesias, Wilf,
Moya & Gandolfo sp. nov. (Figs. 3–6)
Etymology. The specific name refers to the abundance of oil
cells in the wood.
Specific diagnosis. Growth rings indistinct. Tracheids thick
walled with circular bordered pits, mainly in uniseriate, biseriate,
and triseriate rows, alternate to opposite. Axial parenchyma either diffuse or in tangentially or radially oriented pairs of parenchyma strands. Rays of two different types (narrow and broad),
heterocellular and very tall, uniseriate, biseriate, and multiseriate
(3–15 cells wide). Bordered pits in ray cells. Sclerotic nests, oil
cells, and dark contents in rays present.
000
Holotype. MPEF-Pb 3997a–MPEF-Pb 3997e (one macrofossil and four microscope slides).
Locality. LH, early Eocene of northwestern Chubut Province, Argentina (lat. 42727036.2600S, long. 707 2017.8600W), Huitrera Formation.
Description. The description is based on the mature wood of
one stump specimen. In transverse section, the mature wood is
vesselless and composed exclusively of imperforate tracheids
and parenchyma (figs. 3A–3C, 4A), with indistinct growth rings
(fig. 3A–3C). The tracheids are quadrangular to rectangular
(figs. 4A, 4D, 5E) and have a mean tangential diameter of 24
(14–33) mm and a mean radial diameter of 27 (19–31) mm. They
are thick walled (fig. 5E), with a wall thickness of 7 (5–9) mm.
Middle lamellae and pits are observed on the tracheids (fig. 5E).
Triangular or quadrangular intercellular spaces (fig. 4A, 4D)
Fig. 4 Winteroxylon oleiferum sp. nov., MPEF-Pb 3997. A, Detail in transverse section, showing tracheids, axial parenchyma (arrows), and a
multiseriate ray. Scale bar p 200 mm. B, Detail in tangential longitudinal section, showing multiseriate, biseriate (black arrow), and uniseriate
(white arrow) rays. Scale bar p 200 mm. C, Detail in tangential longitudinal section, showing multiseriate rays of up to 15 cells. Scale bar p
200 mm. D, Detail in transverse section, showing axial parenchyma with pits (arrows). Scale bar p 50 mm. E, Detail of a parenchyma pit in transverse section (arrow). Scale bar p 20 mm. F, Detail in tangential longitudinal section, showing a sclerotic nest. Scale bar p 200 mm. G, Detail in
radial longitudinal section, showing a heterocellular ray composed of procumbent and upright cells. Scale bar p 200 mm. H, Detail in tangential
longitudinal section, showing an oil canal (arrow). Scale bar p 200 mm. I, Detail in tangential longitudinal section, showing the dark contents in a
ray cell. Scale bar p 50 mm. J, General view in radial longitudinal section, showing the bordered pits in the ray cells (arrow). Scale bar p 200 mm.
K, Detail in radial longitudinal section, showing the bordered pit in a ray cell (arrow). Scale bar p 50 mm.
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Fig. 5 Winteroxylon oleiferum sp. nov., MPEF-Pb 3997. A, Detail in tangential longitudinal section, showing circular bordered and uniseriate
pits. Scale bar p 20 mm. B, Detail in tangential longitudinal section, showing circular bordered, biseriate, and alternate pitting. Scale bar p 50 mm.
C, Detail in tangential longitudinal section, showing circular bordered, triseriate, and alternate to opposite pitting. Scale bar p 50 mm. D, Detail in
tangential longitudinal section, showing a biseriate ray and trabeculae in the tracheids (arrows). Scale bar p 50 mm. E, Detail in transverse section,
showing three tracheid cells with middle lamellae (white arrow) and a pit (black arrow). Scale bar p 20 mm. F, Detail in radial longitudinal section,
showing bordered pits that are alternate to irregular in arrangement (arrow) in the ray cells. Scale bar p 50 mm. G, Detail in tangential longitudinal
section, showing sclerotic cells (white arrow) and dark amorphous accumulations in a cell (black arrow). Scale bar p 50 mm. H, Detail in tangential
longitudinal section, showing a sclerotic nest. Scale bar p 50 mm.
are present between tracheids. The axial parenchyma is diffuse
and scarce, presenting as occasional radially oriented pairs of
parenchyma strands (fig. 4A, 4D). The parenchyma cell pits are
small, circular, and simple (fig. 4D, 4E).
In tangential longitudinal section, the tracheid pitting is circular, bordered, and contiguous, with elliptic pit apertures (fig. 5A–
5C). The circular pits have a mean diameter of 8 (7–10) mm and
are frequently uniseriate (fig. 5A), occasionally biseriate (figs. 5B,
6C), and rarely triseriate (fig. 5C); when bi-triseriate. pits are alternate to opposite. Some tracheids have trabeculae on their walls
(fig. 5D). The rays are of two distinct types, uniseriate-biseriate
and multiseriate (3–15 cells), and both are heterocellular and
Fig. 6 Winteroxylon oleiferum sp. nov., MPEF-Pb 3997, under scanning electron microscopy. A, Detail in radial longitudinal section, showing bordered
pits in ray cells that are alternate to irregular in arrangement. Scale bar p 100 mm. B, Detail in radial longitudinal section, showing bordered pits. Scale
bar p 30 mm. C, Detail in tangential longitudinal section, showing biseriate, bordered, and alternate to opposite pits in a tracheid. Scale bar p 30 mm.
BREA ET AL.—FIRST SOUTH AMERICAN RECORD OF WINTEROXYLON
composed of predominantly upright cells (figs. 3I, 4G), occasionally with procumbent cells (figs. 3I, 4F).
The sclerotic nests (figs. 3G, 4F, 5H), sclereids (fig. 5G), and
oil cells (figs. 3E–3F, 4H) are abundant and are associated with
ray parenchyma. The oil cells are similar to the parenchyma cells
in size and are found scattered in rays; oil cavities are occasionally present in the central portions of multiseriate rays and
are surrounded by three or more layers of parenchyma cells
(figs. 3E–3F, 4H). Sclereid cells are polygonal or hexagonal in
outline (figs. 4F, 5G, 5H), with a diameter of 99 (43–178) mm,
and are thick walled, with a wall thickness of 34 (8–64) mm
(fig. 5H). Each sclerotic nest has 3–11 sclereid cells. The multiseriate rays have a mean height of 2089 (1035–4105) mm and
a mean width of 547 (188–1504) mm. Probable sheath cells occur in the multiseriate rays (fig. 3D). The uniseriate (fig. 4B) and
biseriate (fig. 4B) rays (86%) are more common than the multiseriate rays (14%; figs. 3D–3G, 4A–4C). The uniseriate rays are
heterocellular and have a mean height of 314 (131–655) mm and
a mean width of 35 (23–55) mm. In both ray types (narrow and
broad), dark amorphous contents are observed inside the ray
cells, probably attributable to resins (figs. 3G, 4I, 5G).
In radial longitudinal section, the tracheid pitting is more
abundant on the radial compared with the tangential walls
(fig. 4J). The rays are heterocellular, composed of upright and
procumbent cells (fig. 4G). The ray cell pits are circular, bordered, and alternate to irregular in arrangement (figs. 4K, 5I,
6A, 6B). The procumbent cells are 97 (73–154) mm in height
and 26 (16–35) mm in width, and upright cells are 51 (43–58) mm
in height and 32 (22–38) mm in width.
Discussion
Comparison with Extant and Fossil Taxa
The absence of the typical conifer cross-field pitting and the
presence of heterocellular uni- to multiseriate rays, axial parenchyma, cells with contents (i.e., oil cells, idioblasts), and sclereids
confirm that this fossil corresponds to a vesselless angiosperm.
Vesselless woods are present in five early-diverging angiosperm
families: Amborellaceae, Tetracentraceae, Trochodendraceae,
Chloranthaceae, and Winteraceae (Bailey and Thompson 1918;
Bailey 1944; Bailey and Swamy 1948; Metcalfe and Chalk 1950;
Swamy and Bailey 1950; Carlquist 1987; Schweingruber et al.
2011). Amborella trichopoda Baill. is the only known member
of Amborellaceae; it is endemic to New Caledonia, inhabiting
the understory of humid forests, where it grows as shrubs or small
trees. Its wood is characterized by vesselless xylem with very
weakly defined growth rings, bordered circular and scalariform
pits on the tracheids, diffuse apotracheal axial parenchyma, dark
contents in parenchyma cells, uniseriate and multiseriate (up to
five cells) rays, and heterocellular rays with more than four marginal upright cells (Carlquist and Schneider 2001; Schweingruber
et al. 2011). This extant species differs from the new fossil specimen in having multiseriate rays that are three to five cells wide,
scalariform pits on the tracheids, and rays with more than four
marginal upright cells.
Tetracentraceae, native to southern China and the eastern
Himalayas, includes the sole extant species Tetracentron sinense
Oliv. It grows along streams or forest margins in broad-leaved
evergreen forests and mixed evergreen-deciduous forests (Suzuki
et al. 1991) as trees that can reach up to 40 m tall. The secondary
000
xylem is characterized by having axial parenchyma that is diffuse and diffuse in aggregates and uniseriate and homocellular
multiseriate rays that are three or four cells wide (Poole and
Francis 2000; InsideWood 2004–). Tetracentron differs from
the fossil and extant Winteraceae woods in having rays that
are three or four cells wide and exclusively procumbent cells.
Also, Tetracentron has unusual thin-walled tracheids arranged
in radial files, with crowded, alternate, circular to elliptical bordered pits in the tangential walls and radial walls without pitting (Suzuki et al. 1991); all of these features are unlike those
of the new fossil.
Trochodendron aralioides Sieb. & Zucc. belongs to the monospecific Trochodendraceae. They are evergreen trees or large
shrubs growing up to 20 m tall that are confined to montane temperate forests in Southeast Asia and Taiwan (APG IV 2016).
Their secondary xylem has distinct growth rings, bordered scalariform pit tracheids, axial parenchyma that is rare or absent,
and rays in two types: uniseriate and heterocellular multiseriate,
three to six cells wide. There are large and simple pits in the ray
cells (Schweingruber et al. 2011). Trochodendron differs from
the new Patagonian taxon in having distinct growth rings, axial
parenchyma that is absent or extremely rare, bordered scalariform pits in the tracheids, simple pits in the cell rays, and multiseriate rays with very tall uniseriate extensions (Scott and
Wheeler 1982; Richter and Dallwitz 2000).
Sarcandra Gardner, the only vesselless genus within the
Chloranthaceae, includes small shrubs native to Southeast Asia;
its wood has distinct growth rings, absent or rare axial parenchyma, tracheids and transitional tracheid-vessel elements, and,
commonly, 4–10 seriate heterocellular rays (Swamy and Bailey
1950; Carlquist 1987; InsideWood 2004–). Sarcandra has fascicular uniseriate rays and interfascicular multiseriate rays.
These large multiseriate (up to five cells wide) parenchyma rays
in Sarcandra are derived from a cambial variant that produces
axial vascular elements in segments and interfascicular multiseriate rays (Pipo et al. 2020). Cambial variant features are absent in Winteroxylon oleiferum sp. nov.
Of all these vesselless angiosperms, only Winteraceae have
woods with 110-seriate rays, oil cells, and sclerotic nests in
heterocellular rays, as seen in the fossil. The new fossil species
shares additional character states with Winteraceae, including
absent growth rings, tracheids that are rectangular in transverse
section with circular bordered pits, diffuse axial parenchyma,
rays of two distinct sizes, uniseriate-biseriate and multiseriate
(3–15 cells wide) rays, and cells with dark contents.
We summarize the anatomical comparison between the new
fossil species and the extant species of Winteraceae (table 1).
Clearly, the new Patagonian fossil species is most similar to the
extant species in the Zygogynum s.l. clade (Bubbia, Belliolum,
Exospermum, and Zygogynum s.s.). The extant genera Pseudowintera, Takhtajania, and Belliolum are different from the
new Patagonian species in their absence of oil cells, silica bodies,
and sclerotic nests. The American genus Drimys does not produce
oil cells or sclerotic nests and has smooth and irregular silica
bodies, a feature absent in the fossil wood. Tasmannia differs in
having uniseriate and biseriate radial tracheid pits with helical
thickenings and rays that do not have oil cells. Exospermum lacks
sclerotic nests in rays and has rectangular tracheids in transverse
section and axial parenchyma in bands. Zygogynum s.s. differs
because it has uniseriate tracheid pitting and an absence of trabeculae in the tracheids (table 1). On the other hand, Bubbia shares
Table 1
Wood Anatomical Comparisons of Winteroxylon oleiferum sp. nov. with Extant and Fossil Taxa of Winteraceae
Taxon
Drimys
Takhtajania
Tasmannia
Tracheid
section
Square to
irregular
Bubbia
Exospermum
Uniseriate, biseriate,
triseriate
Tracheid
diameter
(mm)a
Tracheid pitting
6–16 mm in diameter,
circular, bordered,
opposite, alternate,
scalariform
Quadrangular
Uniseriate, biseriate; 38 (mean) Circular, bordered,
to rectangular
helical thickenings
scalariform
Quadrangular
Uniseriate, biseriate;
to rectangular
helical thickenings
Pseudowintera Square to
irregular
Belliolum
Radial tracheid
pitting
Quadrangular
to rectangular
Uniseriate, biseriate,
triseriate; spiral
thickenings
and trabeculae
Biseriate, triseriate
25–69
16–46
Circular, bordered,
scalariform to
transitional
13–46
Circular, bordered,
alternate, opposite,
scalariform
Circular, bordered,
scalariform to transitional to opposite
Square to
Uniseriate, biseriate,
23–51 7–14 mm in diameter,
irregular
triseriate; trabeculae
circular, opposite,
common
occasionally elongated, scalariform
Quadrangular
Biseriate, triseriate
55 (mean) Circular to elongated,
to rectangular
alternate
Uniseriate
42–60
Zygogynum
s.s.
Square to
irregular
...
W. oleiferum
sp. nov.
14–33
Quadrangular
Uniseriate, biseriate,
to rectangular
triseriate; trabeculae
common
Circular, bordered,
scalariform
7–10 mm in diameter,
circular, alternate
to opposite
Winteroxylon
mundlosi
...
Uniseriate, biseriate;
sometimes
scalariform
23–36
Circular
Winteroxylon
jamesrossi
...
Uniseriate, biseriate;
elongate to
scalariform
30–50
Circular to more
elongate
a
Tracheid diameter is measured in tangential section.
Axial parenchyma
Ray type and
structure
Scarce or absent,
diffuse
Ray height (mm)
Uniseriate,
multiseriate
(4–10 cells),
heterocellular
Scarce, diffuse
Uniseriate, biseriate,
multiseriate (up
to 5 cells),
heterocellular
Scarce, diffuse, occa- Uniseriate, biseriate,
sional tangential or
multiseriate,
radial parenchyma
heterocellular
strands
Scarce, diffuse, diffuse Uniseriate, biseriate,
in aggregates
multiseriate
(7–29 cells),
heterocellular
Scarce, diffuse, in
Heterocellular
short bands
Uniseriate (300–
3370),
multiseriate
(1250–4800)
Uniseriate (mean,
1473),
multiseriate
(mean, 4176)
Uniseriate (286–
1816),
multiseriate
(1093–5148)
Uniseriate,
multiseriate
(300–6100)
Diffuse or in bands
1–3 cells thick
Uniseriate, biseriate,
multiseriate
(3–7 cells),
heterocellular
Diffuse or in bands
Uniseriate,
1–3 cells thick
multiseriate (up
to 7 cells)
Scarce, diffuse, diffuse Uniseriate,
in aggregates, in
multiseriate
bands 2 or 3 cells
thick
Scarce, diffuse, occa- Uniseriate, biseriate,
multiseriate
sional tangential or
(3–15 cells),
radial parenchyma
strands
heterocellular
Uniseriate bands
Uniseriate,
multiseriate
(3–7 cells),
heterocellular
Diffuse or in radial
Uniseriate, biseriate,
pairs and short
multiseriate
strands of up to
(3–13 cells),
ca. 4 cells thick
heterocellular
Cell contents
Oil
cells
Sclerotic
nest
Dark
Absent Absent
amorphous
Tannin-like
...
Absent Absent
Absent Present
Absent
Absent Absent
Resinlike
Absent Absent
600 to 11500
Resinlike
Present Absent
Multiseriate
(mean, 6812)
Resinlike
Present Absent
...
...
...
Present Sclereids
Uniseriate
(131–665),
multiseriate
(1035–4105)
All rays higher
than 2000
Dark
Present Present
amorphous
Present
Absent Present
Uniseriate
(200–1636),
multiseriate
(500–4300)
Occasional
Absent Absent
BREA ET AL.—FIRST SOUTH AMERICAN RECORD OF WINTEROXYLON
with W. oleiferum sp. nov. the uniseriate, biseriate, and triseriate
arrangement of tracheid pitting in the radial walls, the presence of
trabeculae in the tracheids, square to irregular tracheids in transverse section, and oil cells associated with the rays.
Winteroxylon oleiferum sp. nov. is placed in Winteroxylon
based on the presence of indistinct growth rings, predominantly
diffuse axial parenchyma, tracheids with circular bordered pits,
and predominantly multiseriate rays with up to 13 cells or
uniseriate-biseriate rays that are heterocellular and nonstoried
(Poole and Francis 2000). All of the features of the new fossil
fit within Winteroxylon, and thus there is no basis for erecting
a new genus. Until now, there were only two reliable fossil
woods assigned to the Winteraceae, Winteroxylon jamesrossi
Poole & Francis from the early Campanian Santa Marta Formation, Antarctic Peninsula (Poole and Francis 2000; Olivero
2012; fig. 1), and Winteroxylon mundlosi Gottwald from the
late Eocene Helmstedt Formation, lignite opencast mine, Lower
Saxony, Germany (Gottwald 1992; fig. 1). Winteroxylon jamesrossi lacks the oil cells and sclerotic cells seen in the new fossil,
whereas W. mundlosi differs from the Patagonian fossil in having taller rays and an absence of oil cells (table 2). Also, both of
000
the previously known Winteroxylon species have distinct scalariform tracheid pitting not seen in the new species. Page (1979,
1981) described a minute (7 mm in diameter) twig of putative
Winteraceae affinity from the Maastrichtian Great Valley Sequence (California; fig. 1) that can be easily distinguished from
the new fossil because of its abundant axial parenchyma, absence of bi-triseriate rays, and absence of both oil cells and sclerotic cells (table 2).
According to Poole and Francis (2000), the anatomical
characters of W. jamesrossi are related to those exhibited in extant Bubbia. However, as also noted by those authors, there are
many differences between the extant genus and the Antarctic
fossil. It seems clear that W. jamesrossi most closely matches
anatomically with extant Takhtajania and Tasmannia, especially in ray height, the type of tracheid pitting, and the absence
of both trabeculae and oil cells (table 1).
Winteroxylon mundlosi has a central pith with sclerotic cells,
rays greater than 2 mm in height and up to eight cells wide, and
sclerotic cells (table 2). Although Gottwald (1992) did not identify oil cells in W. mundlosi, they were noted as possibly present
in this taxon by Poole and Francis (2000). Gottwald (1992)
Table 2
Further Comparison among Fossil Wood Species of Winteraceae
Winteroxylon jamesrossi
Reference(s)
Fossil locality
Stratigraphic
horizon, age
Growth rings
Axial parenchyma
Tracheids:
Tangential diameter
(mm)
Radial diameter (mm)
Wall thickness (mm)
Pitting diameter (mm),
shape
Overlapped area
Rays:
Structure
Height (mm)
Width
Cell pitting
Cell content:
Dark amorphous
Oil cells
Sclerotic cells
Winteroxylon mundlosi
Winteroxylon?
Winteroxylon oleiferum
sp. nov.
Poole and Francis 2000
Lachman Crags, James
Ross Island, Antarctica
Santa Marta Formation,
early Campanian
Indistinct
Diffuse or in radial pairs;
forms short axial
strands of up to 4 cells
Gottwald 1992
Helmstedt area, Lower
Saxony, Germany
Annenberg Formation,
late Eocene
Indistinct
Uniseriate bands
or in tangential,
apotracheal,
uniseriate bands
Page 1979, 1981
Diablo Range, central
California
Great Valley Sequence,
Maastrichtian
?
Abundant
This contribution
Laguna del Hunco,
Chubut, Argentina
La Huitrera Formation,
early Eocene
Indistinct
Diffuse, occasional
tangentially or radially
oriented strand pairs
30 (35) 50
23 (29) 36
13 (26) 38
14 (24) 33
15 (28) 40
2.5–10
2.5–15, circular to more
elongate
Uniseriate, biseriate,
elongate to scalariform
...
5 (7) 9
7 (9) 11, circular
...
Thick walled
Small, rounded
19 (27) 31
5 (7) 9
7 (8) 10, circular
Heterocellular procumbent
cells becoming square to
periphery; upright cells in
uniseriate and multiseriate
wings
Uniseriate, 200–1636;
multiseriate,
500–4300
Uniseriate, biseriate;
4–13 cells
Circular, bordered
Heterocellular upright
cells in uniseriate
and multiseriate wings
Circular
Uniseriate, 131 (314)
655; multiseriate, 1035
(2089) 4105
Uniseriate, multiseriate;
Uniseriate, biseriate;
4–5 cells
3–15 cells
Minute pits on tangential walls Circular, bordered
Occasional
Absent
Absent
Present
Absent
Present
Absent?
Absent
Absent
Uniseriate, biseriate,
sometimes scalariform
All rays greater than 2000
Uniseriate; 3–8 cells
?
Heterocellular square or
upright cells
Uniseriate, biseriate,
triseriate
Heterocellular upright
and procumbent cells
?
Present
Present
Present
INTERNATIONAL JOURNAL OF PLANT SCIENCES
000
placed W. mundlosi as closely related to extant Drimys and
Bubbia. In table 1, the European fossil matches most closely
with extant Takhtajania and Tasmannia. On the basis of this
discussion, W. oleiferum sp. nov. may represent the sole fossil
sharing wood anatomy with the Zygogynum s.l. clade (following Thomas et al. 2014).
Sherwinoxylon winteroides Boura & Saulnier, a vesselless
angiosperm of uncertain family from the middle Cenomanian
of the Envigne Valley in western France, has exclusively multiseriate rays up to nine cells wide and 1.03–10.53 mm high that
are composed of square cells, as well as up to four upright marginal cells. This fossil shows similarities to extant and fossil
Winteraceae, but the absence of uniseriate rays led Boura et al.
(2019) to suggest that it may belong to an extinct group that either is unrelated to Winteraceae or belongs to stem Winteraceae.
Sherwinoxylon winteroides also differs from W. oleiferum sp.
nov. in having tracheids with exclusively uniseriate bordered pits
and an absence of uniseriate rays, oil cells, and sclerotic cells.
Biogeography and Phylogenetic
Relationships of Winteraceae
The living genera of Winteraceae have disjunct distributions in
Australasia (Pseudowintera, Zygogynum, Exospermum, Bubbia,
Belliolum, Tasmannia), Madagascar (Takhtajania), and the Neotropics (Drimys; e.g., Grímsson et al. 2018). The habit and geographical distribution of the extant genera of Winteraceae are
shown in table 3.
Winteraceae has fossil records from the Cretaceous in Laurasia
and Gondwana, suggesting that the group was globally distributed from the Cretaceous until at least the Eocene in the Northern Hemisphere and that it subsequently became extinct (Grímsson et al. 2018). In the Southern Hemisphere, this family has
been a persistent component of rain forests or wet sclerophyll
forests (Hill 1994; Marquínez et al. 2009), with records since
the middle Cretaceous (Barreda and Archangelsky 2006; fig. 1).
In addition to the Winteraceae fossil wood record (table 2), pollen tetrads of Walkeripollis gabonensis Doyle, Hotton & Ward
were reported from the Barremian-Aptian of Gabon, Africa
(Doyle et al. 1990; fig. 1). Qatanipollis valentini Schrank is a putative Winteraceae pollen type described from the late AptianAlbian of Israel (Schrank 2013) that was originally reported by
Walker et al. (1983) and then designated by Doyle et al. (1990)
as Walkeripollis sp. In Australasia, the fossil record of this family
dates from mid-Campanian sediments of the Otway Basin (Dettmann and Jarzen 1990; Grímsson et al. 2018). Grímsson et al.
(2018) proposed that Winteraceae pollen fossils recorded in the
Paleocene and Eocene of North America and Greenland represent
interchange with Europe via the North Atlantic land bridge. This
hypothesis could also explain the presence of Winteraceae woods
in California and Germany (fig. 1; table 2).
Reliable leaf fossils of Winteraceae are very rare (fig. 1). Zygogynum poratus Liang & Zhou is a leaf compression from the
middle Miocene of Yunnan, southwest China, that shares cuticular features and morphological characters with Zygogynum s.s.
(Liang et al. 2018). A leaf impression assigned to Drimys
Table 3
Comparison of the Stem Morphologies, Habit Preferences, Phenology, Habits, and Geographic Distributions of the Genera of Winteraceae
Stem diameter Stem height
(cm)
(m)
Growth habit
Drimys
Takhtajania
.6–10
Up to 20
Shrubs to
small trees
Evergreen
Up to 4.5
Up to 5
Shrubs to
small trees
Small trees
Evergreen
4–34
Tasmannia
Leaf habit
4 or more
Evergreen
Habitat
Moist mountain forests (tropical and
temperate, frost-free) in Neotropics,
maritime temperate rain forests,
subantarctic temperate forests
Subhumid higher montane forests
(~1000 m)
Moist mountain forests, in wet areas
in the drier forests, alpine and
lowland temperate rain forests
Lowland to higher montane forests
(from lat. 357S to 427S)
Pseudowintera
2.5–6.6
1–8
Shrubs to
small trees
Evergreen
Zygogynum s.l.
clade:
Belliolum
ca. 10
...
Small trees
Evergreen
...
15
Small to large Evergreen
trees
Understory and subcanopy treeless
to trees in subtropical lowland
rain forests
Tropical premontane and
montane cloud forests
Exospermum
ca. 24
...
Large trees
Subtropical lowland rain forests
Zygogynum
s.s.
...
2–3
Small trees to Evergreen
shrubs
Bubbia
Sources.
Evergreen
Subcanopy trees in subtropical
lowland rain forests and
montane cloud forests
Extant geographic
distribution
Neotropics (from southern
Mexico to southern
South America)
Madagascar
Australia, New Guinea,
Celebes, Borneo,
Philippines
New Zealand
Solomon Islands,
New Caledonia
Eastern Australia,
New Guinea,
New Caledonia,
Moluccas
Eastern Australia,
New Guinea, New
Caledonia, Moluccas
New Caledonia
Tortorelli (1956); Patel (1974); Carlquist (1981, 1982, 1983a, 1983b, 1988, 1989, 2000); Feild et al. (2000).
BREA ET AL.—FIRST SOUTH AMERICAN RECORD OF WINTEROXYLON
antarctica Dusén from the Cross Valley Formation, Seymour Island, Antarctic Peninsula, is poorly preserved and lacks diagnostic features that would provide a reliable taxonomic position within Winteraceae (Dusén 1908; Tosolini et al. 2013). In
Patagonia, a leaf impression dubiously assigned to Drimys,
Drimys patagonica Berry from the middle Eocene Río Pichileufú
flora (Berry 1938), Argentina, needs further study to clarify its
taxonomic status.
The oldest occurrence of Winteraceae pollen in South America
was dated to the late Albian-Cenomanian Kachaike Formation
(Barreda and Archangelsky 2006; fig. 1). From the Paleogene,
Pseudowinterapollis couperi (Krutzsch) emend. Mildenhall &
Crosbie pollen grains were recovered from Argentine Patagonia
in the late Eocene Sloggett Formation (Olivero et al. 1998), the
late Oligocene?–Miocene Chenque Formation (Barreda 1997b),
and the Oligocene San Julián Formation (Barreda 1997a), among
others (e.g., Kooyman et al. 2014). According to Doyle (2000),
the sculpture and presence of a well-defined annulus in the Oligocene P. couperi from the Chenque Formation could indicate production by plants closely related to Drimys, whereas Grímsson
et al. (2018) proposed that the South American fossil pollen could
be linked to the extant genera Drimys, Tasmannia, and Pseudowintera, along with the Miocene tetrad Pseudowinterapollis africanensis Grímsson, Neumann & Zetter of South Africa (Grímsson et al. 2017).
As discussed above, W. oleiferum sp. nov. resembles members
of the extant Zygogynum s.l. clade because it has distinctive
sclerotic nests and oil cells. Furthermore, most of its anatomical
characters, including the presence of uniseriate, biseriate, and
triseriate tracheid pitting in the radial walls, trabeculae in
tracheids, square to irregular tracheid transverse sections, and
oil cells associated with ray cells, match those of extant Bubbia
(table 1). Today, the Zygogynum s.l. clade is distributed in eastern Australia, New Guinea, the Moluccas, and New Caledonia
and predominantly in tropical premontane and montane cloud
forests (table 3), locations and environments that are well identified for having large numbers of “survivor” taxa from the LH
flora and late-Gondwanan fossil floras in general (e.g., Wilf et al.
000
2009, 2013, 2019; Kooyman et al. 2014, 2019). The only previous fossil record assigned to the Zygogynum s.l. clade is Miocene leaves of Z. poratus from southwest China, indicating an
additional past distribution of the clade, thought to be sourced
from Gondwana, in mainland Asia (Liang et al. 2018).
The phylogenetic analyses of Suh et al. (1993), Marquínez
et al. (2009), and Thomas et al. (2014) show that the Zygogynum s.l. clade can be resolved into two subclades: the (Zygogynum 1 Belliolum 1 Exospermum) subclade from New Caledonia and the other with the Bubbia species, distributed in eastern
Australia, New Guinea, the Moluccas, and New Caledonia (table 3). Thus, W. oleiferum sp. nov. is the oldest reliable macrofossil record of Winteraceae resembling species of the Zygogynum
s.l. clade—a derived clade within extant Winteraceae—that today
live in Australasian and Malesian rain forests. The presence of
Bubbia-like Winteraceae at middle latitudes of Patagonia during
the early Eocene reinforces the evidence for southern biogeographic connections between South America and Australasia
via Antarctica during the warm early Cenozoic and the subsequent extinction of some Winteraceae clades in South America.
Acknowledgments
For exceptional assistance in the field and laboratory, we are
grateful to M. Caffa, L. Canessa, P. Puerta, and E. Ruigomez,
and we thank the Nahueltripay family and the Secretaría de
Cultura of the Chubut Province Government for land access.
We thank Laboratorio de Microscopía, Grupo de Caracterización de Materiales, Centro Atómico Bariloche for SEM
imaging, M. Medina from the LABGEO-Córdoba University
(CICTERRA-CONICET) for making the petrographic sections,
and two anonymous reviewers and Editor Alexandru M.F.
Tomescu for helpful comments on the manuscript. We acknowledge financial support from National Science Foundation grants
DEB-0345750, DEB-0919071, DEB-0918932, DEB-1556666,
DEB-1556136, EAR-1925755, and EAR-1925481.
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