The fossil flip-leaves (Retrophyllum, Podocarpaceae)

RESEARCH ARTICLE A M E R I C A N J O U R N A L O F B O TA N Y

The fossil flip-leaves (Retrophyllum, Podocarpaceae) of southern South America1 Peter Wilf2,6, Michael P. Donovan2,3, N. Rubén Cúneo4, and María A. Gandolfo5

PREMISE OF THE STUDY: The flip-leaved podocarp Retrophyllum has a disjunct extant distribution in South American and Australasian tropical rainforests and a Gondwanic fossil record since the Eocene. Evolutionary, biogeographic, and paleoecological insights from previously described fossils are limited because they preserve little foliar variation and no reproductive structures. METHODS: We investigated new Retrophyllum material from the terminal Cretaceous Lefipán, the early Eocene Laguna del Hunco, and the early/middle Eocene Río Pichileufú floras of Patagonian Argentina. We also reviewed type material of historical Eocene fossils from southern Chile. KEY RESULTS: Cretaceous Retrophyllum superstes sp. nov. is described from a leafy twig, while Eocene R. spiralifolium sp. nov. includes several foliage forms and a peduncle with 13 pollen cones. Both species preserve extensive damage from sap-feeding insects associated with foliar transfusion tissue. The Eocene species exhibits a suite of characters linking it to both Neotropical and West Pacific Retrophyllum, along with several novel features. Retrophyllum araucoensis (Berry) comb. nov. stabilizes the nomenclature for the Chilean fossils. CONCLUSIONS: Retrophyllum is considerably older than previously thought and is a survivor of the end-Cretaceous extinction. Much of the characteristic foliar variation and pollen-cone morphology of the genus evolved by the early Eocene. The mixed biogeographic signal of R. spiralifolium supports vicariance and represents a rare Neotropical connection for terminal-Gondwanan Patagonia, which is predominantly linked to extant Australasian floras due to South American extinctions. The leaf morphology of the fossils suggests significant drought vulnerability as in living Retrophyllum, indicating humid paleoenvironments. KEY WORDS Argentina; Chile; conifers; Cretaceous; Eocene; disjunctions; fossils; Podocarpaceae; Retrophyllum; transfusion tissue

Retrophyllum C. N. Page (Podocarpaceae; Figs. 1–9; Table 1) is a small genus of tropical rainforest conifers with a disjunct Neotropical–West Pacific distribution and a scarce, Gondwanic fossil record. The six currently recognized living species (Table 1) include a pair of close relatives in each of three areas: Papuasia and Melanesia excluding New Caledonia, New Caledonia itself, and tropical South America (Mill, 2016). Per its name, Retrophyllum is readily identified from its oppositely twisted “flip-leaved” foliage (e.g., Page, 1989; Figs. 1–3, 5). The genus is widely used in studies of the biogeographic 1

Manuscript received 28 April 2017; revision accepted 7 August 2017. Department of Geosciences, Pennsylvania State University, University Park, Pennsylvania 16802, USA; 3 Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20013, USA; 4 Museo Paleontológico Egidio Feruglio, Consejo Nacional de Investigaciones Científicas y Técnicas, Trelew 9100, Chubut, Argentina; and 5 Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853, USA 6 Author for correspondence (e-mail: [email protected]) https://doi.org/10.3732/ajb.1700158 2

and paleoclimatic history of Gondwanan rainforests (Brodribb and Hill, 2004; Carpenter et al., 2012; Kooyman et al., 2014; Merkhofer et al., 2015). The Retrophyllum species are physiologically constrained to require very wet conditions (Brodribb and Holbrook, 2006; Brodribb, 2011; Brodribb et al., 2014); they inhabit a range of humid environments, from lowland rainforest to cloud forest, and can play significant hydrological roles (Jaffré, 1995; Ataroff, 2002; Farjon, 2010; Mill, 2016). The genus includes the rheophytic, small-statured, and endangered R. minus, from low elevations of New Caledonia (de Laubenfels, 1972; Jaffré, 1988; Jaffré et al., 1998, 2010), as well as the tall (to 50 m) Andean timber tree R. rospigliosii (Gray and Buchholz, 1948; de Laubenfels, 1982, 1991; Vicuña-Miñano and Mostacero León, 2003; Veblen et al., 2005). Retrophyllum is unique among all living conifers in having distichous, pectinate juvenile foliage and, in most of its species, adult foliage (Table 1 and references therein) that twists (“flips”) ~90° counterclockwise in relation to the twig at departure, such that the bifacially flattened, opposite leaves deploy in a single plane (Fig. 1).

1344 • A M E R I C A N J O U R N A L O F B OTA N Y 104(9): 1344–1369, 2017; http://www.amjbot.org/ © 2017 Wilf et al. Published by the Botanical Society of America. This work is licensed under a Creative Commons Attribution License (CC-BY-NC).

S E P T E M B E R 2017 , V O LU M E 104

• W I L F E T A L. — S O U T H A M E R I C A N R E T R O P H Y L LU M F O S S I L S

• 1345

FIGURES 1–9 Selected Retrophyllum herbarium material for comparison to fossils. 1. R. filicifolium, showing typical distichous leaf deployment with extensively clasping, overlapping and zigzagging leaf bases and heterofacially flattened free portions (adaxial view). Compare, for example, Figs. 10–17, 90–94, 98, 103. Papua New Guinea, CANB 00518747. 2. R. rospigliosii, showing distichous foliage, immature pollen-cone clusters in leaf axils, and two large peduncles bearing distichous groupings of long-cylindrical, pedicellate, mature pollen cones subtended by narrow, leafy bracts. Compare Figs. 61–72. Perú, R.T. Pennington 1433 (E), photo courtesy of R. R. Mill. 3. R. vitiense, distichous foliage and compound branches bearing pollen cones. Fiji, K 000289118. 4. R. minus, decussate mature foliage with moderate basal twisting of leaves (compare Figs. 39, 40) and distal set of axillary and terminal pollen cones. New Caledonia, CANB 00504516. 5. R. minus, distichous juvenile foliage. Compare Figs. 90–94. New Caledonia, K 000289144. 6. R. minus, leaf from a decussate shoot, showing continuous rows of stomata across the blade and two ridges marking the dried edges of the broad, thick central band of transfusion tissue. Compare Figs. 48–54, 92, 96. New Caledonia, US 1372441. 7. R. minus, shoots of ovoid scale leaves;

1346

•

A M E R I C A N J O U R N A L O F B OTA N Y

Accordingly, the leaves are heterofacially oriented, such that all leaves on the left side of the twig (when viewed from above toward the distal direction, as in Fig. 1) have the abaxial surface facing the sun, and all the opposing leaves display the adaxial surface (Florin, 1940b; Hill and Pole, 1992; Brodribb and Hill, 1999a; Eckenwalder, 2009; Farjon, 2010; Mill, 2016). In all other podocarps with twisted and flattened foliage, such as Afrocarpus (J. T. Buchholz & N. E. Gray) C. N. Page, opposing leaves twist in opposite directions in relation to the twig, and the same surface faces the sun on either side (e.g., Hill and Pole, 1992; Brodribb and Hill, 1999a). Retrophyllum leaves extensively clasp the twig before departure and are single-veined and amphistomatic, with no interruption of the stomatal rows by the midvein and prominent to sunken Florin rings (de Laubenfels, 1953; Gray, 1962; Stockey and Ko, 1988; Hill and Pole, 1992; Farjon, 2010). The rows of stomata extend across the full leaf surface without concentration into stomatal bands and are separated by well-marked longitudinal striations (Figs. 6, 9; Mill, 2016). Most of the Retrophyllum species have multiple foliage forms, including a variety of reduced leaves (scales, bracts) that occur at shoot bases, at growth-increment divisions, on separate shoots, and elsewhere (Figs. 7, 8; Table 1 and references therein). Mature foliage of New Caledonian R. comptonii and R. minus can be fourranked opposite-decussate and minimally or negligibly twisted at the base, always so in adult R. minus (Fig. 4). In addition, leaves of these species feature a thickened central longitudinal band consisting of wings of transfusion tissue that extend from and obscure the true midvein; in dried specimens, the edges of the band may remain raised around the deflated central portion (Figs. 6, 9; Gray, 1962; de Laubenfels, 1969, 1972). Other Retrophyllum species have similarly placed but far less conspicuous transfusion tissue (Bertrand, 1875; Orr, 1944; Gray and Buchholz, 1948). The transfusion tissue facilitates lateral sap transport from the single midvein in the absence of secondary veins, in a manner similar to that of other broad-leaved, single-veined podocarps (Brodribb and Holbrook, 2005; T. Brodribb, personal communication). The trade-off for this adaptation is that the tissues are vulnerable to water transport failure during droughts (Brodribb, 2011; Brodribb et al., 2014). Retrophyllum is dioecious and produces pedunculate seed cones. The pollen cones (Figs. 2–4), which are poorly understood, can be sessile or pedicellate, and ellipsoid or cylindrical in shape (Mill, 2016). They occur solitarily or in a variety of groupings on simple or compound peduncles (Table 1 and references therein); each cone is usually subtended by reduced leaves and has ovate or triangular microsporophylls with acute or apiculate apices. The complex nomenclatural history of Retrophyllum was recently detailed in the comprehensive monograph of Mill (2016). To date, no phylogenetic analysis has included all six living Retrophyllum species. However, those that sampled a majority of the taxa are consistent with Mill’s (2016) three geographic pairs of closely related species and resolve South American R. rospigliosii as sister to a clade comprising the Old World species (Herbert et al., 2002; Sinclair et al., 2002; Leslie et al., 2012). The closest relatives of Retrophyllum

are Afrocarpus, from Africa, and Nageia Gaertn. from South and Southeast Asia (Page, 1989). These three genera together form a clade that is sister to Podocarpus L’Hér. ex Pers., and all four genera form the podocarpoid clade (Conran et al., 2000; Sinclair et al., 2002; Biffin et al., 2012; Knopf et al., 2012; Leslie et al., 2012). Molecular dating estimates have mostly placed the crown node of the entire podocarpoid clade in the Cenozoic (Biffin et al., 2011, 2012; Crisp and Cook, 2011; Leslie et al., 2012, 2017); however, Quiroga et al. (2016; see Discussion) placed this node in the Late Cretaceous. The prior macrofossil record of Retrophyllum is scarce, located far to the south of today’s distribution, and restricted to the Cenozoic (Florin, 1940b; Hill and Pole, 1992; Brodribb and Hill, 1999a; Mill, 2016). To date, all described fossil material has consisted of leafy branches with the classic flip-leaved, pectinate phyllotaxy. From southern Chile, Berry (1922) described “Araucaria” araucoensis Berry from the Eocene Concepción-Arauco Coal Measures (Collao et al., 1987; Kuhn et al., 2010). Florin (1940b) revised those specimens as Podocarpus araucoensis (Berry) Florin of Podocarpus Section Polypodiopsis C. E. Bertr., which is now a synonym of Retrophyllum. However, the fact that Florin (1940b) and subsequent workers never examined the type material, along with other significant issues (see Remarks, Retrophyllum araucoensis comb. nov.), has until now precluded stable nomenclature for the Chilean fossils. In Australasia, R. australe R. S. Hill & Merrifield (1993), from the middle Eocene–Oligocene West Dale flora of southwestern Australia, and R. vulcanense Pole (Pole, 1992, 1997, 2007), from the early Miocene Manuherikia Group of New Zealand’s South Island, are each represented by several foliage-shoot segments with cuticle. Retrophyllum foliage was also reported from additional Manuherikia Group sites (Pole et al., 2008) and the early Eocene Lowana Road site, western Tasmania (Carpenter et al., 2012). In addition, Hill and Pole (1992) introduced two extinct podocarp genera from Paleogene sites in Australia, based on heterofacially flattened foliage with distinctive cuticular micromorphology: Smithtonia R. S. Hill & Pole (Anglesea, Victoria, and Little Rapid River, Tasmania) and Willungia R. S. Hill & Pole (Maslin Bay, South Australia, and Little Rapid River). From the Cenozoic Lightning Ridge locality of New South Wales, Carpenter et al. (2011) reported branches with heterofacially flattened foliage as “Retrophyllum/Smithtonia/Willungia sp.” New fossils of Retrophyllum hold significant interest because of the Old–New World disjunction in the extant genus. Earlier works presciently invoked ancient land connections and Antarctic history to explain the distributions of Retrophyllum and other podocarps (Hooker, 1853; Florin, 1940b, 1963; Buchholz and Gray, 1948), and the genus remains central in evolutionary biogeographic hypotheses (Pole, 2001; Contreras-Medina and Luna Vega, 2002; Knopf et al., 2012; Leslie et al., 2012; Kooyman et al., 2014; Quiroga et al., 2016). The 82 new Eocene Retrophyllum fossils described here (Figs. 10–80) from the early Eocene Laguna del Hunco and early/middle Eocene Río Pichileufú fossil sites in Patagonian Argentina (Berry, 1925, 1938; Wilf et al., 2003, 2005) are the first for this genus to

←

portions of regular leaves at top for size comparison. Compare Figs. 55–57. New Caledonia, University of Illinois Herbarium (ILL) 00010022, used with ILL permission via JStor Global Plants, plants.jstor.org/stable/10.5555/al.ap.specimen.ill00010022. 8. R. filicifolium, cluster of leading shoots with narrow, miniature leaves; portions of regular leaves at top and bottom left for size comparison. Compare Figs. 58–60. New Guinea (Papua, Indonesia), CANB 319115. 9. R. comptonii, leaf from a distichous shoot, showing rows of stomata alternating with typical longitudinal striations and midvein obscured by the thickened transfusion-tissue band (usually narrower in this species than in R. minus, per Fig. 6). Compare, for example, Figs. 13, 15, 50, 92, 103. New Caledonia, E 00137222 (composite image).

Notes: Extant species data primarily from Mill (2016), combined with several additional sources (Gray and Buchholz, 1948; Gray, 1962; de Laubenfels, 1969, 1972; Silba, 1983; de Laubenfels, 1991; Farjon, 2010) and authors’ observations. All measurements in millimeters; extreme measurements omitted; leaf dimensions from free portion of blade only, usually recorded for fossils as the largest nearly complete leaf on a shoot. Other fossil species considered in the present study are not included here because of limited character preservation and space limitations (see text for descriptions). Abbreviations: 4r = 4-ranked; a = adult; abax. = only visible abaxially; ac = acute; acm = acuminate; band–margin = distance from band edge to margin; comp = compound; cyl = cylindrical; dist = distichous; e = elliptic/ellipsoid; j = juvenile; l = lanceolate; ls = leading shoots of reduced foliage; mod. = modified; mx = mixed along shoots with regular leaves; obov = obovate; obt = obtuse; sb = shoot bases below regular leaves; sr = subrounded; ss = other shoot segments with scale/reduced foliage.

ovoid to cyl 5–12 × 2.5 n/a n/a e or cyl 10–25 × 2–2.5 cyl 12.5–20 × 2.6–3.3

cyl 10–25 × 2–2.5

e or short-cyl 4–6 × 2.5–3

e or short-cyl 4–8 × 2–3

dist on peduncle n/a axillary, branch tips comp branches

Shape Apex Pollen cones Arrangement when in groupings > 3–5 cones Shape, mature cones Length × width

dist on peduncle

comp branches

axillary, branch tips

n/a (j), e (a) n/a (j), ac-slightly acm (a)

yes, or abax. none n/a yes rare no dist 15–23 × 3–6 (j), 7–14 × 3–5 (a) l, e ac (j); ac, acm (a) yes none n/a yes rare no unknown (j), dist (a) n/a (j), 9.5–11 × 2–2.5 (a)

yes, or abax. bud scales n/a no ls no dist 18–40 × 4.2–6 (j), 7–25 × 3–4.5 (a) l (j), e (a) ac–slightly acm (j), ac–sr (a) no mod. leaves ≤ band–margin yes sb, mx, ls, ss yes dist or helical 8–18 × 1.6–3.1 (dist), 8–14 × 1.2–2.6 (helical) l, e (dist); e, l (helical) ac–markedly acm

yes, or abax. bud scales n/a no ls no dist 18–40 × 4.2–6 (j), 16–27 × 3.2–6 (a) l ac, obt

no mod. leaves < band–margin no ls, sb, ss yes dist (j), dist or 4r (a) 20–35 × 2.5 (j), 6–15 × 2–5 (a) l, e ac (j); ac, obt, sr (a)

no mod. leaves usually ≥ band–margin no sb, ss yes dist (j), 4r (a) 25–33 × 2.8–4 (j), 10–20 × 3.5–5.5 (a) e, l ac, obt (j); ac, obt, sr (a)

Bolivia to Venezuela W Brazil New Caledonia Fiji & Solomons New Guinea & Moluccas Patagonia, Eocene

Range Sterile foliage Midvein visible Terminal bud protection Central band width Lateral resin canals Reduced leaf location Ovoid reduced leaves Phyllotaxy Length × width

Character

New Caledonia

R. piresii (Silba) C. N. Page R. minus (Carrière) C. N. Page R. comptonii (J. T. Buchholz) C. N. Page R. vitiense (Seem.) C. N. Page R. filicifolium (N. E. Gray) R. R. Mill Retrophyllum spiralifolium Wilf sp. nov.

TABLE 1. Retrophyllum spiralifolium sp. nov., general features compared to the six living Retrophyllum species.

R. rospigliosii (Pilg.) C. N. Page



• 1347

include pollen cones as well as a rich variety of foliage forms and insect damage. This preservation allows comparisons with the living species (Figs. 1–9, 81–89; Table 1) in far more detail than was previously possible. Laguna del Hunco and Río Pichileufú both contain diverse plant lineages that are now extinct in South America but survive in Australasia and Southeast Asia, primarily in subtropical and montane-tropical rainforests (e.g., Wilf et al., 2013; Kooyman et al., 2014; Table 2). This pattern demonstrates biotic connections through Antarctica to Australia while the final stages of Gondwana coincided with Eocene global warmth (e.g., Zachos et al., 2008; Lawver et al., 2011). Few taxa from these Patagonian fossil floras are, like Retrophyllum, extant in both South America and Australasia (see Materials and Methods). We also present the first Mesozoic Retrophyllum fossil (Figs. 90–96), from the terminal Cretaceous (last 1 Myr) portion of the Lefipán Formation (Barreda et al., 2012a; Scasso et al., 2012), also in Patagonian Argentina. The presence of Retrophyllum in latest Cretaceous strata provides a critical new record of Cretaceous–Paleogene (K–Pg) plant survival in southern latitudes and extends the known history of the genus significantly back in time.

MATERIALS AND METHODS Laguna del Hunco and Río Pichileufú are located in caldera-fill lacustrine deposits of the Eocene La Huitrera Formation, respectively exposed in northwestern Chubut and western Río Negro provinces in Patagonia, Argentina (Berry, 1925, 1938; Petersen, 1946; Aragón and Romero, 1984; Aragón and Mazzoni, 1997; Iannelli et al., 2017). There has been a dramatic increase in paleontological research on these deposits over the past 15 yr, involving fossil insects and vertebrates as well as plants, as reviewed elsewhere (Wilf et al., 2009, 2013, 2014). Laguna del Hunco has a 170 m stratigraphic section that has produced two paleomagnetic reversals and three 40Ar-39Ar ages analyzed from tuffs that are intercalated stratigraphically with 28 distinct fossil quarries, LH01–LH28, as previously described and georeferenced (Wilf et al., 2003, 2005; Gandolfo et al., 2011; excepting LH28, a gully exposure located near LH27). The most reliable 40 Ar-39Ar age is 52.22 ± 0.22 Ma (analytical 2σ), based on sanidines analyzed from a sample taken from the middle of the main fossiliferous interval (ash sample LH2211A of Wilf et al., 2003); the other radiometric ages are on plagioclase and have similar means at lower precision (Wilf et al., 2003, 2005, 2017; Wilf, 2012). Accordingly, we use 52.2 Ma (early Eocene, Ypresian) as a working age for the entire Laguna del Hunco flora. Additional locality data for Laguna del Hunco are available from P.W. or from MEF (Museo Paleontológico Egidio Feruglio, Trelew, Chubut, Argentina) collections staff. At Río Pichileufú, the 40Ar-39Ar age analyzed from sanidines in three tuffs closely associated with three fossil quarries (quarries RP1–RP3 of Wilf et al., 2005) is 47.74 ± 0.05 Ma (analytical 2σ; Wilf et al., 2005; Wilf, 2012). The age of the Ypresian/Lutetian (early/ middle Eocene) boundary is currently 47.8 Ma (Gradstein et al., 2012, updated at http://www.stratigraphy.org). Thus, the age of the Río Pichileufú flora, conservatively, is indistinguishable from that of the early/middle Eocene boundary. Additional data for the Río Pichileufú sites are available from P.W. or from BAR (Museo de Paleontología de Bariloche, San Carlos de Bariloche, Río Negro, Argentina) collections staff. Angiosperms account for the majority of plant diversity at Laguna del Hunco and Río Pichileufú, but the conifer taxa from these sites

1348

•


(Table 2) are also speciose and abundant (Wilf et al., 2005). These conifer fossils provide substantial primary evidence for the interpretation of Eocene Patagonia as the westernmost extremity of a belt of tall-statured, mixed conifer–angiosperm rainforests that extended across Antarctica to Australia (e.g., Wilf et al., 2009, 2013; Wilf, 2012; Kooyman et al., 2014). Fossil Agathis, Araucaria Section Eutacta, Papuacedrus, Acmopyle, Dacrycarpus, Phyllocladus (preliminary identification), Podocarpus, and the here-treated Retrophyllum are found together on single bedding planes at the Patagonian sites. They also co-occur in various subsets at many fossil localities in Australia and New Zealand (e.g., Hill, 1995; Brodribb and Hill, 1999a; Kooyman et al., 2014) and today in cool–wet rainforests across Australasia and Southeast Asia (e.g., Gibbs, 1917; Wasscher, 1941; de Laubenfels, 1969; Beaman and Beaman, 1993; Farjon, 2005, 2010). Of these fossil conifers (Table 2), only Podocarpus and Retrophyllum persist together in South American associations (VicuñaMiñano and Mostacero León, 2003; Veblen et al., 2005). The angiosperm Orites bivascularis (Berry) Romero, Dibbern & Gandolfo (Proteaceae, Laguna del Hunco) and the fern Dicksonia patagonica Berry (Dicksoniaceae, both floras) are additional, rare examples of survival of their respective genera in both South America and Australasia (Berry, 1938; Romero et al., 1988; González et al., 2007; Carvalho et al., 2013). As with the conifers, the predominant survival pattern for ferns and angiosperms in the Laguna del Hunco and Río Pichileufú floras is East Gondwanan (Romero and Hickey, 1976; Zamaloa et al., 2006; Gandolfo et al., 2011; Hermsen et al., 2012; Carvalho et al., 2013; Knight and Wilf, 2013; Carpenter et al., 2014; Kooyman et al., 2014; Gandolfo and Hermsen, 2017). However, a few angiosperm taxa have been described with modern biogeographic affinities outside of Australasia. From Laguna del Hunco, these include fruits of the characteristically Laurasian family Juglandaceae (Hermsen and Gandolfo, 2016) and lantern fruits of Solanaceae that belong to the entirely New World genus Physalis L. (Wilf et al., 2017). From Río Pichileufú, the spectacular capitulum Raiguenrayun cura Barreda, Katinas, Passalia & Palazzesi has affinities with both South American and African basal lineages of Asteraceae (Barreda et al., 2010, 2012b). The Gondwanic character of Patagonian floras drastically diminished after the middle Eocene as a result of large-scale extinctions that accompanied Antarctic separation and cooling climates, while Australasia provided a refuge for many taxa (Hill, 1994; Palazzesi and Barreda, 2007; Barreda and Palazzesi, 2010; Kooyman et al., 2014). The Lefipán Formation is a suite of deltaic deposits from a paleoAtlantic embayment in northwestern Chubut that is exposed close to Laguna del Hunco (Scasso et al., 2012; Vellekoop et al., 2017). The single Lefipán Formation fossil considered here (Figs. 90–96) comes from the Cretaceous LefE (= PLE) locality in the San Ramón section of Scasso et al. (2012), which crops out to the southeast of the Laguna del Hunco exposures. The LefE site is a laterally extensive tidal-channel deposit preserving numerous, diverse, compressed plant fossils (e.g., Donovan et al., 2016). The fossiliferous horizon is located 21.5 m stratigraphically below the Danian Turritella marker bed (Donovan et al., 2016). Our handheld GPS trace along the main productive exposure of the LefE bed extended ~40 m along strike on a 108° bearing, from S 42.68366°, W 69.83430° to S 42.68378°, W 69.83382° (WGS 1984 datum). Biostratigraphic data from dinoflagellates, palynomorphs, and marine invertebrates collectively place the locality within the last 1 Myr of the Maastrichtian,

67–66 Ma (Medina et al., 1990; Barreda et al., 2012a; Scasso et al., 2012; Aberhan and Kiessling, 2014; Vellekoop et al., 2017). The K–Pg boundary clay is not preserved in the area, because of bioturbation or regression (Scasso et al., 2012; Vellekoop et al., 2017). The significance of the Lefipán Formation for studies of the K–Pg extinction in Gondwana is considerable. Its palynological data, including the podocarpaceous component, show a relatively muted extinction and rapid rebound of palynomorph composition and diversity across the K–Pg (Barreda et al., 2012a). Fossil molluscs from the same formation indicate significant ecological shifts and severe extinction in nearshore environments, contrasted with a rapid recovery in offshore facies (Scasso et al., 2012; Aberhan and Kiessling, 2014). The oldest therian mammal from South America, Cocatherium lefipanum, was recovered from the Danian portion of the formation (Goin et al., 2006). Diverse, heretofore undescribed compression macrofloras, including the Retrophyllum specimen treated here, have recently been recovered from several beds in the uppermost Cretaceous portion of the Lefipán (Scasso et al., 2012). Donovan et al. (2016) recently examined the insect-feeding damage on angiosperm leaves from these Lefipán floras and their Danian counterparts in the Salamanca and Peñas Coloradas formations of southern Chubut, finding a severe extinction but rapid recovery of Patagonian insect herbivores. The fossil material from Argentina reported here (Figs. 10–96) was collected during several expeditions launched from MEF from 1999 to 2016 and totals 83 specimens: 74 from the Laguna del Hunco main section of Wilf et al. (2003); four from locality AL1, 5 km to the south of the main Laguna del Hunco exposures (see Wilf et al., 2014); four from Río Pichleufú quarry RP3; and one from Lefipán quarry LefE. The Laguna del Hunco and Lefipán material, from Chubut Province, is housed at MEF (repository acronym MPEF-Pb), and the fossils from Río Pichileufú, Río Negro Province, are deposited at BAR; letter suffixes (a, b) indicate parts and counterparts. There are no relevant type or historical specimens to consider for the Argentine material. The type specimens of “Araucaria” araucoensis from Chile, illustrated photographically here for the first time (Figs. 97–104), were collected by E. W. Berry (1922) and are housed in the Paleobotanical Division of the National Museum of Natural History, Smithsonian Institution (USNM). Florin’s (1940b) illustrations of the Podocarpus araucoensis material housed at the Swedish Museum of Natural History, Stockholm (S; Dusén and Halle collections), are very detailed, and we did not physically examine this material. Updated catalog information from S was kindly provided by S. McLoughlin (personal communication). Fossils were manually prepared using air scribes and other hand tools as needed, then examined and photographed at MEF and the Penn State Paleobotany Laboratory using DSLR macrophotography, reflected light microscopy, and epifluorescence microscopy. Imaging was done using the same equipment, methods, and software that were detailed in related studies (Wilf et al., 2009, 2014; Wilf, 2012). The Chilean type specimens are extremely fragile and were not manually prepared. Herbarium specimens of all six extant Retrophyllum species were examined and photographed at the Australian National Herbarium, Canberra (CANB); National Herbarium of New South Wales, Royal Botanic Gardens, Sydney (NSW); U.S. National Herbarium, Smithsonian Institution, Washington, D.C. (US); L.H. Bailey Hortorium Herbarium of Cornell University (BH); Harvard University Herbaria; Royal Botanic Garden Edinburgh Herbarium (E); and Royal Botanical Gardens, Kew (K). Other high-resolution images were



• 1349

1350

•


downloaded from several virtual herbaria, principally including JStor Global Plants (http://plants.jstor.org, a consortium site involving herbaria around the world not separately listed here) and the online herbarium catalogs of E (http://elmer.rbge.org.uk/bgbase/ vherb/bgbasevherb.php), K (http://apps.kew.org/herbcat/navigator. do), and Muséum National d’Histoire Naturelle, Paris (P; http:// science.mnhn.fr/institution/mnhn/collection/p/item/search/form). Images of fossils and herbarium sheets were extensively annotated in Adobe Bridge (San Jose, California, USA) to allow rapid comparisons and filtering, using a common keyword set to index informative morphological characters. A full-resolution image archive of the fossil specimens, going far beyond the coverage that can be shown in this article space, has been deposited open-access at http://figshare.org (Wilf, 2017). The accumulated set of >550 herbarium-sheet images is available from P.W. on request. For a systematic framework and as the starting point for interpreting morphological characters, we followed Mill’s (2016) recent monograph of Retrophyllum. Morphological data were also compared among several additional literature sources (Gray and Buchholz, 1948; Gray, 1962; de Laubenfels, 1969, 1972, 1991; Silba, 1983; Farjon, 2010) and verified on herbarium sheets. We did not attempt a phylogenetic analysis because of the incomplete genetic and morphological data availability for the living Retrophyllum species. Several other research groups (as cited in the Introduction) are undertaking comprehensive phylogenetic analyses of Podocarpaceae and are likely to provide improved frameworks to include the fossils in a phylogenetic context in the near future. Full-sized foliage is referred to here as “principal” or “regular” to avoid unverifiable statements about juvenile vs. adult foliage or leading vs. lateral shoots in the fossils. Similarly, miniaturized fossil foliage is mostly referred to here as “reduced” to eliminate confusion over the uncertain application to these fossils of the terms “scale leaves,” “bracts,” and “reduced leaves.” To categorize insectfeeding damage on fossil leaves, we assigned damage types (DTs) using Labandeira et al. (2007).

SYSTEMATICS Family—Podocarpaceae Endlicher, Synopsis Coniferarum: 203

(Endlicher, 1847). Genus—Retrophyllum C. N. Page, Notes of the Royal Botanic Gar-

den of Edinburgh 45: 379 (1989 [‘1988’, see Mill, 2016]). Species—Retrophyllum spiralifolium Wilf, sp. nov. Specific diagnosis—Foliage with conspicuous central longitudinal band of thickened tissue and obscure midvein not separating rows of stomata. Lateral resin canals present. Principal leaves decurrent and extensively clasping twig, free portions either distichous and

pectinate, with full heterofacial flattening, or spirally deployed with negligible to slight basal twisting, frequently broken off to leave spirally arranged stubs of clasping portions. Leaf apices acuminate to markedly acuminate. Terminal bud protected by reduced, modified leaves. Reduced foliage also including ovoid and narrow forms on separate shoot segments and narrow miniature leaves abruptly or gradually interspersed with principal leaves along shoots. Pollen cones pedicellate, long-cylindrical, in axils of narrow reduced leaves, distichously grouped on a common peduncle. Holotype here designated—MPEF-Pb 8911 (Figs. 19, 32–34, 50– 52, 76), part and counterpart of a branch with helical foliage from Laguna del Hunco, Tufolitas Laguna del Hunco, La Huitrera Formation, early Eocene, northwest Chubut Province, Argentina, quarry LH6 of Wilf et al. (2003), collected 22 November 1999. Paratypes—Laguna del Hunco, La Huitrera Formation, early Eocene, northwest Chubut Province, Argentina. Branches with distichous foliage: MPEF-Pb 8912–8914 (quarry LH4); 8915 (LH6); 8916–8918 (LH13); 8919 (LH27). Branches with helical foliage: MPEF-Pb 8920, 8921, 8981, 8982 (AL1); 8922 (LH5); 8923–8932 (LH6); 8933 (LH13); 8934 (LH14); 8935–8939 (LH15); 8940 (LH22); 8941–8945 (LH25); 8946–8968, 8983–8988 (LH27); 8969, 8970 (LH28); 8971, 8972 (float). Branches solely with reduced foliage: MPEF-Pb 8973 (LH4); 8974, 8975 (LH6); 8976, 8978, 8979 (LH25); 8977 (LH27). Peduncle bearing pollen cones: MPEF-Pb 8980 (LH27). Río Pichileufú, La Huitrera Formation, early/middle Eocene, Río Negro Province, Argentina. Branches with distichous foliage: BAR 4705, 4753–4755 (quarry RP3). Etymology—The species epithet reflects the distinctive spiral deployment of leaves in the foliage form represented by the holotype. Description—Branching is opposite, with the leafy branches deployed distally on penultimate branches (Figs. 10–12, 20–25, 28, 30). Foliage on vegetative shoots is polymorphic, consisting of both distichous (Figs. 10–17) and helical (Figs. 19–41) arrangements of the principal leaves and several types of reduced foliage at shoot bases (e.g., Figs. 19–21, 26, 29, 32); mixed with principal leaves along shoots (e.g., Figs. 19, 27, 34); or on extended twig segments with no principal leaves (Figs. 55–60). All foliage is amphistomatic, with a central, longitudinal band of thickened tissue that obscures the true midvein. The band is often coalified and easily visible as a black stripe of total width from a fifth to a third of total leaf width (i.e., usually less than the distance from the band to the margin; Figs. 13, 33, 50, 57). On the helical foliage form, possibly due to greater original thickness than on the other foliage types, the band may preserve numerous longitudinal rows of coalified stomata (probably coalified Florin rings); the stomatal rows are not interrupted by the midvein (Figs. 48–54). Stomata outside the central band are not preserved, but parallel longitudinal striations presumed to border

←

Retrophyllum spiralifolium sp. nov., distichous foliage form. Numbered arrows indicate crossover points to detail panels, which may show counterparts in mirror orientation that have slight differences in preservation. Figs. 1–16, Laguna del Hunco. Figs. 17, 18, Río Pichileufú. 10–13. Large penultimate branch segment with opposite branch scars (Fig. 10 and inset, as marked by arrows); terminal cluster of leafy branches; potential remains of other branches (not confirmed as attached); linear to slightly expanded reduced foliage at shoot bases (Figs. 11, 12); and longitudinal foliar striations, thickened central band, and trace of midvein or resin canal within the band (Fig. 13). MPEF–Pb 8915a (Figs. 10, 11, 13), 8915b (Fig. 12). 14. MPEF-Pb 8913, with colorful mineral replacement typical of fossil leaves at locality LH4. 15, 16. MPEF-Pb 8917a, showing large, lanceolate, acuminate leaves, hole feeding, and extensive margin feeding. 17. BAR 4705a. 18. BAR 4705b. FIGURES 10–18



• 1351

1352

•


the former stomatal rows are present across the leaf in all foliage types and not concentrated into stomatal bands; the course of the striations is mostly more obtuse than the midvein and margin, recurving admedially toward the apex (e.g., Figs. 13, 45, 50). Epidermal cells are elongate, rectangular to trapezoidal, with irregular length and arranged in longitudinal rows (Fig. 46). Resin canals number at least three by symmetry, based on the frequent ambercast preservation of medial canals (Fig. 43) and a fortuitously preserved lateral canal set well inside the margin (Fig. 44). Distichous principal foliage (Figs. 10–17, 43) is deployed in opposite pairs, pectinate, and decurrent, and extensively clasps the twig along the internodes so that opposing leaf bases overlap in a zigzag pattern then twist ~90° heterofacially at departure into a common plane. Adjacent leaves on the same side of a branch do not overlap or very slightly overlap. Leaf shape is ovate-lanceolate to elliptic, the apex sharp-acute to markedly acuminate. Leaf size is variable, smoothly diminishing into reduced, scale-like or linear leaves at shoot bases; length of the free portion of the blade ranges up to 17.7 mm, width to 3.1 mm, length:width 3.6–8.6:1. Whether abaxial (or adaxial) leaf surfaces faced upward on the left or the right side of the twig in life, and thus abaxial vs. adaxial view, cannot be determined in the compression fossils due to the puzzle presented by amphistomy, unknown positions of xylem and phloem (see Gray and Buchholz, 1948), unknown original position in the sediment, and the mirror-image parts and counterparts. Helical principal foliage (Figs. 19–42, 44–54) is imbricate and decurrent and extensively clasps the twig. Leaves are not twisted to moderately twisted (Figs. 39, 40) at twig departure and arranged in four to eight or more leaves per cycle. The free portions of the leaves are often broken off preservationally to leave behind the spirally arranged stubs of the clasping portions (e.g., Figs. 35–38). Leaf shape is ovate-lanceolate to elliptic, the apex markedly acuminate (e.g., Figs. 47, 50). The length of the free portion is to 14.2 mm, the width to 2.6 mm, and length:width 4.1–8.9:1. Reduced leaves are scale-like to linear at the branch base (e.g., Figs. 21, 32); expand distally abruptly or intergrade with the principal leaves (e.g., Fig. 21); or are mixed along the shoot with the principal leaves, with abrupt or gradual size variation often not associated with growth increments (e.g., Figs. 27, 34). The terminal bud is protected by a cluster of apically directed, reduced leaves, their apices either symmetrical or asymmetrical, with straighter margins on the side closest to the twig axis (Figs. 41, 42). Reduced foliage occurs on principal foliage shoots, as described above, or distichously on heterofacially flattened shoot segments with no principal leaves present. On these segments, the reduced leaves are either short-elliptic to ovoid (Figs. 55–57), with the length of the free portion to 5.5 mm, width to 1.9 mm, and length: width 2.2–3.5:1; or narrow and miniaturized (Figs. 58–60), with leaf attachment alternate, length to 2.1 mm, width to 0.7 mm, and length:width 3.0–4.1:1.

Pollen cones (Figs. 61–72) are arranged on an unbranched peduncle with a nearly complete axis measuring 52 mm by 1.8 mm, via the partially overlapping part and counterpart (see Figs. 63, 64). The peduncle (Figs. 61, 62, 69) bears at least 13 long-cylindrical to slightly ellipsoid, distichous, alternate to subopposite, pedicellate cones that are irregularly spaced but not clustered. Each cone is laterally inserted in the axil of a reduced, narrow subtending leaf. Reduced leaves without accompanying cones are present basally and apically on the peduncle, or possibly the apical leaf subtends the broken base of a terminal cone pedicel. Subtending leaves (Figs. 67, 68) have free portion length to 6.5 mm, width to 1.1 mm, and length:width 5.0– 8.5:1. They clasp the twig extensively, then twist slightly at departure (Fig. 70), and feature a thick central band, a medial resin duct (Fig. 68), and longitudinal striations as in the leaves of vegetative shoots; their apices are acute, not acuminate. Pedicels are stout, with length to 3.2 mm, and expand in width below the cone body. Cone body length ranges to 20 mm, width to 3.3 mm, length:width (based on 2 most complete cones) 4.0–7.7:1. Microsporophylls are helically arranged, numerous (preservation not allowing precise count), and triangular to wide-ovate, the distal margin subround with an acuminate apiculus (Figs. 71, 72). Pollen sacs and pollen are not preserved. Remarks, Retrophyllum spiralifolium sp. nov—Retrophyllum

spiralifolium sp. nov. is the first fossil Retrophyllum species that preserves a rich suite of characters, allowing comparisons with the extant taxa (Table 1). The various organs have not been found in organic attachment. Nevertheless, all the foliage forms, including the distichous and helical regular leaves along with the various types of reduced leaves, share distinctive features of the extant genus Retrophyllum (per references to Table 1); these especially include extensive decurrence along the twig, slight to full heterofacial twisting and flattening at twig departure, presence of ovate and lanceolate leaves, well-marked longitudinal striations, a thickened central band presumed to represent wings of transfusion tissue, amphistomy, and nonseparation of the stomata across an obscure midvein (well preserved in the helical foliage). Apart from their spiral insertion, the helical and distichous foliage only substantively differ in the slightly smaller size of the helical leaves (e.g., Table 1). The configuration of the fossil peduncle with pollen cones is also typical of Retrophyllum (e.g., Mill, 2016), including pedicellate cones with ovate-triangular and acuminate microsporophylls, the cones axillary to reduced leaves having the same characteristic features as the other foliage forms. Based on these shared features and the closely comparable variation that typifies living Retrophyllum species (Table 1), we find it far more likely that all these components represent the natural variation of a single species and not the homogeneous remains of several. The new species brings many novel features to the fossil record of Retrophyllum involving its spiral phyllotaxy, reduced foliage, and axis of pollen cones, clearly justifying the new species designation.

←

Retrophyllum spiralifolium sp. nov., helical foliage form, Laguna del Hunco and AL1 locality (Fig. 25). Specimens show opposite branching, spirally deployed leaves and broken stubs of detached leaves, coalified central bands of transfusion tissue, acuminate apices, and reduced leaves both at shoot bases and mixed with regular leaves along the shoots. 19. Holotype, MPEF-Pb 8911a (also Figs. 32–34, 50–52, 76). 20. MPEF-Pb 8951b. 21. MPEF-Pb 8956a (also Figs. 53, 54), with an unidentified weevil (Curculionidae) species at upper right. 22. MPEF-Pb 8969a (also Fig. 44). 23. MPEFPb 8931a. 24. MPEF-Pb 8926, covered with piercing-and-sucking marks of scale insects along the transfusion-tissue bands (also Fig. 73). 25. MPEF-Pb 8921 (also Figs. 36, 37). 26. MPEF-Pb 8925a. 27. MPEF-Pb 8940b (also Figs. 47, 77, 78). 28. MPEF-Pb 8970a. 29. MPEF-Pb 8923 (also Fig. 40). 30. MPEF-Pb 8944a, with terminal bud area preserved at left (also Fig. 42). 31. MPEF-Pb 8971, longitudinally compressed specimen showing spiral leaf deployment. FIGURES 19–31



• 1353

FIGURES 32–42 Retrophyllum spiralifolium sp. nov., helical foliage details, Laguna del Hunco and AL1 locality (Figs. 36, 37). 32–34. Holotype, MPEF-Pb 8911a (Figs. 32, 33), 8911b Fig. 34) (also Figs. 19, 50–52, 76), showing linear reduced leaves at shoot base (Fig. 32); spiral pattern of broken leaf bases, striated leaf surfaces, and coalified central bands (Fig. 33); and miniature leaves mixed with regular leaves along the shoot (Fig. 34). 35–38. Specimens showing spirally deployed, broken leaf stubs. Fig. 35: MPEF-Pb 8932 (composite image). Figs. 36, 37: MPEF-Pb 8921 (also Fig. 25). Fig. 38: MPEF-Pb 8954. 39. MPEF-Pb 8946 (also Figs. 45, 46), detail of slightly twisted leaf bases at stem departure and leaf stubs. 40. MPEF-Pb 8923 (also Fig. 29), showing a

1354

•


Afrocarpus is the only other living genus that shares several characters of the helical foliage presented here, such as twisted and decurrent leaf bases, amphistomy, wings of transfusion tissue, and in some species spiral and crowded phyllotaxy (e.g., Gray, 1953; Farjon, 2010). However, in contrast to the helical foliage form of R. spiralifolium and the living Retrophyllum species, Afrocarpus foliage is typically much larger, has less continuous stomata across the midvein, and lacks the scale leaves of the fossils and Old World Retrophyllum; the obscure midvein on both leaf surfaces of the fossils and New Caledonian Retrophyllum; and the markedly acuminate apices and lateral resin canals of the fossils and New World Retrophyllum (e.g., Gray, 1953; Page, 1989; Hill and Pole, 1992; Farjon, 2010; Knopf et al., 2012; Table 1). The helical foliage form is not unexpected in the fossil record of Retrophyllum. The South American Retrophyllum species exhibit spiral leaf deployment in seedlings (Mill, 2016), and spiral phyllotaxy also occurs in the closely related genus Afrocarpus as just noted. The helical leaves are not in conflict with the diagnosis of Retrophyllum by Page (1989: p. 379), who also mentioned leaves “spirally arranged on leading shoots” in his description, and both Page (1990) and Farjon (2010) stated that the genus has spiral leaf insertion. The single relevant anatomical study (Florin, 1931; also see Florin, 1940b) found R. rospigliosii leaf insertion at the stele to be decussate (a variation of “spiral”). The characteristic pectinate deployment reflects both gradual torsion within the twig and a second, abrupt heterofacial twist at the base of the leaf’s free portion. Reducing the second twist allows the four-ranked foliage seen in the New Caledonian flip-leaves (Florin, 1940b). Presumably, the presence of additional insertion points in extinct species would be sufficient to produce the fully helical foliage seen in the fossils. Additional anatomical studies of the living species, including seedlings, would help clarify evolutionary developmental hypotheses of leaf twisting and the significance of the fossils’ helical phyllotaxy. In sum, we do not consider the helical foliage a sufficient basis to erect a new genus, especially in light of its distinctive features shared with the associated foliage forms (distichous and reduced), all of which indicate close affinities with living Retrophyllum. Comparisons with the extant Retrophyllum species (Table 1) show that R. spiralifolium is distinguishable from each and that the fossils have a unique mosaic of characters found today in both South American and Old World flip-leaves. The most conspicuous differences of the fossils from all living species are the spirally deployed leaf form, the markedly acuminate leaves, and the substantial size variation of leaves along the shoots. Retrophyllum spiralifolium foliage has many similarities to New Caledonian R. minus and R. comptonii, which are the two living species that have especially wide wings of transfusion tissue and obscure midveins like the fossils (Figs. 6, 9; Buchholz and Gray, 1948; Buchholz, 1949; Gray, 1962; de Laubenfels, 1969). Moreover, they are the only two extant species that exhibit nondistichous adult foliage (Figs. 4, 7). Their additional shared features with the fossils (Table 1) include foliage branches clustered at ends of penultimate branches (Fig. 10), terminal buds protected by modified leaves (Figs. 41, 42), and ovoid reduced leaves; however, the ovoid leaves are distichous in the fossils

(Figs. 55‒57) but decussate in the living species (Fig. 7; Gray, 1962). Shoots of reduced leaves (Figs. 55‒60) are characteristic today in all four Australasian (Figs. 7, 8) but not the two South American Retrophyllum species, which have minimal or no scale leaves on vegetative shoots as well as naked terminal buds (Gray, 1962; Mill, 2016). We note that the narrow-miniature leaf form is alternate in the fossils (Figs. 59, 60), differing from the opposite phyllotaxy of all extant specimens we have seen (Fig. 8). In contrast, the fossil foliage has two characters that are found only in living South American Retrophyllum: acuminate leaf apices (e.g., Figs. 15, 47) and lateral resin canals (Fig. 44; Table 1; Orr, 1944; Buchholz and Gray, 1948; Gray and Buchholz, 1948; Knopf et al., 2012; Mill, 2016). Moreover, the grouping of R. spiralifolium pollen cones (Figs. 61–72) closely resembles some South American R. rospigliosii specimens (Fig. 2; R. piresii pollen cones not known), wherein an enlarged peduncle can accommodate pollen cones that are distichously arranged, long-cylindrical, and subtended by pedicels and narrow leafy bracts. One minor difference is that the bases of the subtending leaves are slightly twisted in the fossils (Figs. 69, 70) but not in R. rospigliosii (Fig. 2; Gray and Buchholz, 1948). The Old World species R. filicifolium and R. vitiense (e.g., Fig. 3) are also dissimilar to the fossils in having their large cone groupings (i.e., of more than about 3‒5 cones) on comparatively thick, often compound fertile branches; their cones are relatively small, with scalelike subtending bracts and more tightly packed microsporophylls. However, solitary cones in these living species are long-cylindrical with comparatively loosely packed microsporophylls, like the fossil cones. The fossil pollen cones are much less similar to the two extant New Caledonian species, whose cones are smaller and, when in large groups, are usually located at the ends of branches, where the cones are axillary to regular leaves that grade terminally to scales (e.g., Fig. 4). The new Retrophyllum species is rapidly recognized in the field from the flip-leaved, distichous form (e.g., Fig. 15); the spiraling leaves, broken leaf bases, and abundant miniature leaves of the helical foliage (e.g., Figs. 34–38); the markedly acuminate leaf apices; and the dark stripe of the coalified central tissue band. Among the other gymnosperms at Laguna del Hunco and Río Pichileufú (Table 2), the most similar leaf morphology appears in the other podocarps. Podocarpus andiniformis leaves are bifacially flattened but not basally twisted or oriented in a plane, and their stomata are well separated by a distinct midvein. Dacrycarpus puertae and Acmopyle engelhardti have bilaterally flattened foliage that is not basally twisted and lines of stomata separated by a well-defined midvein, among many other differences. The pollen cones of R. spiralifolium are also quite distinct in their specialized distichous grouping onto an enlarged peduncle, via large pedicels that are inserted into the axils of narrow, reduced leaves that have thick central bands and longitudinally striated surfaces. The Australasian Retrophyllum fossils (see Introduction) have well-preserved cuticle but little macromorphology available for comparison to the Argentine fossils. Likewise, the extinct podocarpaceous genera Willungia and Smithtonia are represented by shoot fragments with heterofacially flattened foliage and well-preserved

←

slightly twisted leaf base and piercing-and-sucking marks of scale insects along the central bands. 41. MPEF-Pb 8927 (also Figs. 74, 75; composite image), showing modified, asymmetrical terminal leaves protecting the bud area and extensive piercing-and-sucking marks of scale insects along the central bands. 42. MPEF-Pb 8944a (also Fig. 30), detail of terminal bud area showing cluster of modified, reduced protective leaves and abundant amber casts (whitish material).



• 1355

1356

•


cuticle (Hill and Pole, 1992), although attached pollen cones are preserved in Smithtonia victoriensis (= Decussocarpus brownei sensu Greenwood, 1987: figs. 12, 13). Although most of the diagnostic characters of Willungia and Smithtonia are based on cuticular micromorphological features not preserved in R. spiralifolium, we can safely exclude any close relationship. Both the extinct genera have stomata separated by the midvein, quite unlike the continuous stomata of R. spiralifolium (Figs. 48‒54). The pollen cones of Smithtonia victoriensis (Greenwood, 1987: figs. 12, 13) are paired on an axillary shoot, unlike the unpaired Argentine fossil cones, and not closely resembling the configurations seen in extant Retrophyllum (Figs. 2‒4). Retrophyllum spiralifolium also preserves a large suite of macroscopic vegetative and reproductive characters typical of the extant genus, including the conspicuous central transfusion-tissue band, striated leaf surfaces, and multiple foliage forms with regular and reduced leaves. Previous informal references to what is here described as R. spiralifolium include Podocarpaceae leaf morphotypes TY008 and TY176 of Wilf et al. (2005) and mentions of an undescribed Retrophyllum species in several subsequent articles (Wilf et al., 2009, 2013, 2014, 2016; Wilf, 2012; Merkhofer et al., 2015; Quiroga et al., 2016). The holotype was cited informally under field number LH6-112 by Wilf et al. (2005: p. A6); paratype MPEF-Pb 8917 was referenced informally under field number LH13-1006 by Wilf et al. (2005: p. A9). Insect-feeding damage, Retrophyllum spiralifolium sp. nov—

Insect damage on R. spiralifolium leaves at Laguna del Hunco (none found at Río Pichileufú) includes hole feeding (Fig. 15), margin feeding (Figs. 15, 16, 80), and piercing-and-sucking (Figs. 24, 40, 41, 73‒80). Hole feeding (Fig. 15) includes a circular hole 0.5 mm in diameter (DT1) that is surrounded by a 0.1–0.2 mm wide rim of reaction tissue and a polylobate hole 0.6 mm long by 0.2 mm wide (DT3) with a reaction rim 20 marks on a single leaf. The marks have no noticeable relief on the leaf surface and are slightly darker at their centers, which may indicate the position of the puncture mark or a preservational artifact. The positioning suggests that the insects were penetrating the transfusion tissue or possibly the phloem to access transported fluids, as seen in aphid feeding on Pinus sylvestris L. (Scotch Pine; Bliss et al., 1973). Fluid flow is more limited distal to the transfusion tissue, and thus access costs would be higher for insects. One specimen has holes at the sites of piercing-and-sucking (Fig. 80), suggesting that the feeding damage weakened the tissue and led to its dropping from the leaf (Wheeler, 1980). Feeding on or adjacent to the midvein is a common behavior of many extant species of Hemiptera associated with angiosperms, such as Coccidae (Sanders, 1905; Wakgari and Giliomee, 1998), Miridae (Dodge, 1943; Wheeler, 1980), and Pentatomidae (Hori et al., 1984). Few records exist of herbivory on extant Retrophyllum. As summarized by Mill (2016), R. vitiense of Fiji supports a scolytine seed borer (Greenwood, 1975) and an introduced drywood termite (Gray, 1974). The Andean R. rospigliosii is associated with several species of scolytine wood-boring beetles (Schedl, 1965; Wood, 1971; Wood and Bright, 1992). In New Caledonia, unidentified insect larvae occupy the terminal buds of R. minus, causing their enlargement (Gray, 1962). Despite the lack of previously documented folivory, we discovered a wide variety of insect feeding on Retrophyllum herbarium specimens (Figs. 81‒89), including hole and margin feeding, midvein cutting, galling, and piercing-and-sucking by scale insects. Several species are associated with a suite of margin feeding types (Figs. 81‒83) quite similar to those of the fossils, including semicircular excisions into the leaf margin (DT12), apex feeding through the midvein (DT13), and excisions from the margin to the midvein (DT14). Other specimens preserve in situ scale insects (Figs. 85, 86); unlike the Eocene damage, these are located distal to the midveins and transfusion-tissue bands, where the culprits would most likely have accessed mesophyll tissue. Galls include circular to polylobate blisters on R. vitiense that are characterized by slightly raised epidermal tissue and circular exit holes (Figs. 87, 88), as well as small, slightly darkened bumps on seedling leaves of R. comptonii (Fig. 89). Midvein cutting (Fig. 84), not seen in the fossils, is a behavioral strategy that allows the release of unpalatable resins and defensive compounds in the exudate, enabling feeding at more distal leaf locations (Dussourd, 1999). Species—Retrophyllum superstes Wilf, sp. nov. Specific diagnosis—Foliage with slender central band of thickened tissue and obscure midvein. Leaves narrow-lanceolate, apices

←

Retrophyllum spiralifolium sp. nov., distichous (Fig. 43) and helical (Figs. 44–54) foliage, fine details, Laguna del Hunco. 43. MPEF-Pb 8917b (under epifluorescence; lower on the branch and on the counterpart of specimen shown in Figs. 15, 16), showing amber casts of resin canals (white) in the twig and entering the leaf medially within the central band. 44. MPEF-Pb 8969a (also Fig. 22), showing prominent amber cast of a lateral resin canal (arrow). 45, 46. MPEF-Pb 8946 (also Fig. 39; composite image), showing well-striated leaf surface (Fig. 45) covered with elongate-rectangular epidermal cells (Fig. 46); coalified material of the central band mostly lost except at the base. 47. MPEF-Pb 8940b (also Fig. 27, 77, 78), acuminate apex detail. 48, 49. MPEF-Pb 8953, detail of a central band area preserving longitudinal rows of stomata in normal light (Fig. 48) and the same area under epifluorescence (Fig. 49). 50–52. Holotype, MPEF-Pb 8911b (also Figs. 19, 32–34, 76), under epifluorescence, Fig. 50 a composite image; showing striated leaf surface, acuminate apex, and central band with rows of coalified stomata. 53, 54. MPEF-Pb 8956a (also Fig. 21), as for Figs. 51, 52. FIGURES 43–54



• 1357

FIGURES 55–60 Retrophyllum spiralifolium sp. nov., distichous shoots of reduced leaves, Laguna del Hunco. 55–57. MPEF-Pb 8973, heterofacially flattened shoot of ovoid reduced leaves, with broad, coalified central band areas, amber casts of medial resin canals visible as whitish central stripes, and longitudinally striated leaf surfaces (Figs. 56, 57 from base of shoot in Fig. 55). 58–60. Shoots of narrow, alternate, heterofacially flattened, miniaturized leaves with thickened midvein area and longitudinally striated leaf surfaces. Figs. 58, 59: MPEF-Pb 8974a. Fig. 60: MPEF-Pb 8977.

1358

•


FIGURES 61–68 Retrophyllum spiralifolium sp. nov., peduncle with remains of 13 distichous, pedicellate pollen cones subtended by narrow, reduced leaves with thickened central bands and longitudinally striated surfaces (continued in Figs. 69–72). Smaller leaves free on the axis basally and distally (or terminal cone formerly present above distal leaf ); amber casts of resin ducts throughout. Laguna del Hunco, MPEF-Pb 8980a,b. 61. Distal portion, MPEF-Pb 8980a. 62. Counterpart preserving base to partial overlap of distal portion in Fig. 61, MPEF-Pb 8980b. 63, 64. Map of pollen cone parts and counterparts as shown in Figs. 61 and 62, respectively. 65. Pollen cone 10a (per map in Fig. 63), with well-preserved, distally expanded pedicel and subtending leaf not preserved. 66. Pollen cone 7b (composite image). 67. Pollen cones 1b and 3b, and base of cone 2b at lower right, with subtending leaves (composite image). 68. Pollen cone 2b (composite image), showing striations, central band of subtending leaf, and a prominent amber cast of a medial resin canal on the clasping leaf at bottom left (arrow).



• 1359

1360

•


subrounded, partially overlapping along shoot, size abruptly reduced toward base of shoot. Holotype here designated—MPEF-Pb 8910 (Figs. 90‒96), a leafy

shoot part and counterpart from the LefE locality, San Ramón Section, Lefipán Formation, terminal Maastrichtian, northwest Chubut, Argentina, collected 18 November 2006. Etymology—Latin, superstes, surviving, because this fossil shows that the Retrophyllum lineage evolved during the Mesozoic and survived the end-Cretaceous extinction. Description—The only known specimen (Figs. 90‒96) is a leafy twig segment of 64 mm length with a nearly intact base and a broken apex, bearing the remains of ≥13 leaf pairs. The foliage is distichous, pectinate, opposite, partially overlapping, decurrent, and extensively clasps the twig along the internodes so that opposing leaf bases overlap in a zigzag pattern. The leaves twist heterofacially into a common plane at twig departure. Leaf shape is lanceolate, and the apex is acute and subrounded, not acuminate. Three pairs of abruptly reduced leaves are present at the base, the basalmost much smaller (two pairs not complete); length of the free portion of the reduced leaves is 5.4–10.7 mm, width 1.7–2.2 mm, and length:width 3.2– 4.9:1. Subsequent leaves are abruptly larger; length of their free portion is 12.6–18.8 mm, width 2.0–2.9 mm, and length:width 5.3–6.6:1. The leaves are apparently amphistomatic, with a central, longitudinal band of thickened tissue that obscures the true midvein; the band is coalified and easily visible as a black stripe of total width about onefifth of leaf width. Parallel, longitudinal striations are present across both leaf surfaces and not concentrated into stomatal bands; the course of the striations is mostly more obtuse than the midvein and margin, recurving admedially toward the apex. Remarks, Retrophyllum superstes sp. nov—The single specimen of Cretaceous R. superstes is generally similar to the distichous principal foliage form of Eocene R. spiralifolium (Figs. 10‒17). Both are flip-leaved and have similar leaf dimensions, coalified central bands presumed to represent wings of transfusion tissue, and longitudinal striations over the remaining leaf surface like those that border stomatal rows in extant Retrophyllum. On the basis of these shared features, it is reasonable to presume that R. superstes also had stomata continuous across the midvein without interruption, even though they did not survive fossilization except as degraded traces in the central stripe (Fig. 96). The thickened central band, longitudinal striations, and continuous stomata are all compatible with Retrophyllum and not the extinct flip-leaved genera Smithtonia and Willungia (Hill and Pole, 1992). Despite their similarities, the subrounded leaf apices and more slender central band (band width about a fifth of leaf width) of R. superstes are different from the acuminate apices and thicker central band (band width about a fifth to a third of leaf width) of R. spiralifolium. Moreover, R. superstes has greater leaf overlap, less convex margins, and more abruptly reduced basal leaves (Figs. 90, 91)

than distichous R. spiralifolium (Figs. 11–17). Pollen cones for R. superstes are not yet known and cannot be compared. In addition to the morphological differences, conspecificity is unlikely given the ~14 Ma greater age (66–67 vs. 52 Ma) of R. superstes and its completely different paleoenvironment (Cretaceous coastal lowlands vs. Eocene caldera lake). The generic assignment of R. superstes is provisional, given its unknown foliar variation and reproductive structures, but its preserved characters are sufficient to support it either as a Retrophyllum or an extinct but close relative. The fossil lacks diagnostic characters necessary to establish any such extinct taxon and possesses several characters unique to Retrophyllum, and thus we prefer to assign it to Retrophyllum. The new species, especially in its combination of a thickened central band, indistinct midvein, lanceolate leaves with subrounded apices, and a basal pair of highly reduced leaves, is very similar to the distichous foliage of New Caledonian R. minus (Fig. 5; Gray, 1962). Additional specimens are clearly needed to better characterize and diagnose this fossil species. Insect-feeding damage, Retrophyllum superstes sp. nov—Retro-

phyllum superstes is associated with numerous dark, circular marks 0.1‒0.2 mm in diameter that most likely represent piercing-andsucking damage of hemipteran insects (Figs. 90–92, 95). The marks are arranged in rows that are typically 0.2‒0.3 mm to as far as 0.7 mm from the central band, mostly absent within 0.3 mm of the leaf margins, and less frequently occurring on the band itself. This positioning suggests that the culprits primarily penetrated mesophyll close to the transfusion tissue and more rarely fed on transported fluids through the transfusion tissue or phloem. The consistent circular shapes and small sizes of the marks are typical of styletal damage; however, the damage is not well preserved, and individual marks do not display central depressions as is characteristic of many fossil piercing-and-sucking marks (Labandeira et al., 2007). Some of the marks have relief suggestive of galls (Labandeira et al., 2007), which remain an alternative possibility. Species—Retrophyllum araucoensis (Berry) Wilf, comb. nov.

Decussocarpus araucoensis (Berry) Greenwood, Australian Journal of Botany 35: 131 (1987). Podocarpus araucoensis (Berry) Florin, Svenska Vetenskapsakademiens Handlingar 19: 8 (1940). Basionym: Araucaria araucoensis Berry, Johns Hopkins University Studies in Geology 4: 122 (1922). Lectotype—USNM 320631, part (Fig. 97) and counterpart of a penultimate branch with ~10 ultimate leafy branches, presumed to be the specimen drawn by Berry (1922: pl. III, fig. 4) from Lota, Chile, which Florin (1940b: p. 8) designated as the lectotype of Podocarpus araucoensis by reference to that drawing. Syntypes—USNM 320632 (Figs. 102‒104); and USNM 320633, a block containing two leafy shoots (Figs. 98‒100) and an isolated leaf (Fig. 101; possibly drawn by Berry, 1922: pl. III, fig. 2), both from

←

Retrophyllum spiralifolium sp. nov., peduncle with pollen cones (continued from Figs. 61–68), Laguna del Hunco, MPEF-Pb 8980a,b. See Figs. 63, 64 for cone maps. 69. Detail of distal area preserved on MPEF-Pb 8980b (Figs. 62, 64), pollen cones 4b and 6–11b, showing abundant amber casts of resin canals, subtending leaves with slightly twisted bases, pedicels, and large cone 4b pressed against and parallel to the left side of the axis (composite image). 70. Base of pollen cone 13a, showing slightly twisted base of subtending leaf and pedicel laterally inserted into the peduncle axis. 71. Segment of pollen cone 10b with cone axis and ovate, apiculate microsporophylls. 72. Single microsporophyll with apiculate apex, pollen cone 12a. FIGURES 69–72



• 1361

1362

•


Ríos Mine, Curanilahue, Chile. USNM 545368 and 545369, blocks with 2‒3 leafy shoot fragments each, recently discovered in Berry’s collections and labeled in his handwriting as “Araucaria araucoensis Berry, Miocene, Conception [sic], Chile.” These two specimens were without doubt part of the original gathering of material for the protologue and thus merit syntype status. Additional material—Leafy branches illustrated by Florin (1940b): S165205-01, Curanilahue site, pl. 1, figs. 1, 2 of Florin (1940b); S160415, Buen Retiro, pl. 1, fig. 11; S160127, Peumo, pl. 1, fig. 12 and S117974 for slide preparations thereof shown in pl. 2, figs. 4–6 and pl. 3, fig. 1; S160784, Curanilahue, pl. 1, fig. 3; S160819, Curanilahue, pl. 1, fig. 4; and S165206a, Buen Retiro, pl. 1, figs. 8–9 and S117985 for slide preparations thereof in pl. 1, fig. 10 and pl. 2, figs. 1–3. Florin designated S165206a as a hypotype (an exemplar that carries no nomenclatural status). Additional leafy branches not illustrated by Florin: S165206b (counterpart of S165206a); S160808, Curanilahue; S160016-01, S160050, and S160117-02, Peumo; S117975, S117976, and S160016-01, unfigured slide preparations, Peumo. In case they are eventually relocated, we also include in the new combination some of the leafy branches figured as “Sequoia” chilensis by Engelhardt (1905: material shown in pl. 1, figs. 2 and 4–8 only; repository history unknown), although the specimens are probably lost (L. Kunzmann and T. Wappler, personal communication in Wilf, 2012). Both Berry (1922) and Florin (1940b) included these specimens in their previous concepts of the present species. The other apparently lost specimen of “S.” chilensis shown by Engelhardt (1905: pl. 1, fig. 3) remains in Dacrycarpus (formerly “Sequoia”) chilensis (Engelhardt) Wilf, which has surviving type specimens from an earlier publication (Engelhardt, 1891; see Florin, 1940b; Wilf, 2012). Remarks, Retrophyllum araucoensis comb. nov—Florin (1940b)

did not examine Berry’s (1922) type specimens of “Araucaria” araucoensis (here Figs. 97–104), which were originally published without photographs and only as inaccurate (as deduced by Florin and confirmed here) drawings. Instead, Florin based his revision on material housed at the Swedish Museum of Natural History, Stockholm, that he considered to represent the same species as the unseen type specimens and on his interpretations of Berry’s drawings. Greenwood (1987) made the combination Decussocarpus araucoensis (Berry) Greenwood; however, the name Decussocarpus was ruled illegitimate (see Mill, 2001, 2016; Mill and Hill, 2004). Thus, despite general past agreement that some or all of the Chilean material represents Retrophyllum (Hill and Pole, 1992; Brodribb and Hill, 1999a), the problems listed have until now prevented the establishment of a stable nomenclature for these fossils.

We find no significant differences in morphology among the USNM types and the S material and consider all to represent the same extinct species, Retrophyllum araucoensis, even though cuticle was prepared only from the S material (Florin, 1940b) and not from the very fragile and coalified type specimens. Moreover, all the collecting sites are located in close proximity to each other within a small area of exposure of the Eocene Concepción–Arauco Coal Measures (Florin, 1940b; Collao et al., 1987), and specimens from Curanilahue occur in both the type and S collections. Thus, all the material can reasonably be inferred to be of similar age and provenance, despite the lack of precise locality data and the need to relocate and stratigraphically constrain the collecting sites. Florin’s (1940b) diagnosis and description remain adequate when the type material is included and are not emended here. We concur with Florin’s (1940b) placement of the species into Retrophyllum (then Podocarpus Section Polypodiopsis) and with statements by subsequent authors based on Florin’s work that some or all of the material represents Retrophyllum (Hill and Pole, 1992; Brodribb and Hill, 1999a). The fossils are clearly flip-leaved with opposite distichous deployment, and the leaves bear a single midvein and the typical longitudinal striation pattern across the blade that corresponds to the striations separating stomatal rows in Retrophyllum (Figs. 99, 103, 104). The stomatal pattern illustrated by Florin (1940b: pl. 1, fig. 10; pl. 2, figs. 4–6) is characteristic of Retrophyllum as he described (see also Florin, 1931); likewise, Hill and Pole (1992) did not observe any diagnostic cuticle characters of Smithtonia and Willungia in Florin’s illustrations. We note that the midvein of R. araucoensis is distinct and appears slightly thickened (Fig. 103), probably due to the presence of relatively short wings of transfusion tissue. Retrophyllum araucoensis clearly differs from R. spiralifolium from the Eocene of Argentina (Figs. 10‒54), most notably in its lack of the diagnostic spiral-leaved foliage form, obscure midvein, wide central band, and markedly acuminate apices of R. spiralifolium. Comparing R. araucoensis with the single specimen of terminal Cretaceous R. superstes (Figs. 90‒96), both have ovate-lanceolate leaves with subrounded apices and widths to ~3 mm. However, R. superstes leaves have an obscure midvein, a more prominent central band, and a much narrower aspect than R. araucoensis because they are longer (to 18.8 mm vs. to 11 mm for R. araucoensis per Florin, 1940b). Previous authors have noted similarities of R. araucoensis to South American R. rospigliosii and R. piresii as well as West Pacific R. vitiense (Florin, 1940b; Silba, 1983; Greenwood, 1987). Although the type material of R. araucoensis preserves no characters that might further clarify its relationships, we agree that what is preserved most resembles the South American flip-leaves, at least by elimination. Retrophyllum araucoensis exhibits little similarity to the New Caledonian species R. minus and R. comptonii (Figs. 4‒7, 9).

←

Piercing-and-sucking insect-feeding damage marks associated with central transfusion-tissue band of Retrophyllum spiralifolium sp. nov. leaves, Laguna del Hunco (Figs. 73–80), and insect-feeding damage found on herbarium specimens of extant Retrophyllum (Figs. 81–89). 73. MPEF-Pb 8926 (also Fig. 24; light color due to weathered matrix). 74, 75. Marks positioned on the transfusion-tissue band. MPEF-Pb 8927 (also Fig. 41). 76. Marks overlapping the transfusion-tissue band and lamina. Holotype, MPEF-Pb 8911b (also Figs. 19, 32–34, 50–52). 77–79. Marks densely clustered along the transfusion-tissue band. MPEF-Pb 8940b (Fig. 77; also Figs. 27, 47); MPEF-Pb 8940a (Fig. 78; also Figs. 27, 47); MPEF-Pb 8939 (Fig. 79). 80. Marks along the transfusion-tissue band, including holes where tissue weakened from the insect damage dropped from the leaf. MPEF-Pb 8950. 81. Varied margin feeding on R. rospigliosii, Peru, E 00198820, downloaded from http://data.rbge.org.uk/herb/E00198820 and used with permission. 82. Margin feeding to midvein, excision nearly straight-sided. R. vitiense, Fiji, NSW 527512. 83. Margin feeding to midvein, excision arcuate, R. comptonii, New Caledonia, K 000289127. 84. Midvein cutting, R. vitiense, Fiji, K 000289109. 85. In situ scale insect on R. rospigliosii, Perú, E 00198820 (same specimen as in Fig. 81). 86. In situ scale insect on R. comptonii, New Caledonia, E 00099929. 87. Numerous blister galls on R. vitiense, Fiji, K 000289108. 88. Blister galls on R. vitiense, Fiji, E 00094524. 89. Gall on seedling leaf of R. comptonii, New Caledonia, E 00099935. FIGURES 73–89



• 1363

TABLE 2. Gymnosperm flora of Laguna del Hunco and Río Pichileufú.

Taxon Ginkgoaceae Ginkgoites patagonicus (Berry) Villar de Seoane, Cúneo, Escapa, Wilf & Gandolfo Zamiaceae Austrozamia stockeyi Wilf, Stevenson & Cúneo a Araucariaceae Agathis zamunerae Wilf Araucaria pichileufensis Berry (of A. Section Eutacta) Cupressaceae Papuacedrus prechilensis (Berry) Wilf, Little, Iglesias, Zamaloa, Gandolfo, Cúneo & Johnson Podocarpaceae Acmopyle engelhardti (Berry) Florin Dacrycarpus puertae Wilf Podocarpus andiniformis Berry Retrophyllum spiralifolium Wilf, sp. nov. cf. Phyllocladus sp. a a

Organs preserved

Citations

Leaves

Berry, 1935, 1938; Villar de Seoane et al., 2015

Leaves

Wilf et al., 2016

Leafy branches, isolated leaves, pollen cones, seed cones, cone scales, cone scale with seed Leafy branches, pollen cones (unpublished), cone scales with seeds

Berry, 1938; Wilf et al., 2014

Leafy branches, leafy branch with seed cone

Berry, 1938; Wilf et al., 2009

Leafy branches Leafy branches, leafy branch with pollen cones, leafy branch with seed cones Leafy branches, leafy branch with pollen cone (unpublished), isolated leaves Leafy branches, peduncle with pollen cones Branches with phylloclades

Berry, 1938; Florin, 1940a; Wilf, 2012 Berry, 1938; Wilf, 2012

Berry, 1938; Wilf et al., 2005, 2014

Berry, 1938; Wilf et al., 2005 Present study Unpublished, preliminary identification

Laguna del Hunco only.

These two living species feature much broader bands of transfusion tissue and can have opposite-decussate foliage, unlike all the Chilean fossils. The other Old World species, R. filicifolium and R. vitiense, have larger and more lanceolate leaves than R. araucoensis, with markedly more acute apices (e.g., Fig. 3). However, R. araucoensis does not exhibit obovate leaves or acuminate leaf apices as seen among the living South American species (Table 1). Florin’s lectotype (Fig. 97) is the only type specimen that can be correlated with some confidence to one of Berry’s (1922) drawings, because it is the sole sample with branching; Berry drew only one specimen with branching, however incorrectly in the details. The leaves and leaf bases of the lectotype are poorly preserved, quite unlike their portrayal in Berry’s drawing, and many parts of the specimen are obscured by the matrix and would benefit from manual preparation (see Materials and Methods). Without the additional specimens available, it would be difficult to assign the lectotype to Retrophyllum, but using this material it is clear that all represent the same fossil species of this genus.

DISCUSSION AND CONCLUSIONS This report substantially increases the evolutionary, biogeographic, and paleoecological knowledge of Retrophyllum, a morphologically distinctive and geographically disjunct genus of Podocarpaceae. Retrophyllum superstes is by far the oldest representative of the Retrophyllum lineage; it provides one of the only examples, together with the well-known case of Araucaria, of an extant conifer genus surviving the end-Cretaceous extinction in Gondwana. The new species demonstrates that the divergence of Retrophyllum from its sister clade comprised of Afrocarpus and Nageia, or, very conservatively, from Podocarpus (see Introduction), must have occurred at least by the K–Pg boundary (66 Ma). This finding is concordant with recent molecular divergence dating of the Retrophyllum– Podocarpus split at ~85 Ma (Quiroga et al., 2016), while otherwise the same node has been considered Cenozoic (Biffin et al., 2011,

2012; Crisp and Cook, 2011; Leslie et al., 2012, 2017). The Quiroga et al. (2016) estimate was calibrated using the then-undescribed 52.2 Ma occurrence (citing Wilf, 2012) of what is here fully presented as R. spiralifolium, along with several other recently discovered (or recently well-dated) fossil podocarp occurrences from Patagonia that were not used in the other molecular studies. This outcome reinforces the growing importance of Patagonian plant fossils for temporally calibrating the tree of life, as discussed in detail elsewhere (Wilf and Escapa, 2015, 2016; Wilf et al., 2017). We note that podocarps with flattened, single-veined foliage have a deeper history in Patagonia deserving of closer study, such as the leafy branches and pollen cones of Apterocladus lanceolatus Archangelsky from the Early Cretaceous Baqueró Group (Archangelsky, 1966; Archangelsky and Del Fueyo, 2010). Eocene R. spiralifolium brings a wealth of information to the fossil record that will be informative for phylogenetic and biogeographic studies of conifer evolution. This fossil species combines novel features, such as spiral leaf deployment and reduced foliage abruptly interspersed with regular leaves; characters found in the living South American flip-leaves, such as lateral resin canals, acuminate apices, and distichous pedunculate pollen-cone configuration; and features of the New Caledonian species such as nondistichous foliage, broad transfusion-tissue band, and ovoid reduced leaves. This suite of features linking R. spiralifolium to both Neotropical and Australasian flip-leaves is consistent with its occurrence on terminal Gondwana and concretely supports long-hypothesized origins of the modern disjunction through vicariance (Florin, 1940b, 1963; Buchholz and Gray, 1948). The fossils also support the monophyly of the disjunct genus by directly associating its living species through the fossils’ mosaic of preserved morphological characters. Retrophyllum joins a small list of lineages known from the Paleogene of Patagonia that survived in South America (see Materials and Methods), in comparison to the predominant pattern of extinction on that continent and survival in Australasia or elsewhere in the Old World (“eastern survival” per Kooyman et al., 2014).

1364

•


FIGURES 90–96 Retrophyllum superstes sp. nov., LefE locality, MPEF-Pb 8910a (Figs. 90, 92, 93, 95, 96), 8910b (Figs. 91, 94). 90–92. General aspect of shoot, showing reduced basal leaves, extensively clasping leaf bases overlapping in a zigzag pattern, heterofacial leaf twisting at twig departure, coalified central band, subrounded apices, longitudinal striations, and longitudinally oriented rows of likely piercing-and-sucking marks. 93, 94. Details of clasping, zigzagging leaf bases with heterofacial twisting. 95. Detail of insect-damage marks on leaf shown at left in Fig. 92. 96. Detail of a central band, showing coalified remains of presumed degraded stomata.



• 1365

FIGURES 97–104 Retrophyllum araucoensis (Berry) comb. nov., type material of Berry (1922). 97. Lectotype, USNM 320631a, a penultimate branch with ~10 ultimate leafy branches. 98–101. USNM 320633, a block preserving two leafy twigs (Fig. 98 and its detail in Fig. 99, showing striated leaf surfaces; Fig. 100) and an isolated leaf showing longitudinal striations (Fig. 101). 102–104. USNM 320632, showing leaf clasping and twisting at twig departure, midvein areas, and longitudinal striations.

1366

•


Pending new macrofossil discoveries from other regions of South America, we cannot answer the compelling question of why today’s Neotropical rainforests have Retrophyllum and not, for example, Agathis and Dacrycarpus. However, floristic distinctiveness between Patagonia and the Neotropics is ancient, as demonstrated by Paleogene palynological data (Jaramillo and Cárdenas, 2013) that include very low abundances of podocarp pollen in the Neotropics by comparison with Patagonia. The most likely scenario is that Retrophyllum (and probably Podocarpus) is an exception that proves the rule; this genus successfully crossed barriers that thwarted most other Gondwanic taxa, such as the subtropical arid zone (e.g., Ziegler et al., 2003), and shifted its range northward. The result is that Neotropical Retrophyllum has entered into comparatively novel floral associations, albeit with other podocarps included such as Podocarpus and Prumnopitys (Vicuña-Miñano and Mostacero León, 2003; Veblen et al., 2005). On the other hand, Australasian Retrophyllum still participates in assemblages with diverse Gondwanic elements that include many other genera known from the Paleogene of Patagonia (see Introduction and Materials and Methods; Wasscher, 1941; de Laubenfels, 1969, 1972; Jaffré, 1988, 1995; Farjon, 2010; Kooyman et al., 2014; Mill, 2016). The contrasting environmental settings of the three species studied here document significant habitat specialization early in the history of the Retrophyllum lineage. Retrophyllum superstes occupied Cretaceous Atlantic-coastal lowlands adjacent to tidal channels (e.g., Scasso et al., 2012), R. araucoensis lived in Eocene Pacificcoastal swamps (e.g., Collao et al., 1987), and R. spiralifolium grew on the margins of caldera lakes embedded within massive volcanic complexes in the interior of Eocene Patagonia (e.g., Aragón and Mazzoni, 1997). The climatic distributions of the living flip-leaves (Farjon, 2010; Biffin et al., 2012; Carpenter et al., 2012; Brodribb et al., 2014; Mill, 2016) and the characteristics of all the fossil assemblages where Retrophyllum is found (Carpenter et al., 2012; Kooyman et al., 2014) strongly associate the genus with frost-free, mesic to warm rainforest environments through time, consistent with other interpretations of the fossil sites studied here (e.g., Wilf et al., 2009; Barreda et al., 2012a; Wilf, 2012; Merkhofer et al., 2015). The past and present climatic distributions of Retrophyllum and other podocarp genera that have flattened, single-veined leaves that allow them to compete for light with angiosperms (e.g., Brodribb and Hill, 1997; Biffin et al., 2012) have been explained through physiological data that indicate high vulnerability to drought (Brodribb and Hill, 1999b, 2004; Brodribb, 2011; Brodribb et al., 2014). Even within this group, Retrophyllum is among the least drought resistant (Brodribb and Holbrook, 2006; Brodribb et al., 2014). One significant constraint is the limited lateral sap transport that is possible using a single vein in an expanded leaf, accomplished in many podocarps through specialized sclereids and other xylem tissues that are susceptible to failure under drought conditions (Brodribb and Holbrook, 2005; Brodribb, 2011). The transfusion-tissue bands found straddling the midveins in R. superstes and R. spiralifolium as in their living relatives, along with the abundant marks of sap-feeding insects associated directly with the tissue (Figs. 73‒80, 95), provide physical evidence of this trade-off operating in the past. ACKNOWLEDGEMENTS The authors thank M. Caffa, L. Canessa, I. Escapa, E. Hermsen, K. Johnson, P. Puerta, L. Reiner, E. Ruigómez, R. Wilf, S. Wing, and many others for invaluable field and laboratory assistance; E. Ruigomez

and A. Iglesias for help with international loans; A. Leslie and an anonymous colleague for very helpful reviews; the staff of USNM (J. Wingerath), CANB (B. Lepschi, C. Cargill), NSW (L. L. Lee, L. Murray), US (R. Russell), Harvard University Herbaria (J. Shapiro, E. Wood), E (L. Scott, R. Mill), K (S. Dawson), BH (A. Stalter, J. Svitko), and L (R. Bijmoer) for collections support; S. McLoughlin for updated information on collections housed at S; T. Brodribb, C. Labandeira, and D. de Laubenfels for valuable comments on leaf functional hydrology, insect damage, and conifer taxonomy, respectively; and Secretaría de Cultura de la Provincia del Chubut, the Nahueltripay family, and Instituto de Investigaciones Aplicadas for land access. Recent support for this research came from National Science Foundation (NSF) grants DEB-1556666 and DEB-1556136 and the Evolving Earth Foundation, and prior support came from NSF grants DEB-0919071, DEB-0918932, and DEB-0345750, Agencia Nacional de Promoción Científica y Tecnológica (Argentina), Proyecto de Investigación Científica y Tecnológica PICT 2433-2014, the David and Lucile Packard Foundation, National Geographic Society grant 7337-02, the University of Pennsylvania Research Foundation, and the Andrew W. Mellon Foundation.

DATA ACCESSIBILITY STATEMENT A high-resolution image archive of the fossils reported in this article is available open-access at Figshare (Wilf, 2017), https:// doi.org/10.6084/m9.figshare.5305420. LITERATURE CITED Aberhan, M., and W. Kiessling. 2014. Rebuilding biodiversity of Patagonian marine molluscs after the end-Cretaceous mass extinction. PLoS ONE 9: e102629. Aragón, E., and M. M. Mazzoni. 1997. Geología y estratigrafía del complejo volcánico piroclástico del Río Chubut medio (Eoceno), Chubut, Argentina. Revista de la Asociación Geológica Argentina 52: 243–256. Aragón, E., and E. J. Romero. 1984. Geología, paleoambientes y paleobotánica de yacimientos Terciarios del occidente de Río Negro, Neuquén y Chubut. Actas del IX Congreso Geológico Argentino, San Carlos de Bariloche, Argentina 4: 475–507. Archangelsky, S. 1966. New gymnosperms from the Ticó flora, Santa Cruz Province, Argentina. Bulletin of the British Museum (Natural History), Geology 13: 259–295. Archangelsky, S., and G. M. Del Fueyo. 2010. Endemism of Early Cretaceous conifers in western Gondwana. In C. T. Gee [ed.], Plants in Mesozoic time, 247–268. Indiana University Press, Bloomington, Indiana, USA. Ataroff, M. 2002. Precipitación e intercepción en ecosistemas boscosos de los Andes Venezolanos. Ecotropicos 15: 195–202. Barreda, V. D., N. R. Cúneo, P. Wilf, E. D. Currano, R. A. Scasso, and H. Brinkhuis. 2012a. Cretaceous/Paleogene floral turnover in Patagonia: Drop in diversity, low extinction, and a Classopollis spike. PLoS ONE 7: e52455. Barreda, V. D., and L. Palazzesi. 2010. Vegetation during the Eocene-Miocene interval in central Patagonia: a context of mammal evolution. In R. H. Madden, A. A. Carlini, M. G. Vucetich, and R. F. Kay [eds.], The paleontology of Gran Barranca, 375–382. Cambridge University Press, Cambridge, UK. Barreda, V. D., L. Palazzesi, L. Katinas, J. V. Crisci, M. C. Tellería, K. Bremer, M. G. Passalia, et al. 2012b. An extinct Eocene taxon of the daisy family (Asteraceae): Evolutionary, ecological, and biogeographical implications. Annals of Botany 109: 127–134. Barreda, V. D., L. Palazzesi, M. C. Tellería, L. Katinas, J. V. Crisci, K. Bremer, M. G. Passalia, et al. 2010. Eocene Patagonia fossils of the daisy family. Science 329: 1621.


Beaman, J. H., and R. S. Beaman. 1993. The gymnosperms of Mount Kinabalu. Contributions from the University of Michigan Herbarium 19: 307–340. Berry, E. W. 1922. The flora of the Concepción-Arauco coal measures of Chile. Johns Hopkins University Studies in Geology 4: 73–143. Berry, E. W. 1925. A Miocene flora from Patagonia. Johns Hopkins University Studies in Geology 6: 183–251. Berry, E. W. 1935. A Tertiary Ginkgo from Patagonia. Torreya 35: 11–13. Berry, E. W. 1938. Tertiary flora from the Río Pichileufú, Argentina. Geological Society of America Special Paper 12: 1–198. Bertrand, C.-E. 1875. Anatomie comparée des tiges et des feuilles chez les Gnétacées et les Conifères. Libraire de l’Académie de Médicine, Paris, France. Biffin, E., T. J. Brodribb, R. S. Hill, P. Thomas, and A. J. Lowe. 2012. Leaf evolution in Southern Hemisphere conifers tracks the angiosperm ecological radiation. Proceedings of the Royal Society B 279: 341–348. Biffin, E., J. G. Conran, and A. J. Lowe. 2011. Podocarp evolution: A molecular phylogenetic perspective. Smithsonian Contributions to Botany 95: 1–20. Bliss, M. Jr., W. G. Yendol, and W. H. Kearby. 1973. Probing behavior of Eulachnus agilis and injury to Scotch Pine. Journal of Economic Entomology 66: 651–655. Brodribb, T. J. 2011. A functional analysis of podocarp ecology. Smithsonian Contributions to Botany 95: 165–173. Brodribb, T. J., and R. S. Hill. 1997. Light response characteristics of a morphologically diverse group of Southern Hemisphere conifers as measured by chlorophyll fluorescence. Oecologia 110: 10–17. Brodribb, T. J., and R. S. Hill. 1999a. Southern conifers in time and space. Australian Journal of Botany 47: 639–696. Brodribb, T. J., and R. S. Hill. 1999b. The importance of xylem constraints in the distribution of conifer species. New Phytologist 143: 365–372. Brodribb, T. J., and R. S. Hill. 2004. The rise and fall of the Podocarpaceae in Australia—a physiological explanation. In A. R. Hemsley and I. Poole [eds.], The evolution of plant physiology: From whole plants to ecosystems, 381–399. Academic Press, London, UK. Brodribb, T. J., and N. M. Holbrook. 2005. Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiology 137: 1139–1146. Brodribb, T. J., and N. M. Holbrook. 2006. Declining hydraulic efficiency as transpiring leaves desiccate: Two types of response. Plant, Cell & Environment 29: 2205–2215. Brodribb, T. J., S. A. M. McAdam, G. J. Jordan, and S. C. V. Martins. 2014. Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proceedings of the National Academy of Sciences, USA 111: 14489–14493. Buchholz, J. T. 1949. Additions to the coniferous flora of New Caledonia. Bulletin du Muséum National d'Histoire Naturelle (Paris) sér. 2 21: 279–286. Buchholz, J. T., and N. E. Gray. 1948. A taxonomic revision of Podocarpus I. The sections of the genus and their subdivisions with special reference to leaf anatomy. Journal of the Arnold Arboretum 29: 49–63. Carpenter, R. J., M. P. Goodwin, R. S. Hill, and K. Kanold. 2011. Silcrete plant fossils from Lightning Ridge, New South Wales: New evidence for climate change and monsoon elements in the Australian Cenozoic. Australian Journal of Botany 59: 399–425. Carpenter, R. J., G. J. Jordan, M. K. Macphail, and R. S. Hill. 2012. Neartropical Early Eocene terrestrial temperatures at the Australo-Antarctic margin, western Tasmania. Geology 40: 267–270. Carpenter, R. J., P. Wilf, J. G. Conran, and N. R. Cúneo. 2014. A Paleogene trans-Antarctic distribution for Ripogonum (Ripogonaceae: Liliales)? Palaeontologia Electronica 17: article 17.13.39A. Carvalho, M. R., P. Wilf, H. Barrios, D. M. Windsor, E. D. Currano, C. C. Labandeira, and C. A. Jaramillo. 2014. Insect leaf-chewing damage tracks herbivore richness in modern and ancient forests. PLoS ONE 9: e94950. Carvalho, M. R., P. Wilf, E. J. Hermsen, M. A. Gandolfo, N. R. Cúneo, and K. R. Johnson. 2013. First record of Todea (Osmundaceae) in South America, from the early Eocene paleorainforests of Laguna del Hunco (Patagonia, Argentina). American Journal of Botany 100: 1831–1848. Collao, S., R. Oyarzun, S. Palma, and V. Pineda. 1987. Stratigraphy, palynology and geochemistry of the lower Eocene coals of Arauco, Chile. International Journal of Coal Geology 7: 195–208.


• 1367

Conran, J. G., G. M. Wood, P. G. Martin, J. M. Dowd, C. J. Quinn, P. A. Gadek, and R. A. Price. 2000. Generic relationships within and between the gymnosperm families Podocarpaceae and Phyllocladaceae based on an analysis of the chloroplast gene rbcL. Australian Journal of Botany 48: 715–724. Contreras-Medina, R., and I. Luna Vega. 2002. On the distribution of gymnosperm genera, their areas of endemism and cladistic biogeography. Australian Systematic Botany 15: 193–203. Crisp, M. D., and L. G. Cook. 2011. Cenozoic extinctions account for the low diversity of extant gymnosperms compared with angiosperms. The New Phytologist 192: 997–1009. de Laubenfels, D. 1953. The external morphology of coniferous leaves. Phytomorphology 3: 1–20. de Laubenfels, D. J. 1969. A revision of the Malesian and Pacific rainforest conifers, I. Podocarpaceae, in part. Journal of the Arnold Arboretum 50: 315–369. de Laubenfels, D. J. 1972. Flore de la Nouvelle Calédonie et dépendances, vol. 4: Gymnosperms. Muséum National D’Histoire Naturelle, Paris, France. de Laubenfels, D. J. 1982. Podocarpaceae. Flora de Venezuela 11: 7–41. de Laubenfels, D. J. 1991. Las Podocarpáceas del Perú. Boletín de Lima 73: 57–60. Dodge, B. O. 1943. The sycamore plant bug. Journal of the New York Botanical Garden 44: 214–215. Donovan, M. P., A. Iglesias, P. Wilf, C. C. Labandeira, and N. R. Cúneo. 2016. Rapid recovery of Patagonian plant-insect associations after the end-Cretaceous extinction. Nature Ecology & Evolution 1: 0012. Dussourd, D. E. 1999. Behavioral sabotage of plant defense: Do vein cuts and trenches reduce insect exposure to exudate? Journal of Insect Behavior 12: 501–515. Eckenwalder, J. E. 2009. Conifers of the world: The complete reference. Timber Press, Portland, Oregon, USA. Endlicher, S. 1847. Synopsis coniferarum. Scheitlin und Zollikofer, Sangalli (Sankt Gallen), Switzerland. Engelhardt, H. 1891. Ueber Tertiärpflanzen von Chile. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 16: 629–692. Engelhardt, H. 1905. Bemerkungen zu chilenischen Tertiärpflanzen. Abhandlungen der Naturwissenschaftlichen Gesellschaft Isis in Dresden 1905: 69–72. Farjon, A. 2005. A monograph of Cupressaceae and Sciadopitys. Royal Botanic Gardens, Kew, UK. Farjon, A. 2010. A handbook of the world’s conifers. Brill, Leiden, Netherlands. Florin, R. 1931. Untersuchungen zur Stammesgeschichte der Coniferales und Cordaitales. Kungl. Svenska Vetenskapsakademiens Handlingar 10: 1–588. Florin, R. 1940a. Die heutige und frühere Verbreitung der Koniferengattung Acmopyle Pilger. Svensk Botanisk Tidskrift 34: 117–140. Florin, R. 1940b. The Tertiary fossil conifers of south Chile and their phytogeographical significance. Kungl. Svenska Vetenskapsakademiens Handlingar 19: 1–107. Florin, R. 1963. The distribution of conifer and taxad genera in time and space. Acta Horti Bergiani 20: 121–312. Gandolfo, M. A., and E. J. Hermsen. 2017. Ceratopetalum (Cunoniaceae) fruits of Australasian affinity from the early Eocene Laguna del Hunco flora, Patagonia, Argentina. Annals of Botany 119: 507–516. Gandolfo, M. A., E. J. Hermsen, M. C. Zamaloa, K. C. Nixon, C. C. González, P. Wilf, N. R. Cúneo, and K. R. Johnson. 2011. Oldest known Eucalyptus macrofossils are from South America. PLoS ONE 6: e21084. Gibbs, L. S. 1917. Dutch N.W. New Guinea. A contribution to the phytogeography and flora of the Arfak Mountains. Taylor and Francis, London, UK. Goin, F. J., R. Pascual, M. F. Tejedor, J. N. Gelfo, M. O. Woodburne, J. A. Case, M. A. Reguero, et al. 2006. The earliest Tertiary therian mammal from South America. Journal of Vertebrate Paleontology 26: 505–510. González, C. C., M. A. Gandolfo, M. C. Zamaloa, N. R. Cúneo, P. Wilf, and K. R. Johnson. 2007. Revision of the Proteaceae macrofossil record from Patagonia, Argentina. Botanical Review 73: 235–266. Gradstein, F. M., J. G. Ogg, M. Schmitz, and G. Ogg. 2012. The geologic time scale 2012. Elsevier, Amsterdam, Netherlands. Gray, B. 1974. Forest insect problems in the South Pacific islands. Commonwealth Forestry Review 53: 39–48. Gray, N. E. 1953. A taxonomic revision of Podocarpus. VII. The African species of Podocarpus: Section Afrocarpus. Journal of the Arnold Arboretum 34: 163–175.

1368

•


Gray, N. E. 1962. A taxonomic revision of Podocarpus XIII. Section Polypodiopsis in the South Pacific. Journal of the Arnold Arboretum 43: 67–79. Gray, N. E., and J. T. Buchholz. 1948. A taxonomic revision of Podocarpus III. The American species of Podocarpus: section Polypodiopsis. Journal of the Arnold Arboretum 29: 117–122. Greenwood, D. R. 1987. Early Tertiary Podocarpaceae: Megafossils from the Eocene Anglesea locality, Victoria, Australia. Australian Journal of Botany 35: 111–133. Greenwood, W. 1975. Food plants or hosts of some Fijian insects. V. Proceedings of the Linnean Society of New South Wales 101: 237–241. Herbert, J., P. M. Hollingsworth, M. F. Gardner, R. R. Mill, P. J. Thomas, and T. Jaffré. 2002. Conservation genetics and phylogenetics of New Caledonian Retrophyllum (Podocarpaceae) species. New Zealand Journal of Botany 40: 175–188. Hermsen, E. J., and M. A. Gandolfo. 2016. Fruits of Juglandaceae from the Eocene of South America. Systematic Botany 41: 316–328. Hermsen, E. J., M. A. Gandolfo, and M. C. Zamaloa. 2012. The fossil record of Eucalyptus in Patagonia. American Journal of Botany 99: 1356–1374. Hill, R. S. 1994. The history of selected Australian taxa. In R. S. Hill [ed.], History of the Australian vegetation: Cretaceous to Recent, 390–419. Cambridge University Press, Cambridge, UK. Hill, R. S. 1995. Conifer origin, evolution and diversification in the Southern Hemisphere. In N. J. Enright and R. Hill, S. [eds.], Ecology of the southern conifers, 10–29. Smithsonian Institution Press, Washington, D.C., USA. Hill, R. S., and H. E. Merrifield. 1993. An Early Tertiary macroflora from West Dale, southwestern Australia. Alcheringa 17: 285–326. Hill, R. S., and M. S. Pole. 1992. Leaf and shoot morphology of extant Afrocarpus, Nageia and Retrophyllum (Podocarpaceae) species, and species with similar leaf arrangement, from Tertiary sediments in Australasia. Australian Systematic Botany 5: 337–358. Hooker, J. D. 1853. The botany of the Antarctic voyage of H.M. Discovery Ships Erebus and Terror in the years 1839–1843, under the command of Captain Sir James Clark Ross. II. Flora Novae-Zelandiae. Part I. Flowering plants. Reeve Brothers, London, UK. Hori, K., Y. Kondō, and K. Kuramochi. 1984. Feeding site of Palomena angulosa Motschulsky (Hemiptera: Pentatomidae) on potato plants and injury caused by the feeding. Applied Entomology and Zoology 19: 476–482. Iannelli, S. B., V. D. Litvak, L. Fernández Paz, A. Folguera, M. E. Ramos, and V. A. Ramos. 2017. Evolution of Eocene to Oligocene arc-related volcanism in the North Patagonian Andes (39–41°S), prior to the break-up of the Farallon plate. Tectonophysics 696–697: 70–87. Jaffré, T. 1988. Végétation et flore de la Chute de la Madeleine. Laboratoire de Botanique, ORSTOM, Nouméa, New Caledonia. Jaffré, T. 1995. Distribution and ecology of the conifers of New Caledonia. In N. J. Enright and R. S. Hill [eds.], Ecology of the southern conifers, 171–196. Smithsonian Institution Press, Washington, D.C., USA. Jaffré, T., P. Bouchet, and J.-M. Veillon. 1998. Threatened plants of New Caledonia: Is the system of protected areas adequate? Biodiversity and Conservation 7: 109–135. Jaffré, T., J. Munzinger, and P. P. Lowry II. 2010. Threats to the conifer species found on New Caledonia’s ultramafic massifs and proposals for urgently needed measures to improve their protection. Biodiversity and Conservation 19: 1485–1502. Jaramillo, C., and A. Cárdenas. 2013. Global warming and Neotropical rainforests: A historical perspective. Annual Review of Earth and Planetary Sciences 41: 741–766. Knight, C. L., and P. Wilf. 2013. Rare leaf fossils of Monimiaceae and Atherospermataceae (Laurales) from Eocene Patagonian rainforests and their biogeographic significance. Palaeontologia Electronica 16: article 16.3.26A. Knopf, P., C. Schulz, D. P. Little, T. Stützel, and D. W. Stevenson. 2012. Relationships within Podocarpaceae based on DNA sequence, anatomical, morphological, and biogeographical data. Cladistics 28: 271–299. Kooyman, R. M., P. Wilf, V. D. Barreda, R. J. Carpenter, G. J. Jordan, J. M. K. Sniderman, A. Allen, et al. 2014. Paleo-Antarctic rainforest into the modern Old World Tropics: The rich past and threatened future of the “southern wet forest survivors.” American Journal of Botany 101: 2121–2135.

Kuhn, P. P., H. Echtler, R. Littke, and G. Alfaro. 2010. Thermal basin modelling of the Arauco forearc basin, south central Chile—heat flow and active margin tectonics. Tectonophysics 495: 111–128. Labandeira, C. C., P. Wilf, K. R. Johnson, and F. Marsh. 2007. Guide to insect (and other) damage types on compressed plant fossils. Version 3.0. Smithsonian Institution, Washington, D.C., USA. http://paleobiology. si.edu/insects/index.html. Lawver, L. A., L. M. Gahagan, and I. W. D. Dalziel. 2011. A different look at gateways: Drake Passage and Australia/Antarctica. In J. B. Anderson and J. S. Wellner [eds.], Tectonic, climatic, and cryospheric evolution of the Antarctic Peninsula, 5–33. American Geophysical Union, Washington, D.C., USA. Leslie, A. B., J. M. Beaulieu, and S. Mathews. 2017. Variation in seed size is structured by dispersal syndrome and cone morphology in conifers and other nonflowering seed plants. New Phytologist. doi: 10.1111/nph.14456 Leslie, A. B., J. M. Beaulieu, H. S. Rai, P. R. Crane, M. J. Donoghue, and S. Mathews. 2012. Hemisphere-scale differences in conifer evolutionary dynamics. Proceedings of the National Academy of Sciences, USA 109: 16217–16221. Medina, F. A., H. H. Camacho, and E. C. Malagnino. 1990. Bioestratigrafía del Cretácico superior-Paleoceno marino de la Formación Lefípán, Barranca de los Perros, Río Chubut, Chubut. Actas del V Congreso Argentino de Paleontología y Bioestratigrafía, Tucumán, Argentina I: 137–142. Merkhofer, L., P. Wilf, M. T. Haas, R. M. Kooyman, L. Sack, C. Scoffoni, and N. R. Cúneo. 2015. Resolving Australian analogs for an Eocene Patagonian paleorainforest using leaf size and floristics. American Journal of Botany 102: 1160–1173. Mill, R. R. 2001. A new sectional combination in Nageia Gaertn. (Podocarpaceae). Edinburgh Journal of Botany 58: 499–501. Mill, R. R. 2016. A monographic revision of Retrophyllum (Podocarpaceae). Edinburgh Journal of Botany 73: 171–261. Mill, R. R., and R. S. Hill. 2004. Validations of the names of seven Podocarpaceae macrofossils. Taxon 53: 1043–1046. Orr, M. 1944. The leaf anatomy of Podocarpus. Transactions of the Botanical Society of Edinburgh 34: 1–54. Page, C. N. 1989. New and maintained genera in the conifer families Podocarpaceae and Pinaceae. Notes from the Royal Botanic Garden Edinburgh 45: 377–395. Page, C. N. 1990. Podocarpaceae. In K. Kubitzki [ed.], The families and genera of vascular plants, vol. 1: Pteridophytes and gymnosperms, 332–346. Springer, Heidelberg, Germany. Palazzesi, L., and V. Barreda. 2007. Major vegetation trends in the Tertiary of Patagonia (Argentina): A qualitative paleoclimatic approach based on palynological evidence. Flora 202: 328–337. Petersen, C. S. 1946. Estudios geológicos en la región del Río Chubut medio. Dirección de Minas y Geología Boletín 59: 1–137. Pole, M. S. 1992. Early Miocene flora of the Manuherikia Group, New Zealand. 2. Conifers. Journal of the Royal Society of New Zealand 22: 287–302. Pole, M. S. 1997. Miocene conifers from the Manuherikia Group, New Zealand. Journal of the Royal Society of New Zealand 27: 355–370. Pole, M. S. 2001. Can long-distance dispersal be inferred from the New Zealand plant fossil record? Australian Journal of Botany 49: 357–366. Pole, M. S. 2007. Conifer and cycad distribution in the Miocene of southern New Zealand. Australian Journal of Botany 55: 143–164. Pole, M. S., J. Dawson, and T. Denton. 2008. Fossil Myrtaceae from the early Miocene of southern New Zealand. Australian Journal of Botany 56: 67–81. Quiroga, M. P., P. Mathiasen, A. Iglesias, R. R. Mill, and A. C. Premoli. 2016. Molecular and fossil evidence disentangle the biogeographical history of Podocarpus, a key genus in plant geography. Journal of Biogeography 43: 372–383. Romero, E. J., M. C. Dibbern, and M. A. Gandolfo. 1988. Revisión de Lomatia bivascularis (Berry) Frenguelli (Proteaceae) del yacimiento de la Laguna del Hunco (Paleoceno), Pcia. del Chubut. Actas del IV Congreso Argentino de Paleontología y Bioestratigrafía, Mendoza 3: 125–130. Romero, E. J., and L. J. Hickey. 1976. A fossil leaf of Akaniaceae from Paleocene beds in Argentina. Bulletin of the Torrey Botanical Club 103: 126–131.


Sanders, J. G. 1905. The cottony maple scale (Pulvinaria innumerabilis Rathvon.). U.S. Department of Agriculture, Bureau of Entomology Circular No. 64. Government Printing Office, Washington, D.C., USA. Scasso, R. A., M. Aberhan, L. Ruiz, S. Weidemeyer, F. A. Medina, and W. Kiessling. 2012. Integrated bio- and lithofacies analysis of coarse-grained, tide-dominated deltaic environments across the Cretaceous/Paleogene boundary in Patagonia, Argentina. Cretaceous Research 36: 37–57. Schedl, K. E. 1965. Ein neuer Platypus aus Venezuela. Anzeiger für Schädlingskunde 38: 87. Silba, J. 1983. A new species of Decussocarpus de Laub. (Podocarpaceae) from Brazil. Phytologia 54: 460–462. Sinclair, W. T., R. R. Mill, M. F. Gardner, P. Woltz, T. Jaffré, J. Preston, M. L. Hollingsworth, et al. 2002. Evolutionary relationships of the New Caledonian heterotrophic conifer, Parasitaxus usta (Podocarpaceae), inferred from chloroplast trnL-F intron/spacer and nuclear rDNA ITS2 sequences. Plant Systematics and Evolution 233: 79–104. Stockey, R. A., and H. Ko. 1988. Cuticle micromorphology of some New Caledonian podocarps. Botanical Gazette (Chicago, Ill.) 149: 240–252. Veblen, T. T., J. J. Armesto, B. R. Burns, T. Kitzberger, A. Lara, B. León, and K. R. Young. 2005. The coniferous forests of South America. In F. Andersson [ed.], Coniferous forests, 293–317. Elsevier, Amsterdam, Netherlands. Vellekoop, J., F. Holwerda, M. B. Prámparo, V. Willmott, S. Schouten, N. R. Cúneo, R. A. Scasso, and H. Brinkhuis. 2017. Climate and sea-level changes across a shallow marine Cretaceous-Palaeogene boundary succession in Patagonia, Argentina. Palaeontology. Vicuña-Miñano, E., and J. Mostacero León. 2003. Notas sobre Podocarpáceas de cuatro Bosques Montanos de la provincia de San Ignacio—Cajamarca, Perú. Arnaldoa 10: 19–44. Villar de Seoane, L., N. R. Cúneo, I.H. Escapa, P. Wilf, and M. A. Gandolfo. 2015. Ginkgoites patagonica (Berry) comb. nov. from the Eocene of Patagonia, last ginkgoalean record in South America. International Journal of Plant Sciences 176: 346–363 [and Erratum, p. 364]. Wakgari, W. M., and J. H. Giliomee. 1998. Description of the stages of the white wax-scale, Ceroplastes destructor Newstead (Homoptera: Coccidae). African Entomology 6: 303–316. Wasscher, J. 1941. The genus Podocarpus in the Netherlands Indies. Blumea 4: 359–481. Wheeler, A. G. Jr. 1980. Life history of Plagiognathus albatus (Hemiptera: Miridae), with a description of the fifth instar. Annals of the Entomological Society of America 73: 354–356. Wilf, P. 2012. Rainforest conifers of Eocene Patagonia: Attached cones and foliage of the extant Southeast Asian and Australasian genus Dacrycarpus (Podocarpaceae). American Journal of Botany 99: 562–584.


• 1369

Wilf, P. 2017. Image library: Retrophyllum spiralifolium Wilf, Retrophyllum superstes Wilf, and Retrophyllum araucoensis (Berry) Wilf, doi 10.6084/ m9.figshare.5305420. Wilf, P., M. R. Carvalho, M. A. Gandolfo, and N. R. Cúneo. 2017. Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae. Science 355: 71–75. Wilf, P., N. R. Cúneo, I. H. Escapa, D. Pol, and M. O. Woodburne. 2013. Splendid and seldom isolated: The paleobiogeography of Patagonia. Annual Review of Earth and Planetary Sciences 41: 561–603. Wilf, P., N. R. Cúneo, K. R. Johnson, J. F. Hicks, S. L. Wing, and J. D. Obradovich. 2003. High plant diversity in Eocene South America: Evidence from Patagonia. Science 300: 122–125. Wilf, P., and I. H. Escapa. 2015. Green Web or megabiased clock? Patagonian plant fossils speak on evolutionary radiations. New Phytologist 207: 283–290. Wilf, P., and I. H. Escapa. 2016. Molecular dates require geologic testing. New Phytologist 209: 1359–1362. Wilf, P., I. H. Escapa, N. R. Cúneo, R. M. Kooyman, K. R. Johnson, and A. Iglesias. 2014. First South American Agathis (Araucariaceae), Eocene of Patagonia. American Journal of Botany 101: 156–179. Wilf, P., K. R. Johnson, N. R. Cúneo, M. E. Smith, B. S. Singer, and M. A. Gandolfo. 2005. Eocene plant diversity at Laguna del Hunco and Río Pichileufú, Patagonia, Argentina. American Naturalist 165: 634–650. Wilf, P., S. A. Little, A. Iglesias, M. C. Zamaloa, M. A. Gandolfo, N. R. Cúneo, and K. R. Johnson. 2009. Papuacedrus (Cupressaceae) in Eocene Patagonia: A new fossil link to Australasian rainforests. American Journal of Botany 96: 2031–2047. Wilf, P., D. W. Stevenson, and N. R. Cúneo. 2016. The last Patagonian cycad, Austrozamia stockeyi gen. et sp. nov., early Eocene of Laguna del Hunco, Chubut, Argentina. Botany 94: 817–829. Wood, S. L. 1971. New records and species of American Platypodidae (Coleoptera). The Great Basin Naturalist 31: 243–253. Wood, S. L., and D. E. Bright Jr. 1992. Index for Scolytidae. Great Basin Naturalist Memoirs 13: 1460–1553. Zachos, J. C., G. R. Dickens, and R. E. Zeebe. 2008. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451: 279–283. Zamaloa, M. C., M. A. Gandolfo, C. C. González, E. J. Romero, N. R. Cúneo, and P. Wilf. 2006. Casuarinaceae from the Eocene of Patagonia, Argentina. International Journal of Plant Sciences 167: 1279–1289. Ziegler, A. M., G. Eshel, P. M. Rees, T. A. Rothfus, D. B. Rowley, and D. Sunderlin. 2003. Tracing the tropics across land and sea: Permian to present. Lethaia 36: 227–254.