First South American Agathis (Araucariaceae), Eocene of Patagonia.

American Journal of Botany 101(1): 156–179. 2014.

FIRST SOUTH AMERICAN AGATHIS (ARAUCARIACEAE), EOCENE OF PATAGONIA1 PETER WILF2,7, IGNACIO H. ESCAPA3, N. RUBÉN CÚNEO3, ROBERT M. KOOYMAN4, KIRK R. JOHNSON5, AND ARI IGLESIAS6 2Department

of Geosciences, Pennsylvania State University, University Park, Pennsylvania 16802 USA; 3Museo Paleontológico Egidio Feruglio, Consejo Nacional de Investigaciones Científicas y Técnicas, Trelew 9100, Chubut, Argentina; 4National Herbarium of New South Wales, Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney 2000, New South Wales, Australia; 5National Museum of Natural History, Smithsonian Institution, Box 37012 MRC 106, Washington, D.C. 20013 USA; and 6División Paleontología, Universidad Nacional del Comahue, Instituto de Investigaciones en Biodiversidad y Ambiente–Consejo Nacional de Investigaciones Científicas y Técnicas, San Carlos de Bariloche 8400, Río Negro, Argentina. • Premise of the study: Agathis is an iconic genus of large, ecologically important, and economically valuable conifers that range over lowland to upper montane rainforests from New Zealand to Sumatra. Exploitation of its timber and copal has greatly reduced the genus’s numbers. The early fossil record of Agathis comes entirely from Australia, often presumed to be its area of origin. Agathis has no previous record from South America. • Methods: We describe abundant macrofossils of Agathis vegetative and reproductive organs, from early and middle Eocene rainforest paleofloras of Patagonia, Argentina. The leaves were formerly assigned to the New World cycad genus Zamia. • Key results: Agathis zamunerae sp. nov. is the first South American occurrence and the most complete representation of Agathis in the fossil record. Its morphological features are fully consistent with the living genus. The most similar living species is A. lenticula, endemic to lower montane rainforests of northern Borneo. • Conclusions: Agathis zamunerae sp. nov. demonstrates the presence of modern-aspect Agathis by 52.2 mya and vastly increases the early range and possible areas of origin of the genus. The revision from Zamia breaks another link between the Eocene and living floras of South America. Agathis was a dominant, keystone element of the Patagonian Eocene floras, alongside numerous other plant taxa that still associate with it in Australasia and Southeast Asia. Agathis extinction in South America was an integral part of the transformation of Patagonian biomes over millions of years, but the living species are disappearing from their ranges at a far greater rate. Key words: Río Pichileufú.

Agathis; Araucariaceae; Argentina; Borneo; conifers; Eocene; extinction; Laguna del Hunco; rainforests;

Agathis R. A. Salisbury (Araucariaceae; kauri, dammar) is one of the most impressive and valuable tree genera in the world, but little is known about its evolutionary and biogeographic history. Several recent molecular-clock studies have given a wide range of estimates of its age (Knapp et al., 2007; Biffin et al., 2010; Crisp and Cook, 2011; Leslie et al., 2012). We begin with a brief introduction to living Agathis, followed

by an overview of its limited fossil record, which was, until now, entirely from Australia and New Zealand. Living Agathis—Agathis has ca. 17 species distributed across lowland to upper montane rainforests in Australasia and Southeast Asia (Table 1). Agathis has broad leaves, outlives most competing canopy angiosperms, and characteristically emerges above them at giant size (several species reach 50–65 m height). The genus is a backbone element of forest architecture and element cycling, supports diverse epiphytes and fungi, and is an important source of animal food, shade, roosting space, and shelter (Dumbleton, 1952; Mirams, 1957; Wise, 1962; Ripley, 1964; Gorman, 1975; Towns, 1981; Ecroyd, 1982; Enright and Ogden, 1987; Bishop, 1992; Greene, 1998; Silvester and Orchard, 1999; Jongkind et al., 2007; Verkaik and Braakhekke, 2007; Wyse, 2012). Most areas where Agathis grows are rainforests with many rare or endemic species of plants and animals (e.g., Enright, 1995; Wong and Phillipps, 1996; Morrogh-Bernard et al., 2003; Balete et al., 2009; Wilcove et al., 2013). Agathis can be an important component of tropical peatlands (Yii, 1995), whose organic carbon flux has increased ca. 32% since 1990 in Southeast Asia as a result of disturbance (Moore et al., 2013). Thus, Agathis removal and related disturbance on a large scale are likely to have significant detrimental effects on carbon balance, biodiversity, and ecosystem structure and function. Human impacts on Agathis populations are indeed enormous (Whitmore, 1977, 1980a; Bowen and Whitmore, 1980a, 1980b;

1 Manuscript received 9 September 2013; revision accepted 21 November 2013. The authors thank M. Caffa, L. Canessa, B. Cariglino, M. Carvalho, M. Gandolfo, C. González, R. Horwitt, M. Gandolfo, E. Hermsen, K. Kitayama, S. Little, H. Mujih, P. Puerta, L. Reiner, E. Ruigómez, and S. Wing for their extraordinary assistance in the field and laboratory and/or helpful and timely comments; the staff at CANB (B. Lepschi and C. Cargill), NSW (L. L. Lee and L. Murray), US (A. Clark, I. Lin, K. Rankin, and R. Russell), and USNM (J. Wingerath) for expediting specimen access and loans; and the Nahueltripay family and Instituto de Investigaciones Aplicadas for land access. This work received primary support from National Science Foundation grants DEB-0919071, DEB-0918932, and DEB-0345750 and from the David and Lucile Packard Foundation, as well as early support from National Geographic Society grant 7337-02, the University of Pennsylvania Research Foundation, and the Andrew W. Mellon Foundation. 7 Author for correspondence (e-mail: [email protected])

doi:10.3732/ajb.1300327

American Journal of Botany 101(1): 156–179, 2014; http://www.amjbot.org/ © 2014 Botanical Society of America

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99% loss) in only ca. 50 yr (Whitmore, 1977; Farjon, 2010). Agathis microstachya (Australia) lost about half its population, and A. dammara (Malesia) has been reduced by ≥30% (Farjon, 2010). In New Caledonia, nickel mining impacts have greatly reduced Agathis populations, as well as logging (Farjon, 2010; Jaffré et al., 2010). In addition, Agathis is especially resiniferous (Salisbury, 1807), and its Manila copal was extensively tapped and dug from underground deposits (“gum-digging”) for diverse industrial uses (Kirk, 1889; Soerianegara et al., 1993; Mabberley, 2002). The remaining populations of several species have limited protection in nature reserves, but many of these are vulnerable to poaching, degazetting, clearing of surrounding buffer areas, and climate change. As adjacent lowlands are cleared and pressures from marginal tropical agriculture move upslope, the montane populations of Agathis are increasingly threatened. Agathis reproductive organs and adult foliage are notoriously difficult to sample without felling or shooting (Howcroft, 1987). They are mostly borne above long trunks that are dangerous to climb because of copious slippery resin and abscision of the lower branches. Many species are endemic to very remote or steep montane areas. Also, the large, globose seed cones shatter at maturity. Even when well sampled, there is little morphological variation among the species, such that minute technical characters of pollen cones found in the litter are usually needed to identify a giant tree (Meijer Drees, 1940; Whitmore, 1980b). As a result, detailed knowledge of morphological and genetic variation—and, thus, a solid systematic framework—have not yet been established for Agathis. Even the two most recent treatments differ substantially in species delimitations (Eckenwalder, 2009; Farjon, 2010). Fossil Agathis— The evolutionary and biogeographic history of Agathis remains poorly known from the fossil record, in sharp contrast to the outstanding, global Mesozoic and Southern Hemisphere Cenozoic fossil record of its familial relative Araucaria. There is a long history of uncertain or dubious identifications of Mesozoic and Cenozoic material to Agathis, as discussed elsewhere (Seward and Ford, 1906; Florin, 1940a;

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Stockey, 1982; Hill, 1994; Brodribb and Hill, 1999; Hill et al., 2008; Pole, 2008). According to the most recent reviews (Hill et al., 2008; Pole, 2008), the only reliable fossil Agathis occurrences are Cenozoic and from the limited area of southern Australia, late Paleocene to early Miocene, and New Zealand, late Oligocene–Miocene. While clearly suggesting a Gondwanan origin for what is now mostly a tropical genus, nearly all these fossil occurrences are of leaf fragments with in situ cuticle or of dispersed cuticles, and several of the interpretations are contentious. Agathis tasmanica R. S. Hill and Bigwood (1987), early Oligocene of Little Rapid River and Cethana, Tasmania, is one of the few examples that convincingly preserves the complete leaf form. This includes the typical Agathis short petiole (“false petiole,” sensu Offler, 1984), the basal constriction of the blade that is not found in the other living Araucariaceae, Araucaria Juss. and Wollemia W. G. Jones et al., nor in the extinct Araucarioides Bigwood and R. Hill, which co-occurs with Agathis and Araucaria in Cenozoic sediments of Tasmania (Bigwood and Hill, 1985; Hill et al., 2008). Pole (2008) disputed some of the other Australian examples as potentially belonging to other genera. In New Zealand, abundant but isolated leaves from Newvale Mine (Oligocene–Miocene) were first assigned to Agathis sp. aff. A. australis (Lee et al., 2007) and later to Agathis sp. (Jordan et al., 2011); these were stated to lack petioles (although no leaf base was shown), which is unusual for Agathis but does occur on adult leaves of A. australis (Kirk, 1889), and to have a sharply acute apex, a feature found in few living Agathis species and not in A. australis (Offler, 1984; see also Hill et al., 2008). Moreover, Pole (2008) found the cuticular characters of the Newvale Mine fossils inconclusive. The possibility remains that the Newvale Mine fossils represent a species of Araucariaceae outside of Agathis. Regarding reproductive organs, Cookson and Duigan (1951) reported two seed cones and one pollen cone containing araucariaceous pollen, both associated with Agathis yallournensis Cookson and Duigan leaves (Oligocene–Miocene, Victoria), that they considered to be reproductive organs of A. yallournensis. Although the pollen cone did not preserve basal bracts, the remaining features are consistent with Agathis and distinct (as discussed by Cookson and Duigan) from Araucaria pollen cones also found at the site with associated Araucaria lignitici leaves. Otherwise, Agathis pollen cones have no fossil record prior to the present study, although they are the principal organs that show variation reliably at the species level (Whitmore, 1980b; Farjon, 2010) and, thus, are essential for any refined interpretation of fossils. The oldest previously illustrated fossil of a likely bract-scale unit (here, “cone scale” as widely used) dispersed from an Agathis seed cone is from the early Oligocene Cethana flora of Tasmania ( Carpenter et al., 1994), although Agathis cone scales have been mentioned without illustration from the late Eocene Vegetable Creek flora, New South Wales (Hill, 1995). In New Zealand, a late Miocene cone scale and leaf base from the Oruawharo locality (Pole, 2008)

←

in the inset, showing an attached leaf base with obliquely raised, darkened abscision zone; upper arrow expands to Fig. 10. 3. Spray with three abscision scars on one side of twig opposite the attached leaves, small terminal bud, and insect-feeding damage. MPEF-Pb 6303b, from quarry LH6. 4. Spray showing opposite branching, prominent grooves on twigs, numerous abscision scars with supporting tissues decurrent on the twig, well-preserved leaf bases with twisted petioles, and large, scaly terminal bud subtended by a prominent growth-increment scar. MPEF-Pb 6319, from LH25. 5. Spray showing opposite branching, two terminal buds (arrows), copious amber preserved as white, longitudinal stripes in twigs and leaves (note long distal leaf). MPEF-Pb 6313, from LH13. 6. Spray with terminal bud, weathered white. MPEF-Pb 6304b, from LH6. 7. Spray portion showing twisted leaf bases and large, scaly terminal bud. MPEF-Pb 6321a, from LH27 (also Fig. 8).

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Figs. 8–15. Agathis zamunerae sp. nov., twig features, from Laguna del Hunco except Fig. 10, from Río Pichileufú. Arrows with same orientations indicate corresponding points. 8. Detail of terminal bud shown in Fig. 7, under partial epifluorescence, showing overlapping, closely adpressed bud scales and remnant surface relief. 9. Spray portion showing small terminal bud and subtending pair of opposite leaves. Note abundant amber (white). MPEF-Pb 6312, from LH13. 10. Detail of twig at a leaf attachment point (corresponding to upper arrow in Fig. 1), showing grooved twig and leaf divergences typical for Agathis in a historical specimen. 11. Well-preserved twig with one remaining attached leaf, strong longitudinal grooves, several (sub)opposite, decussate abscision scars, swellings, and breakage scars. MPEF-Pb 6305a (left), b (right and Figs. 12–14), from LH6. 12. Detail, well-developed grooves and ridges and blanketing mesh of tiny, quadrangular epidermal cells of the former green twig. 13. Detail, grooves and epidermal cells. 14. Detail of dark, raised abscision scar supported by woody supply tissues extending from the twig. 15. Composite image (9 panels) of a grooved twig, apical direction to right, with several opposite decussate pairs of abscision scars and one attached leaf at right (three others attached to this twig are outside of frame). MPEF-Pb 6320b, from LH27.

provide a more convincing, though younger example of fossil Agathis than the Newvale Mine fossils mentioned above. Given the sparse, fragmentary record, the fossils so far assigned to Agathis may or may not represent plants that had abundant features of the living genus. Based on the known fossil record exclusive to Australia and New Zealand, it has long been suggested that Agathis probably evolved in those areas

(Florin, 1963:181; Gilmore and Hill, 1997; Hill and Scriven, 1998; Kunzmann, 2007). Likewise, no fossil or native living Agathis has previously been recorded from South America. The Eocene fossil sites of Patagonia are producing a large number of extant conifer, fern, and angiosperm genera that show trans-Antarctic connections to fossil and extant Australasian floras (see Materials and Methods). These occurrences

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Figs. 16–24. Agathis zamunerae sp. nov., leaves. Note dark abscision scars with elliptical cross sections, well-defined petioles, blunt apices, range of aspect ratios, and parallel, straight venation. Figs. 17 and 23, Río Pichileufú (arrows show corresponding points), others from Laguna del Hunco. 16. Leaf with abundant coalified mesophyll. MPEF-Pb 6365, from LH13. 17. Specimen figured as “Zamia tertiaria” by Berry (1938: pl. 8, fig. 4, USNM 40378f counterpart). Note typical Agathis features listed above, plus abundant, longitudinal amber casts of the resin ducts (also Fig. 23). 18. MPEF-Pb 6363, from LH13. 19. MPEF-Pb 6374, from LH27 (also Figs. 26, 27, and 30). 20. MPEF-Pb 6359a, from LH13 (also Figs. 21 and 22). 21, 22. Details at and near base of MPEF-Pb 6359a (Fig. 20), showing constricted petiole and bifurcating veins. 23. Detail, left-margin of leaf in Fig. 17, showing resin ducts (white amber casts) alternating with veins (dark, coalified). 24. Petiole detail, showing elliptical cross section. MPEF-Pb 6334, from LH6.

notably include evidence for the other two extant genera of Araucariaceae: Wollemia-type pollen (Dilwynites) has recently been discovered in the early middle Eocene Ligorio Márquez

Formation in Santa Cruz Province, Argentina, although some living species of Agathis can produce similar pollen (Macphail et al., 2013; Macphail and Carpenter, 2013), and Araucaria

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Figs. 25–31. Agathis zamunerae sp. nov., fine leaf-surface features, all with long axis of leaf vertical and apex upward, Laguna del Hunco. All under epifluorescence except Fig. 27. 25. Set of parallel veins, no stomata preserved. MPEF-Pb 6386, from LH27. 26, 27. Veins with intervening rows of numerous, coalified, randomly oriented Florin rings, from leaf shown in Fig. 19 (also Fig. 30). Same approximate leaf area under epifluorescence (Fig. 26) and under reflected light to show visual cues as under a hand lens (Fig. 27), corresponding Florin rings circled. 28. As in Fig. 26, different leaf, with resin duct remains (white amber cast) and coalified mesophyll. MPEF-Pb 6322b, from LH27 (also Figs. 29 and 31). 29. Detail from leaf shown in Fig. 28 (also Fig. 31). 30. Guard cell casts preserved within coalified Florin rings, from leaf shown in Figs. 19, 26, and 27. 31. Guard cell cast, from leaf shown in Figs. 28 and 29.

macrofossils have long been known from many Patagonian sites (Panti et al., 2012), including those studied here (Berry, 1938; Wilf et al., 2005). In his classic monograph on the middle Eocene Río Pichileufú flora of Río Negro Province, Argentina, Berry (1938) illustrated a number of foliar specimens, several attached to axes (Figs. 1 and 2), that he assigned to the putative cycad “Zamia” tertiaria Engelhardt (1891), a name based on a fragmentary leaf fossil from Eocene deposits in Chile. Zamia L. is an entirely New World genus. We have recovered numerous new specimens of “Zamia tertiaria” sensu Berry 1938 at Río Pichileufú

and, especially, from the early Eocene Laguna del Hunco flora, where it is the seventh most abundant leaf type among >150 overall, and by far the most common gymnosperm leaf type (Wilf et al., 2005: fig. 3). The leaves also preserve a notable richness of insect-feeding damage, under separate study (C. C. Labandeira et al., unpublished data). A priori, this high relative abundance of broad fossil leaves, indicating very significant biomass (e.g., Burnham et al., 1992) and a large component community, seemed very unlikely for a presumably small cycad species within a forest of tall rainforest trees (e.g., Wilf, 2012), and it became clear from a number of features, especially the bumpy

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Figs. 32–36. Agathis zamunerae sp. nov., (presumed) immature seed cone from Laguna del Hunco, terminal on a thickened branch, with large, transverse growth increment scar (rightward arrows). Numerous imbricate, upturned cone-scale apices are preserved across the cone base as impressions with very low but visible relief, their distal margins coalified, forming a pattern of numerous, darkened, concave-downward arcs (the margins) capping slight bulges in the matrix (the apex impressions). MPEF-Pb 6391b, from LH27. Arrows with same orientations indicate corresponding points. Fig. 35 equals Fig. 34 with colors reversed. 32. Whole specimen. 33. Detail of the area preserving cone-scale impressions/margin compressions, subtended by the growth increment scar, composite image under low-angle light. 34–36. Details of surface.

twigs with well-defined terminal buds and decussate phyllotaxy, that “Z. tertiaria” sensu Berry 1938 is a conifer with simple leaves, not a compound-leaved cycad. Here, we show that “Z. tertiaria” leafy branches and isolated leaves from Eocene Patagonia (Figs. 1–31), and a suite of newly discovered, associated female and male reproductive organs (Figs. 32–72), can all be assigned to a new fossil species of Agathis. Agathis is revealed as the dominant conifer of Eocene Patagonian rainforests, where it presumably towered over many of the same taxa that it associates with today in Australasia and Southeast Asia and had equally great ecological importance.

MATERIALS AND METHODS Laguna del Hunco and Río Pichileufú—The early Eocene Laguna del Hunco flora (LH, ca. 52.2 mya) and the early middle Eocene Río Pichileufú flora (RP, ca. 47.7 mya) come from northwestern Chubut and western Río Negro provinces, respectively, in northwestern Patagonia, Argentina. Locality information, maps, and stratigraphic and geochronologic data have been given in several recent papers (e.g., Wilf et al., 2003; Wilf, 2012). These classic sites were first reported in the 1920s and 1930s (Berry, 1925, 1935a, b, c, 1938) and preserve fossiliferous caldera-lake deposits within a regional volcanic province (Aragón and Romero, 1984; Aragón and Mazzoni, 1997). Paleontological and geological investigations at Laguna del Hunco and Río Pichileufú have increased greatly over the past decade. As recently reviewed (Wilf et al., 2009; Wilf, 2012): the

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Figs. 37–39. Agathis zamunerae sp. nov., cone scale with in situ seed, Laguna del Hunco. MPEF-Pb 6398, from LH13. The seed is preserved mostly as a very thin sediment cast, with some dark organic material remaining in the seed body. The rounded, larger wing (extending to distal left in this view) is broken near its apex. The rudimentary wing is clearly visible, extending to distal right (in this view) from the seed body. 37, 38. Standard image and grayscale-inverted duplicate. 39. Composite of 84 images in 44 panels, each taken with very low-angle, unidirectional lighting to show fine-scale relief features. In addition to the seed remains, note typical Agathis cone-scale features as detailed in next plate.

ages are well onstrained from recent 40Ar-39Ar analyses and supplemented at Laguna del Hunco by paleomagnetic data from a 170-m stratigraphic section; the paleoenvironments were similar to those of Australasian subtropical and montane tropical rainforests; the fossil compression floras and their insect damage are among the most diverse known in the world; and a large number of novel insect taxa are present, along with fish and other vertebrate fossils. A striking biogeographic pattern emerging from recent systematic studies is the Gondwanan signature from the numerous plant taxa that are found at Laguna del Hunco, or from both Laguna del Hunco and Río Pichileufú, that are extant in Australasian rainforests and often extinct in South America. In addition, many of these elements are commonly associated with each other, and with Agathis, in their extant ranges. The long and growing list of “southern connection” examples from one or both of these floras, many of which constitute the only fossil occurrences of the respective taxon in South America, requires updating here. Ferns include Todea (Osmundaceae; extant in New Zealand, Australia, New Guinea, and southern Africa; Carvalho et al., 2013) and Dicksonia (Dicksoniaceae; Malesia, Australia, New Caledonia, New Zealand, South and Central America; Berry, 1938; Carvalho et al., 2013). Broadleaved conifers, which collectively provide the most significant evidence for a rainforest environment with a tall canopy, include Papuacedrus (Cupressaceae; New Guinea and Moluccas; Wilf et al., 2009); Araucaria section Eutacta (Australasia; Berry, 1938) and Agathis reported here; and in the Podocarpaceae, Podocarpus (global, primarily Southern Hemisphere; Berry, 1938), Dacrycarpus (Australasia and Southeast Asia; Florin, 1940a; Wilf, 2012), Acmopyle (Fiji and New Caledonia;

Florin, 1940b; Wilf, 2012), and an undescribed species of Retrophyllum (Fiji, New Caledonia, Moluccas, Neotropics; Wilf, 2012). Basal (noneudicot) angiosperms include leaves of the primarily Gondwanan families Atherospermataceae and Monimiaceae that are most similar to the living Australian genera Daphnandra and Wilkiea, respectively (Berry, 1935c; Knight and Wilf, 2013). Eudicots include the iconically Australian Eucalyptus (Myrtaceae; Gandolfo et al., 2011; Hermsen et al., 2012), thought to represent colonization of volcanically deforested areas adjacent to standing rainforest; Akania (Akaniaceae, Australia; Romero and Hickey, 1976; Gandolfo et al., 1988); three species of Gymnostoma (Casuarinaceae; Malesia, Australia, Southeast Asia; Zamaloa et al., 2006); several Cunoniaceae, including fruits likely to represent Weinmannia (Andes, New Zealand, Malesia, Madagascar) and Ceratopetalum (Australia and New Guinea; Gandolfo and Hermsen, 2012); and diverse Proteaceae, including Orites (Australia, South America; González et al., 2007). It is noteworthy that no genus currently endemic to the Americas has so far been verified at Laguna del Hunco or Río Pichileufú. Several historical examples of endemics have turned out, after systematic revision, to represent taxa now extinct in South America (e.g., Austrocedrus/Libocedrus to Papuacedrus, Fitzroya to Dacrycarpus, and here Zamia to Agathis). Provenance and repositories—Material reported here mostly includes collections made during expeditions from Museo Paleontologico Egidio Feruglio (MEF, Trelew, Chubut, Argentina): to Laguna del Hunco in 1999, 2002, 2004, 2006, and 2009, from quarries LH2, LH4, LH6, LH10, LH13, LH15, LH22, LH23, LH25, and LH27, from float rocks, and from quarry AL-1, located 5 km

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Figs. 40–51. Agathis zamunerae sp. nov., additional cone scales. Note typical Agathis features: basal scallops, large seed-depressions, concave-upward, asymmetrical seed-detachment scars, rounded upper corners, and thickened to recurved distal margins. All from Laguna del Hunco except Figs. 50 and 51, from Río Pichileufú. 40, 41. Specimens showing prominent seed depressions, detachment scars, and recurved apices. MPEF-Pb 6393 and MPEFPb 6392b, respectively, both from LH6. 42, 43. Details of seed-detachment scars for specimens shown in Figs. 40 and 41, respectively. Note preserved relief, admedially curving architecture below scar, and exmedially curving architecture above. 44. Detail of hooked left basal scallop of specimen shown in Fig. 41. 45. Specimen with deep seed depression and adjacent-ovule impression at basal right (arrow). MPEF-Pb 6397, from LH15. 46, 47. Specimen showing shallow left-basal kink and deep right-basal scallop (hooked tip broken). MPEF-Pb 6396, from LH13. 48. Specimen with deep seed depression. MPEF-Pb 6394a, from LH13. 49. Small scale, presumably from near the base or apex of its cone. MPEF-Pb 6395b, from LH13. 50, 51. BAR 4752 and BAR 4751, respectively, both from RP3.

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Figs. 52–61. Agathis zamunerae sp. nov., pollen cones. Note typical Agathis features: variably short to long peduncles, cluster of rounded, spoonshaped basal bracts, and peltate microsporophylls with thick stalks and rounded distal margins. Microsporophylls preserved in both external and lateral view, often on the same cone (e.g., Fig. 54). 52, 53. Holotype of A. zamunerae, part and counterpart, MPEF-Pb 6399a and 6399b, respectively, from LH6 (also Figs. 62 and 70–72). Note quadrangular cross section of the long peduncle (Fig. 53) and one basal bract pulled down, showing its inner surface (also

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south of the main section; and to Río Pichileufú in 2002 and 2005, from quarry RP3 and near quarry RP1, all as described in earlier studies (Wilf et al., 2003, 2005, 2009; Gandolfo et al., 2011; Wilf, 2012). The Laguna del Hunco collections from these field seasons are curated at MEF (repository prefix MPEF-Pb), and the Río Pichileufú specimens are curated at Museo de Paleontología de Bariloche (BAR), San Carlos de Bariloche, Río Negro, Argentina; letter suffixes (a, b) indicate parts and counterparts. A few additional specimens from Río Pichileufú were found in older collections at BAR. Also, we examined the historical collections of “Zamia tertiaria” from Río Pichileufú (Berry, 1938) that were collected and sent to Berry by J. R. Guiñazu, exact quarry sites unknown. This included previously uncited and unfigured cohort material as well as the figured specimens, all housed at the National Museum of Natural History, Smithsonian Institution (USNM). The small type and cohort collections from Laguna del Hunco (Berry, 1925), also located at USNM, consist entirely of angiosperm remains and, thus, are not relevant to the present study. The total collection presented here as protologue for a new species contains 154 elements: 1 twig, 36 leafy twigs, 86 isolated leaves, 1 immature seed cone, 10 seed-cone scales (1 of these with an in situ seed), and 20 pollen cones. Nearly all the fertile material is from Laguna del Hunco, which has much better preservation, but we also found three cone scales at Río Pichileufú. The new species is most common in the uppermost well-sampled level at LH (quarries LH6, 22, 25, and 27; 47% of total specimens). Fossil preparation and imaging—Techniques, software, locations, and equipment for fossil preparation, macro- and microphotography, epifluorescence microphotography, and image compositing and processing at MEF and the Penn State University Paleobotany Laboratory are the same as those reported in the recent, preceding paper on fossil conifers from these sites (Wilf, 2012), with the following minor technical notes. First, in addition to the PaleoAro and Micro-Jack #2 air scribes listed previously (Wilf, 2012), we also used the more powerful ME-9100 for fossil preparation when needed (all from Paleotools, Brigham City, Utah, USA). Second, very low-angle, unidirectional light was often used to bring out fine surface features, especially for pollen cones and cone scales; image contrast was usually set high, and some image colors were inverted (Figs. 35 and 38) to make important fine features of the fossils more visible. Third, for some epifluorescence imaging of specimens that showed low excitation response and required long exposures, a small amount of normal reflected light was sometimes allowed to mix into the exposure along with the fluorescence, with good results that better showed surface textures in combination with the dimly fluorescing features (e.g., Fig. 8, “partial epifluorescence”). All photographs are by P.W., except Figures 49–51 (I.H.E.). Field photographs in Borneo were taken on a Sony DSC-RX100 compact camera. Cuticle was usually coalified, with remnants of epidermal cells sometimes visible under epifluorescence. Only two leaf specimens preserved traces of stomatal apparati preserved as coalified Florin rings, some with guard-cell casts (e.g., Figs. 30 and 31). Extant material and characters—Herbarium collections of Agathis, comprising most of the living species, were examined by P.W. at the U.S. National Herbarium, Smithsonian Institution, Washington, D.C. (US); the Australian National Herbarium, Canberra (CANB); the National Herbarium of New South Wales, Royal Botanic Gardens, Sydney (NSW); and Royal Botanic Gardens, Kew (K). In addition, P.W. and R.M.K. examined wild Agathis trees extensively in the field, in the Atherton Tablelands region of Queensland, Australia, in August 2010 (A. atropurpurea, A. microstachya, and A. robusta), and on and around Mount Kinabalu in northern Borneo, Sabah, Malaysia, in September 2012 (A. borneensis, A. kinabaluensis, and A. lenticula). Collectively, the authors have examined all living species of Araucariaceae in herbaria, in the field, and/or in cultivation. Although it is an easily recognized genus, the species-level taxonomy of Agathis remains contentious, as seen in the large number of disagreements among the principal modern treatments (de Laubenfels, 1972, 1988; Whitmore, 1980b;

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Eckenwalder, 2009; Farjon, 2010). Moreover, even agreed-upon names can incorporate varying sets of synonymized taxa and reference specimens and, thus, are not consistent in practical use. Here, we use Farjon’s (2010) treatment because of its relatively detailed coverage of reproductive morphology; unless otherwise noted, Farjon (2010) is the source of all nomenclature and measurements of extant conifer species mentioned below. However, all descriptions and comments made in the principal treatments cited above were tabulated and also used in the comparisons, if it was possible to adjust for synonymies. A general comparative summary of principal measurements and character states for the new fossil species, and for the extant species as described by Farjon (2010), is given in Table 1 (for additional comparisons, see Description and Discussion). As would be expected from the unsettled species-level taxonomy and generally poor genetic sampling of Agathis, there is no robust systematic framework of all the species into which to place the fossils, and no phylogenetic analysis was attempted here. Numerous recent papers have produced variable results for relationships within Agathis (e.g., Gilmore and Hill, 1997; Setoguchi et al., 1998; Stefanović et al., 1998; Conran et al., 2000; Quinn et al., 2002; Stöckler et al., 2002; Rai et al., 2008; Liu et al., 2009; Biffin et al., 2010; Leslie et al., 2012; Escapa and Catalano, 2013). Critically, the living species that we found to have greatest morphological similarity to the fossils (A. lenticula; see Discussion) has never been analyzed in a phylogenetic context with either morphological or molecular data. Thirteen (the maximum to date) Agathis species were included in a recent molecular analysis as part of a large-scale study of all conifer groups (Leslie et al., 2012). This showed Wollemia as sister to Agathis, Agathis australis of New Zealand as sister to all other sampled Agathis species, a clade containing the New Caledonian species, and a clade containing the three Australian species (A. atropurpurea, A. microstachya, and A. robusta; Hyland, 1977) that is sister to the remaining West Pacific-Asian tropical species. The distinct position of A. australis and the consistency of the New Caledonian clade appear to be robust in other studies (e.g., Escapa and Catalano, 2013), and the status of Wollemia as sister to Agathis, and of both together as sister to Araucaria, is the prevailing result from many molecular analyses (Gilmore and Hill, 1997; Stefanović et al., 1998; Conran et al., 2000; Quinn et al., 2002; Rai et al., 2008; Liu et al., 2009; Biffin et al., 2010; Escapa and Catalano, 2013). To evaluate the phylogenetic position of this and other fossil species of Agathis, the previously developed morphological matrix of Escapa and Catalano (2013) needs to be expanded to include additional living species and detailed characters of microsporophyll morphology.

SYSTEMATICS AND RESULTS Family— Araucariaceae J. B. Henkel & W. Hochstetter, Synopsis der Nadelhölzer: xvii (1865), nom. cons. Genus— Agathis R. A. Salisbury, Transactions of the Linnean Society of London 8: 311 (1807), nom. cons. Species— Agathis zamunerae Wilf, sp. nov. Coniferales, morphotypes TY010 “Zamia” tertiaria, “TY012 “Araucariaceae pollen cone” (part), and TY014 “Araucaria wide cone scale” (Wilf et al., 2005: A6). Zamia tertiaria Engelhardt, Geological Society of America Special Paper 12: 57 (1938), cited Río Pichileufú material only. Etymology— In memory of the life and work of Dra. Alba B. Zamuner, 1959–2012, paleobotanist and valued colleague (see Iglesias, 2013).

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Fig. 62). Fig. 52 arrows: thin arrow corresponds to same in Figs. 70 and 71; thick arrow corresponds to same in Fig. 72. 54. Specimen with short peduncle and exposed cone axis. MPEF-Pb 6403a, from LH13 (also Fig. 66). 55. Specimen with long peduncle and well-preserved bract cluster. MPEF-Pb 6402, from LH13 (also Figs. 63–65). 56. MPEF-Pb 6409a, from LH25. 57. Specimen exhibiting cone axis and numerous individual microsporophylls in lateral view, showing thick, reflexed stalks and peltate heads. MPEF-Pb 6405a, from LH15. 58. Specimen with short peduncle and exposed cone axis. MPEF-Pb 6408b, from LH25. 59. Specimen with tightly adpressed basal bracts and exposed cone axis. MPEF-Pb 6401b, from LH13. 60. Specimen with compressed microsporophylls (dark, coaly areas) and underlying impressions exposed at right. MPEF-Pb 6406a, from LH25. 61. Elongate specimen with short peduncle and exposed cone axis. MPEF-Pb 6404, from LH15 (also Fig. 67).

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Figs. 62–72. Agathis zamunerae sp. nov., fine features of pollen cones and microsporophylls. Figs. 62–66, 68, 69, and 72 under epifluorescence. 62. Base of the holotype (Fig. 52; also Figs. 70–72), showing resin ducts in peduncle, basal bract cluster with rightmost bract pulled down, and basal microsporophylls in lateral view. 63–65. Details of cone shown in Fig. 55. Fig. 63, basal bract cluster. Figs. 64 and 65, microsporophyll heads in external view; note obscuration of the bases by neighboring heads and convexity, rounded apices, and lack of marginal denticulations. 66, 67. Cone axes in longitudinal view. Fig. 66, set of closely spaced, longitudinally elongate depressions where microsporophyll stalks detached. Counterpart of cone shown in Fig. 54. Fig. 67, basal remnants on the axis where stalks broke near the base and did not detach cleanly, and departing attached stalks to left, from cone shown in Fig. 61. 68, 69. Cone (naturally) broken obliquely, showing microsporophyll stalks and heads in oblique-dorsal view, MPEF-Pb 6313, from LH13. Note large resin ducts, thick stalks that expand distally, and (especially in Fig. 69) markedly convex, apically and basally recurved heads. 70–72. Details of microsporophylls and pollen sacs preserved in lateral view on right margin of the holotype (Figs. 52 and 62). Thin arrows indicate corresponding points in Figs. 52, 70, and 71. Thick arrow in Fig. 72 corresponds to same in Fig. 52, in same relative orientation (image here rotated counterclockwise to fit the layout). Fig. 70, set of sporophylls with light brown pollen sac clusters preserved abaxial to each stalk. Fig. 71, detail of expanding stalk termination with adaxial ridge, striated surface, and abrupt insertion into the peltate head. Fig. 72, detail, set of elongate pollen sacs, abaxial and subparallel to the dark stalk vertical at frame left. Note curving tip of the sac at lower right; the tip is lying free on the rock surface. Composite of 68 images in 9 panels.

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Holotype— MPEF-Pb 6399 (Figs. 52, 53, 70–72), a pollen cone part and counterpart from Laguna del Hunco, Tufolitas Laguna del Hunco, early Eocene, Chubut Province, Argentina, quarry LH6 of Wilf et al. (2003). Paratypes— Laguna del Hunco, Tufolitas Laguna del Hunco, early Eocene, Chubut Province, Argentina. Twig: MPEF-Pb 6301 (quarry LH13). Leafy twigs: MPEF-Pb 6302 (LH2); 6303–6306 (LH6); 6307 (LH10); 6308–6315 (LH13; 6313 also with unattached pollen cone); 6316–6318 (LH22); 6319, 6422 (LH25); 6320–6323, 6423 (LH27); 6324 (float). Leaves (isolated): MPEF-Pb 6325 (AL1); 6326, 6327 (LH2); 6328–6330 (LH4); 6331 (level of LH4); 3160, 6332–6342, 6344–6348 (LH6); 6349 (LH10); 6350–6367 (LH13); 6368 (LH23); 6369– 6373 (LH25); 6374–6388, 6420, 6421 (LH27); 6389, 6390 (float). Seed cone: MPEF-Pb 6391 (LH27). Cone scales: MPEFPb 6392, 6393 (LH6); 6394–6396 (LH13); 6397 (LH15). Cone scale with attached seed: MPEF-Pb 6398 (LH13). Pollen cones: MPEF-Pb 6313 (LH13, on block with leafy twigs per above); 6400 (LH6); 6401–6403 (LH13); 6404, 6405 (LH15); 6406– 6409 (LH25); 6410–6417 (LH27). Río Pichileufú, La Huitrera Formation, early middle Eocene, Río Negro Province, Argentina. 1. Original, historical collection, exact quarry sites unknown, figured material referred to “Zamia” tertiaria Engelhardt by Berry (1938). Leafy twigs: USNM 40378c, 40378d, 40378h (Berry 1938: pls. 8.2, 8.5, and 9, respectively). Leaves (isolated): USNM 40378e, 40378f, 40378g (Berry 1938: pls. 8.1, 8.4, and 8.3, respectively). 2. Additional cohort material from the historical collection, not previously reported, identified as “Zamia tertiaria” on Berry’s handwritten tags. Leafy twig(s): USNM 545227, 545230, 545235. Leaves (isolated): USNM 545223–545226, 545228, 545229, 545231– 545234, 545236–545238. 3. Older BAR collections. Leafy twig(s): BAR 288-20, 1214-20, 5002-20. Leaves (isolated): BAR 1211-20, 1214-20. 4. Recent collections for current project. Leafy twigs: BAR 4748 (near RP1), 4749 (RP3). Leaf (isolated): BAR 4750. Cone scales: BAR 4751–4753. Specific diagnosis—Leaves with consistently elliptic to lanceolate shape; long length (to ≥132 mm); and a generally high length:width ratio (observed 3.9–11.5:1). Seed body ca. 12 × 7 mm, and larger seed wing ca. 13 × 8 mm. Pollen cones with stout, short to long peduncle (to ≥7.3 mm); relatively few basal bract pairs (3 pairs observed), arranged in a tightly imbricate cluster with width less than that of the cone body (sporophyll-bearing region) and no elongated bracts; cylindrical to slightly convex cone body with long length (to ≥56 mm); and imbricate microsporophylls with head width ≤2 mm and entire distal head margins. Description—Resin, preserved as amber, abundant in all organs. Twigs (Figs. 1–15) opposite, strongly grooved longitudinally, with quadrangular epidermal cells sometimes present (on presumed green twigs in life) and obliquely exserted leaf-abscision scars subtended by woody supply tissues that are long-decurrent on the axis. Terminal bud conspicuously globose, with many tightly imbricate bud scales. Leaves (Figs. 1–7, 9–11, and 15–31) well separated along the twig, opposite to subopposite decussate, deployed distichously via basal twisting of the narrow petiole. Petioles elliptical in cross section (e.g., Fig. 24), width at base 1.2–4.2 mm (mean ± 1 SD = 2.3 ± 0.8 mm; N = 51), darkened in distinct abscision zone. Blades symmetrical, elliptical to lanceolate, the widest portion occurring at 35–63% of the total blade length (48 ± 6%, N = 52), the base and apex acute, the apex

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slightly rounded or blunted, never sharp-pointed, not acuminate or falcate. Blade length 24.3–132.4 mm (66.7 ± 17.1 mm, N = 59), width 5.7–18.5 mm (10.6 ± 2.7 mm, N = 94), length:width ratio 3.9–11.5:1 (6.6 ± 1.7, N = 53). Blade dimensions vary continuously among samples, such that no clear recognition of juvenile versus adult foliage is possible. Veins parallel, midvein absent, course nearly straight and little influenced by margin curvature, and numerous, via dichotomies from the petiolar veins (Fig. 22). Resin ducts alternate with the veins (Fig. 23; see Kausik, 1976). Stomata (Figs. 25–31) rarely preserved but numerous and densely packed wherever observed, usually in two rows per vein, randomly oriented (oblique, perpendicular, or parallel to the veins), preserved as casts of guard cells and/or as coalifed Florin ring compressions of maximum long-axis length ca. 65 μm. Amphistomy, variation in stomatal distribution or size along the leaf length, and variation in the length or continuity of stomatal strips (Kausik, 1976) could not be confidently discerned. Immature seed cone (one specimen, Figs. 32–36) ovate, length 34 mm, width 33 mm, terminal on a thickened branch (width 21 mm) that has a prominent growth-increment scar. Cone scales (ovuliferous bract-scales) helically arranged in the cone, their apices upturned in smooth arcs, without spiny distal projections. When preserved separately (Figs. 37–51), presumably as mature, dispersed units, cone scales as wide as or wider than long, length 18.6–26.1 mm (22.9 ± 2.2 mm, N = 9), width 21.4–35.7 mm (27.7 ± 4.9 mm, N = 9), distal margins thickened and upturned or recurved, the apex broad and slightly expanded, with either an attached seed (Figs. 37–39) or with a narrow, elliptical seed depression and an asymmetrically curved, distally concave seed-detachment scar (Figs. 40–43). An impression of the adjacent ovule in the cone may be present (Fig. 45). Longitudinal architecture (fibers, resin ducts, vasculature) within the seed depression area oriented more linearly than outside, converging slightly admedially into the detachment scar, then curving exmedially in the area distal to the scar (Figs. 42 and 43). Cone-scale base scalloped (auriculate) on both sides where preserved, usually hooked to a sharp point on at least one side, sometimes reduced to a kink on other side, the scallops incised 1.1–5.2 mm from the base and without frilly projections. Cone scale upper corners rounded, the distal margin smooth, straight to rounded, thickened to recurved, and with a slight, broad distal expansion in the center. Pollen tubes not preserved (see Kaur and Bhatnagar, 1986). Seed (one specimen, Figs. 37–39) at center of the cone scale base, single, inverted, and ovoid, length ca. 11.8 mm, width ca. 7 mm, its long axis aligned to that of the scale, its body protruding slightly below the scale basal margin, with two opposite wings: one large and well-rounded apically, directed at ca. 40° in relation to the left basal margin (in adaxial view as preserved and shown), length ca. 13.4 mm, and one small, rudimentary, length ca. 3 mm, with an acute, pointed apex. Pollen cones (Figs. 52–72) cylindrical to slightly convexsided, inserted on a stout peduncle, with subtending bract clusters, apex smoothly curved. Peduncles short to long, straight-sided to semiconical, rounded to quadrangular (Fig. 53) in cross section, expanding distally to the approximate width of the cone bracts, distally concave upward. Peduncle length 2.2–7.3 mm (4.3 ± 1.6 mm, N = 7), minimum width 1.0– 3.5 mm (2.8 ± 0.8 mm, N = 8), maximum width 4.1–6.8 mm (5.6 ± 0.8 mm, N = 13). Cone length, including bracts but not peduncle, 23–56 mm (40.0 ± 9.5 mm, N = 10), diameter 6.6–10.8 mm (7.7 ± 1.2 mm, N = 16). Bracts tightly imbricate, apparently consistently in three pairs, ovate, apices rounded, forming a cluster 4.7–8.4 mm wide (6.1 ± 1.0 mm, N = 13) that is 68–97%

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Figs. 73–81. Extant Agathis, selected features of dried material for comparison to fossils. All except Fig. 77 are litter samples of a cultivated A. robusta, Myocum, New South Wales, Australia. Figs. 76 and 80 under epifluorescence. 73. Twigs with terminal buds of varying sizes. Note marked longitudinal striations, prominently and obliquely raised abscision scars with decurrent supporting tissue, and scaly, rounded buds. Compare Figs. 1–15. 74. Detail of a large terminal bud, showing numerous overlapping scales and crowded, subtending abscision scars. Compare Fig. 8. 75, 76. Twig closeup showing longitudinal ridges and grooves and quadrangular epidermal cells. Compare Figs. 12 and 13. 77. Seed-cone base, Agathis macrophylla (Aneityum Island, Vanuatu, S.F. Kajewski 760, US Fruit Collection 325). Note thickened fertile branch and large growth-increment scar subtending the cone, and imbricate, upturned scale tips with rounded, convex-upward margins. Compare Figs. 32–36. 78. Distal left corner (in adaxial view) of seed-abscision area of a cone

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the width of the sporophyll-bearing region of the cone (80.3 ± 9.3%, N = 12) and is fully constrained below the first microsporophylls, with no elongate or leaflike basal bracts present. Bract length 2.4–4.7 mm (3.5 ± 0.5 mm, N = 8), width 2.3–3.5 mm (2.8 ± 0.5 mm, N = 7). Microsporophylls (Figs. 67–72) imbricate, peltate, numerous (ca. 250–500 cone–1), helically arranged. Stalks striated and with an adaxial median ridge, reflexed basally to accommodate mass of the head and pollen sacs, where detached leaving irregular pits (if cleanly detached, Fig. 66) or basal remnants (Fig. 67) on the cone axis. Stalk length 1.9–2.9 mm (2.4 ± 0.4 mm, largest values from 11 cones), stalk plus head total length 2.4–3.7 mm (3.0 ± 0.5, from 11 cones). Stalk and its median ridge expand distally (Figs. 69–71), before their peltate insertion into most of the microsporophyll head. Heads (Figs. 64, 65, and 68–71) abruptly angled from the stalks, then strongly recurved apically and deeply basally, outwardly markedly convex, the shape ovate, the margin and apex smoothly rounded and without angled tips, notches, serrations, or denticulations. In external view (e.g., Figs. 64 and 65), the basal margins of the heads are obscured by imbrication. Head height in external view 1.5–2.1 mm (1.7 ± 0.2 mm, from 12 cones), width 1.3–2.0 mm (1.6 ± 0.3 mm, from 13 cones). Pollen sacs (Figs. 70 and 72) apparently immature where observed, attached to the inner abaxial portion of the microsporophyll head, preserved as light brown patches, each containing several narrow, elongate sacs, the sac outlines subparallel to the microsporophyll stalks; number of sacs could not be determined with confidence; pollen not preserved. Remarks— We designate a pollen cone as the holotype for the new species because it is well recognized that pollen cones are the only organs of the genus Agathis that have relatively abundant and distinctive characters at species level, once the generic diagnosis is made from all available material (e.g., Whitmore, 1980b; Farjon, 2010). The holotype was collected 6 December 2002 (by P.W., K.R.J., and crew). We refer all the cited fossil-plant organs to a single species because there is no evidence that more than one taxon is definably present. There are also no differences yet apparent among samples from the two sites (L.H. and R.P.), despite intensive sampling of their bulk floras. Moreover, each organ type recovered is independently assignable to Agathis using most of the standard botanical characters for the genus (see Familial and generic affinities) and exhibits a self-consistent set of features and dimensions, and the various organs are all found very closely associated on single bedding surfaces. The certain attachments include the 36 specimens of twigs with attached leaves (e.g., Figs. 1–7) and one seed in place on a cone scale (Figs. 37–39). DISCUSSION The Zamia tertiaria problem—“Zamia” tertiaria Engelhardt (1891:646 and pl. 2 [Fig. 16]) is based on the single, holotype

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foliage specimen from the Eocene of Coronel, Chile, which is now apparently lost, along with most other material from Engelhardt’s important 1891 monograph (Wilf, 2012). Engelhardt’s drawing shows a parallel-veined leaf or leaflet with curved margins and no clear base or apex. Engelhardt further described this foliage as pinnate, leathery, and sessile, without illustration of these traits. Little can be said here to affirm or reject the identification to Zamia, especially with the holotype unavailable. Thus, Engelhardt’s “Z.” tertiaria from Chile cannot be linked in any meaningful way to the specimens described here from Argentina, nor to Agathis. Much later, Berry (1922:120 and pl. 1 [Fig. 4], pl. 2 [Figs. 1–3]) assigned several Eocene foliar specimens that he collected from Arauco Mine, Curanilahue, Chile, to “Z.” tertiaria Engelhardt. He also claimed that several specimens, including one figured specimen (his pl. 1 [Fig. 4]), showed attachment to a rachis “imbedded in the matrix.” Berry’s figured specimens survive (USNM 320640–43, not shown), and on examination they are somewhat different from his drawings and show typical monocot features, including at least two orders of parallel veins (i.e., A and B veins sensu Hickey and Peterson (1978), and distinct plications along the A veins, best seen in USNM 320643). There is no evidence of attachment to a rachis. Berry (1922) also assigned to “Z. tertiaria” a second specimen from Engelhardt’s monograph that Engelhardt (1891: pl. 1 [Fig. 4]) had identified as a monocot leaf fossil (“Monokotyler Blattrest”). On the basis of Engelhardt’s illustration, the only information available, this specimen was quite different from the “Z.” tertiaria holotype, and in fact very monocot-like, in having many more parallel veins, numerous cross veins, and a much more elongate, strap-shaped aspect. It is possible that Engelhardt’s “Monokotyler Blattrest” was indeed related to the material from Arauco that Berry assigned to “Z. tertiaria,” but not in the way Berry thought (all monocots, vs. all cycads per Berry). In any case, Berry’s (1922) “Zamia tertiaria” specimens show no affinity to Engelhardt’s (1891) “Zamia” tertiaria, as suggested long ago by Hollick (1932), nor to conifers. However, of historical note, Hollick (1932:177) explicitly noted a general similarity of Berry’s (1922) specimens (probable monocots) to Agathis. Subsequently, Berry (1938) referred specimens from Río Pichileufú to “Zamia” tertiaria Engelhardt (e.g., Figs. 1, 2, and 17; see also Familial and generic affinities), and these, including Berry’s previously unreported cohort material, are the only historical specimens of “Zamia” tertiaria that are reassigned here to Agathis zamunerae. Berry’s Río Pichileufú material is quite distinct from all the Chilean entities discussed above, excepting perhaps the lost, fragmentary holotype of “Z.” tertiaria. Even if this specimen were found and determined to have features of Agathis, it would still lack the large suite of characters, including those of leaf attachment and female and male reproductive organs, that is preserved in A. zamunerae. In summary,

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scale. Note strong relief, incurved architecture immediately basal to the scar, and outwardly curved architecture immediately distal to the scar. Compare Figs. 42 and 43. 79–81. Pollen cone with upward-facing microsporophylls removed manually, remaining microsporophylls in approximate lateral view as in several of the fossils. Fig. 79 shows large pits on the cone axis where the enlarged microsporophyll bases had inserted and from which they detached completely (cf. Fig. 66), as well as some remnants where the stalks broke off near the base (cf. Fig. 67). Epifluorescence in Fig. 80 clearly distinguishes tissues of the stalks (note striations and adaxial ridges as in the fossils), the abaxial pollen sacs, and the peltate, convex, apically and deeply basally recurved heads (cf. Figs. 69–72). Fig. 81, Single microsporophyll (compare Figs. 69–72). Note enlarged base, prominent, distally enlarged adaxial ridge, and the distinct tissues of the head and the pollen sacs, which have dehisced, in contrast to those in the fossils (Fig. 72).

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Figs. 82–88. Agathis lenticula in Kinabalu National Park and environs, Sabah, Malaysian Borneo, September 2012. 82. Large emergent tree, lower Mesilau Trail. 83. Young shoot, lower Mesilau Trail, showing typical Agathis features: green twig, opposite-decussate leaf attachment, distichous leaf deployment via basal twisting of petioles, parallel venation, and rounded terminal bud. Compare, e.g., Figs. 1–7. The lens-shaped juvenile leaves are typical for this living species (and not the fossils). 84. Litter sample from below large tree, bank of Mesilau River. Note raised, opposite-decussate abscision scars on twigs with decurrent supporting tissues (compare Figs. 11, 14, and 15), petioles with abscision scars on the leaves (compare Figs. 16–21 and 24), and pollen cone fragments. 85. Litter sample of pollen cones, from large tree below Kiau View trailhead. Note numerous similarities to the fossils: tightly adpressed basal bracts with width less than that of the full cone, variably short to long and quadrangular (second from left) peduncles, cylindrical to convex cone shape, and imbricate, convex microsporophyll heads (compare Figs. 52–72). Each small scale tick = 1 mm. 86, 87. Cone scales in litter below large tree, Mempening Trail, with (Fig. 86) and without (Fig. 87) the seed still in place. Note typical Agathis features: hooked basal scallops, rounded apical

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“Zamia” tertiaria Engelhardt is an unsuitable basionym for the Agathis fossils reported here, thus requiring the new species. Of additional historical interest, Petersen (1946:49), referring to Berry (1938), made the first record of “Zamia tertiaria” Engelhardt at Laguna del Hunco as part of his outstanding geological survey of the middle Chubut River region. Although Petersen’s collections are apparently lost, it is reasonable to infer that his identification (sensu Berry, 1938) was probably correct, and therefore that Petersen was the first scientist known to collect what is here designated as Agathis zamunerae, at its type locality. Familial and generic affinities— Each of the preserved organs of the new species displays a large number of distinctive features that, in combination and often singly, are only found in Agathis. These characters include most of those used by botanists to identify living Agathis and its species. Pending confirmation from a phylogenetic analysis, which would require much more data from the extant species, we conclude from the wealth of preserved morphological data that Agathis zamunerae sp. nov. is, in all probability, closely related to the living species of Agathis and belongs at least in the crown of the genus, and perhaps in a derived position therein. A selection of comparative details from extant live, litter, and dried material is shown in Figures 73–87. Beginning with vegetative features: conspicuously grooved, stout “green” twigs with globose, scaly terminal buds, bearing opposite to subopposite, decussate, distichously deployed, simple, symmetrical, well-separated, multiveined, straight-veined leaves with narrow petioles, a blunt apex, and randomly oriented stomata with Florin rings, are, collectively, firmly diagnostic of Agathis. Wollemia and some Araucaria species also have multiveined leaves, but these are sessile (and decurrent in Wollemia), overlap densely along the twig, lack conspicuous Florin rings, and have more longitudinally oriented stomata in most species (Florin, 1931; Cookson and Duigan, 1951; Stockey and Taylor, 1981; Stockey, 1982; Bigwood and Hill, 1985; Stockey and Atkinson, 1993; Chambers et al., 1998; Burrows and Bullock, 1999; Hill et al., 2008; Pole, 2008; Escapa and Catalano, 2013). Araucaria foliage is helically arranged, not decussate nor distichously deployed, and nearly always with a sharp apex; Wollemia leaves are distichous to four-ranked and trimorphic. Araucaria pichileufensis Berry (1938) foliage, which occurs abundantly at the same fossil localities at Laguna del Hunco and Río Pichileufú, is easily recognized as distinct from Agathis zamunerae in having the typically narrow, short, single-veined, imbricate, helically deployed leaves of Araucaria Section Eutacta. Outside Araucariaceae, the only living genus with vegetative features similar to Agathis (including A. zamunerae), especially in often having opposite–subopposite, elliptic, well-spaced, petiolate, multiveined leaves, is Nageia (Podocarpaceae). However, this genus has a completely different, podocarpaceous-type,

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acute terminal bud and veins that much more noticeably curve with the margin and recurve toward the apex; both these features are used to distinguish living Nageia from Agathis where they co-occur (Sterling, 1958; de Laubenfels, 1988; Beaman and Beaman, 1993). In addition, Nageia, like most podocarps and unlike A. zamunerae, has longitudinally oriented stomata (Florin, 1931; Hill and Pole, 1992). We note that broad, multiveined conifer leaves that are generally similar to our vegetative fossils are abundant throughout the Mesozoic and early Cenozoic and attributed to various conifer lineages (e.g., Heidiphyllum, Nageiopsis, Podozamites, Araucarioides (see Axsmith et al., 1998; Hill et al., 2008; Miller and Hickey, 2010), but the full combination of leaf and twig features preserved here is characteristic only of Agathis. Although the new material cited here from Río Pichileufú shows abundant Agathis twig and leaf features and includes associated cone scales (Figs. 50 and 51), it would be difficult to fully refute Berry’s (1938) assignment of his original suite of vegetative specimens from that site, considered alone, to Zamia without the strong corroboration from these new fossils. There are indeed many relevant similarities between some Zamia leaves and Agathis leafy branches, including grooved twigs/rachises, petioles/narrow leaflet bases, leaf(let) articulation and/or abscision, elongate and narrow leaves/leaflets, and parallel venation. However, even Berry’s specimens show features not found in Zamia, nor any cycads to our knowledge: the twigs are notably bumpy and include expanded support tissue under the obliquely raised abscision zones (e.g., Figs. 1, 2, and 10); leaf attachment is decussate (e.g., Fig. 2); and the leaves have copious resin and thick abscision zones that would be very unlikely in Zamia (Figs. 17 and 23). The Zamia problem aside, special care must be taken when identifying foliage with parallel venation at the two fossil sites, because of the presence of monocots and because of two other parallel-veined gymnosperm taxa, which, along with the conifers listed earlier (see Materials and Methods), complete the gymnosperm flora so far known. First, Ginkgo patagonica Berry (1935b) can quickly be distinguished from Agathis because it is palmately lobed and is usually preserved with thick, abundant cuticle unlike any Agathis studied here; however, the lobe tips can be confused with Agathis if found isolated and without cuticle. Second, we have recently found fossils of a true cycad at Laguna del Hunco (Wilf et al., 2003: fig. 1I). These have petiolulate, long leaflets with parallel venation that are much like Agathis, but the leaflets are toothed with decurrent bases and lack articulations or abscision zones. Preliminary indications are that this cycad closely resembles the African genus Encephalartos (P. Wilf, unpublished data). The female reproductive features described here are also stereotypical for Agathis. As in all Araucariaceae, the cone (Figs. 32–36), though not well preserved, arises on a thickened branch, is large and rounded (here subround due to presumed immaturity), and has flattened, densely and helically arranged cone scales with

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corners, and thickened, recurved, nonprojecting apex of the scale; large, ovoid seed body and corresponding depression in the scale; lateral impressions of adjacent seed bodies; presence of one enlarged, broadly curved wing extending at an angle distally and to right (in this view) and one rudimentary wing to left (individual cones may be “right-handed” or “left-handed;” this does not appear to have taxonomic significance), and corresponding impressions and discoloration of the scale; and small, curved seed-abscision zone. Compare Figs. 37–51. 88. A large area east of the park’s Mesilau entrance that was recently degazetted, deforested, and planted for a cabbage monoculture, requiring intensive pesticide use. The cleared landscape is dense with large stumps. Remaining intact, primary montane rainforest of the main body of the park, containing numerous, large Agathis lenticula and Dacrycarpus kinabaluensis in this area, is in the background. The current park boundary is several tens of meters behind the forest line visible on the green slopes. Inset, stump of a felled Agathis from this unprotected strip and its exuded copal.

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upturned tips. However, the large, prominently visible growthincrement scar subtending the fossil cone (see Fig. 77), the lack of well-developed subtending foliage (or any foliage in this case), and the lack of spinose or elongate cone-scale tips are collectively typical for Agathis and not for Araucaria or Wollemia (de Laubenfels, 1972; Jones et al., 1995). An important feature of Agathis cone scales that is easily seen in the isolated fossil scales is the marked basal scallops (e.g., Figs. 44, 47, 86, and 87), which function in life to provide accommodation space for the seeds of adjacent scales within the tightly packed seed cone. These are not present in Araucaria and, likewise, are not seen in the cone scales of the cooccurring A. pichileufensis. Wollemia cone scales have basal embayments, but these are broader than in Agathis, and the overall scale shape is markedly rhombic, unlike in Agathis and the fossils. Further, as just mentioned, the cone scales of Araucaria, including A. pichileufensis, and Wollemia typically have triangular to spinose, projecting tips (especially in Wollemia; Jones et al., 1995) that comprise the ovuliferous scale portion that is free of the bract, whereas in Agathis (excepting A. australis) and the fossils, there is consistently no apical projection, or only a very broad, blunt expansion (e.g., Fig. 40), and the bract and scale components appear to be fully fused. We also note that Dettmann et al. (2012: table 2) reviewed the best-preserved fossil seed-cone taxa of Araucariaceae, all of them Mesozoic, and none of these has scalloped (“auriculate”) cone scale bases as in Agathis, nor petiolate, opposite associated leaves. All Araucariaceae have a single, inverted seed per cone scale, as in the fossils. However, the seeds of Agathis and its sister Wollemia are adpressed but attached to the scale only by a weak stalk from which they are usually, though not always, shed, leaving on the scale a characteristic, rhomboidal (Wollemia) or asymmetrical curved (Agathis and fossils) abscision scar and a marked, longitudinally grooved seed depression, as seen in the fossils (e.g., Figs. 40–43, 45, 46, and 48; Owens et al., 1997; Chambers et al., 1998; Dettmann et al., 2012). In Araucaria, including A. pichileufensis from the same fossil localities, the seed is embedded in the tissues of the cone scale. The fossil seed in situ on its cone scale (Figs. 37–39), preserved extremely fortuitously and mostly as a very thin sediment cast, clearly shows typical Agathis positioning and morphology, including an ovoid body that projects slightly below the scale base, a concave-upward detachment area, and two, strongly asymmetrical wings, this asymmetry being a recognized synapomorphy for the genus (Escapa and Catalano, 2013). Wollemia has a single, relatively narrow wing that surrounds its seed and does not resemble the fossil. We note for general interest that DiMichele et al. (2001) reported an Early Permian gymnosperm seed with unequal wings that looks surprisingly similar to Agathis, although the wing architecture is quite different. The fossil pollen cones exhibit several features that are distinctive for Agathis. Most notably, the peduncle is well defined and can be elongate, and the basal bracts are broad, smoothly rounded, and contained below the lowest microsporophylls (e.g., Figs. 53–55, 62, 63, and 85). These features are typical for living Agathis when present, although some species can have sessile pollen cones (A. montana, and sometimes A. dammara, A. macrophylla, A. microstachya, and A. silbae) or can produce a single, extended, leaflike lower bract pair (A. australis and A. kinabaluensis). In Araucaria, the pollen cones are usually sessile or have a very short, never elongate peduncle, and the basal bracts, like the foliage leaves, are more numerous and much

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more narrow and sharp-pointed, extending well above the lowest microsporophylls (Cookson and Duigan, 1951; de Laubenfels, 1972, 1988; Barrett, 1998; Hill, 1998; Farjon, 2010). Araucaria pollen-cone size can also be much greater (≤25 cm in length) than in Agathis (≤9 cm), and the fossils (≤5.6 cm). Wollemia pollen cones are sessile and also range above Agathis in size (≤12.5 cm in length); the basal bracts are small, triangular to semirounded, and sharp-pointed and extend onto the basal microsporophylls (Hill, 1998; Eckenwalder, 2009; Farjon, 2010). Wollemia pollen cones are also shed without the bracts, which therefore would not be seen in isolated fossil cones as described here, and they easily disaggregate on drying (as also observed in Araucaria bidwillii), such that the microsporophylls break and leave the cone axis covered in their stubs (Chambers et al., 1998). This situation is unlike that reported for Agathis robusta (Chambers et al., 1998), whose microsporophylls remained intact when separated from the axis of the dried cone axis and left behind “footprint” depressions that appear to be similar to those in some of the fossils (Fig. 66). However, other fossils show broken remnants of the stalk bases rather than pits (Fig. 67). Likewise, when we tried this experiment, also on dried pollen cones of A. robusta (Fig. 79), mostly pits but some base remnants resulted, corresponding to intact (Fig. 81) and “footless” detached microsporophylls, respectively. Peltate microsporophylls, as seen in the fossils (Figs. 57 and 68–72), are typical for Araucariaceae (Gilmore and Hill, 1997). Agathis microsporophylls (in species where these are imbricate; Fig. 81), like those of the fossils, have rounded apices and a thick, long stalk. Unlike the fossils, Araucaria microsporophylls tend to have more pointed, acute apices and a relatively thin, weak, stalk, and Wollemia microsporophylls have very short stalks and thickened, shield-shaped heads with large, angular surface projections (Cookson and Duigan, 1951; Jones et al., 1995; Hill, 1998; Eckenwalder, 2009; Farjon, 2010). Epifluorescent imaging of an A. robusta pollen cone, with microsporophylls in lateral view (Fig. 80), very clearly distinguishes the tissues of the stalk and its expanding median ridge, the apically and deeply basally recurved head, and the abaxial pollen sacs under the basal portion of the recurved head. The same distinctions can be seen in the fossils (Figs. 69–72). Consistent with the observations above, a separate araucariaceous pollen cone morphotype from Laguna del Hunco (exemplar specimen LH13–1135 mentioned by Wilf et al., 2005), under separate study, is larger than the fossils described here and has a very short peduncle, numerous narrow, long, sharppointed, mucronate basal bracts that extend onto the basal microsporophylls, and large, triangular microsporophyll heads with acute to acuminate apices. This morphotype is the probable pollen cone of the Araucaria pichileufensis plant. Comparisons to extant species— Agathis zamunerae is the first fossil Agathis to be so completely preserved as to allow detailed comparisons to living species, using most of the typical botanical characters (Table 1). The following combined character states of Agathis zamunerae, and those of the pollen cones alone, are unlike any other Agathis species (also see Specific diagnosis): leaves with consistently elliptic to lanceolate shape, long length, and generally high length:width ratio; unique combination of seed and wing dimensions; and pollen cones with cylindrical or slightly convex shape, long length, and stout, long, peduncle, relatively few (3) basal bract pairs forming a tightly imbricate cluster with width less than that of the cone body and no elongate basal bracts, and imbricate microsporophylls

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with head width ≤2 mm and entire head margins. Without a phylogenetic context for the genus, it is problematic to evaluate the importance and polarity of the various characters. However, overall, and especially when considering pollen cone characters, Agathis lenticula (Figs. 82–88) emerges as the living species with the greatest morphological similarity to the fossils, though with several differences (Table 1). This species has not been considered in the limited phylogenetic analyses done so far for Agathis, and correcting this omission would have obvious importance for evaluating the phylogenetic position of A. zamunerae, as well as for the conservation of A. lenticula. In A. lenticula, the pollen cones (Fig. 85) are somewhat shorter than the longest fossil cones but otherwise broadly consistent in cylindrical shape (of mature cones), length and stoutness of the peduncle, number and imbrication of bracts, and microsporophyll height, width, and imbrication. However, A. lenticula microsporophylls are noticeably denticulate at the apex, versus entire in the fossils. This difference could be preservational, but the denticulations we have observed in the living species are large enough to be easily seen with a 10× hand lens, and similar structures should be visible in our best-preserved fossils (e.g., Figs. 65 and 71). The seed-cone scales of A. lenticula are consistent with the fossils in size and general shape. The namesake lens-shaped juvenile leaves of A. lenticula (Figs. 83 and 84) were not seen in the fossils. Agathis moorei shows some morphological overlap with the fossils, but its pollen cones have important dissimilarities, and in general its corresponding organs range much larger in size. Pollen cones of A. moorei are consistent with the fossils in cylindrical shape, peduncle length (although this can be significantly longer than in the fossils), imbrication of bracts and microsporophylls, and height and width of microsporophyll heads, although the width can be much greater. However, compared with the fossils, A. moorei pollen cones arise from more slender peduncles, do not become so long, have 4–8 pairs of bracts (vs. three pairs in the fossils), and have relatively flattened microsporophyll heads with denticulate distal margins, compared to convex heads with entire margins in the fossils. The seed-cone scales are also similar to the fossils, but again they tend to be larger, especially in length. Leaf shape is more variable than in the fossils, and leaf size can be similar or much larger. Agathis macrophylla pollen cones are comparable with the fossils in cylindrical shape, peduncle stoutness and length, the imbrication of basal bracts, and the imbrication, height, and width of microsporophylls. However, in A. macrophylla, the attachment of the microsporophyll stalk is not peltate but to the abaxial edge of the head, and the microsporophyll apex is denticulate and can be notched. According to Farjon (2010; Table 1), there are four bract pairs, and the cone does not become so long as in the fossils, whereas Eckenwalder (2009) reported 3–4 bract pairs and cone length that rarely reaches that of the fossils. Seed-cone scales of A. macrophylla are generally larger than in the fossils. Leaf shape is not usually elliptic in A. macrophylla and, consistent with the name, leaf length and width can be significantly larger than in A. zamunerae. Agathis robusta has pollen cones with several dissimilarities from those of A. zamunerae, despite the similar long-cylindrical aspect in both species, most notably: in A. robusta the peduncle can be much longer, there are usually more bract pairs and these are often distinctly less imbricate, and the microsporophylls are often tessellate or only weakly imbricate. Also, cone scales of A. robusta are usually larger than in the fossils. These living and fossil species are most similar to each other in leaf size and shape.

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Agathis australis of New Zealand, of general interest because it emerges as the sister of all the remaining species in most molecular phylogenies, and because its history in New Zealand is frequently debated (see General remarks), has many important morphological differences from A. zamunerae. Many of these are smaller dimensions of the organs (Table 1), but additional differences from the fossils are that A. australis has: pollencone peduncles that can be much longer; pollen-cone bract clusters loosely arranged and extending past the width of the cone, often with subtending, leaflike, long bracts; microsporophyll heads wider; seed-cone scales with very distinct narrow, triangular, mucronate apical projections; (adult) leaves often with a truncate apex and longitudinally oriented stomata; and seed-wings with a square shape. These numerous differences from A. australis support the idea that A. zamunerae occupies a derived position within the genus. Agathis dammara resembles and is often considered conspecific with A. lenticula (Whitmore, 1980b; Eckenwalder, 2009). In A. dammara, the basal bracts of pollen cones can be more numerous (2–4 pairs) than in A. lenticula (2–3) and the fossils (3) and are spreading rather than imbricate. Other differences from the fossils are mostly dimensional (e.g., A. dammara has shorter pollen cones and peduncles, and larger seed-cone scales). The microsporophylls of A. dammara, A. lenticula, and A. zamunerae are very similar, except that microsporophyll height in A. dammara is distinctly lower than in the other two species, and in both the living species the apical margins are denticulate, versus entire in the fossils. Finally, A. borneensis is another species with some general similarities to the fossils, mostly in the leaves, but its pollen cones are very different. They are not strongly cylindrical and can be globose when immature, but most notably, the pollen cones and microsporophylls become dramatically larger than those of the fossils or of any other living Agathis species. Remarks on Agathis lenticula— Agathis lenticula (Figs. 82–88) may possess special evolutionary and biogeographic importance for the genus, given its similarity to the fossil species A. zamunerae. Agathis lenticula is a large tree (≤45 m) that is endemic to the lower montane forests of northern Borneo (Malaysia; de Laubenfels, 1979; Yii, 1995). The Kinabalu Park Headquarters Meteorological Station (1680 m), around which A. lenticula is abundant, has a mean monthly temperature of ca. 20°C, with an annual range of 14.4–22.2°C, and annual precipitation of 2000–3800 mm, including drought years (Kitayama, 1992). Where it is still protected, we found the species to be common and often dominant, for example along the lower reaches of the Mesilau trail, in the eastern portion of Kinabalu National Park (P. Wilf and R. M. Kooyman, personal observation). This species is considered Vulnerable and suffers ongoing losses within its limited range (Fig. 88) that are not well documented because loggers do not discriminate it from A. borneensis (Beaman and Beaman, 1993; Farjon et al., 1993; Farjon, 2010; IUCN, 2013). We note that Whitmore (1980b) and Eckenwalder (2009) did not recognize A. lenticula as distinct from the more widespread A. dammara, which if incorrect would be very likely to have negative conservation effects on A. lenticula. In our experience, the characters of A. lenticula are reliably distinct from A. dammara as originally proposed (de Laubenfels, 1979; Farjon, 2010), and we recommend that the species be managed in that context.

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It is remarkable that Mt. Kinabalu alone has three species of Agathis (A. borneensis, A. lenticula, and A. kinabaluensis) and that these form part of a diverse and entirely Gondwanan conifer assemblage that also has six genera and 16 species of Podocarpaceae, along with their close relative Phyllocladus hypophyllus (Beaman and Beaman, 1993, 1998). Including A. orbicula, Borneo as a whole has four species of Agathis, equal to New Caledonia (Table 1). Also striking is that one of the tall podocarps that frequently cooccurs with Agathis lenticula, Dacrycarpus imbricatus, is extremely similar to D. puertae from Laguna del Hunco and Río Pichileufú (Wilf, 2012) at ca. 16 000 km modern distance, further illustrating the vast temporal and geographic reach of a Gondwanan association surviving in an Asian rainforest. General comments— The evidence from Agathis zamunerae, including the strong possibility that it represents a derived lineage, suggests that modern-aspect Agathis not only occupied a vast land area by the early Eocene but was already well diversified. As for Eucalyptus and many other taxa (see Materials and Methods), Eocene Agathis fossils from Patagonia show that Australia can no longer be assumed to be the area of origin for the genus. Agathis evolved in and became a dominant element of the extensive southern rainforest biome of the Eocene, and in all likelihood it once inhabited Antarctica, which had very warm temperatures at this time (Pross et al., 2012), along with Australia and South America. Agathis was probably restricted primarily to rainforest environments throughout its history, partly because it possesses accessory xylem tissues parallel to the leaf veins (Kausik, 1976) that are likely to collapse during drought (Brodribb and Holbrook, 2005; these run adjacent to the veins and could not be distinguished in the compression fossils). There is a vigorous debate concerning the origins of Agathis in New Zealand and, along with many other components of the New Zealand biota, regarding its possible survival there through a proposed interval of partial or complete submergence during the Oligocene (Cooper and Millener, 1993; Stöckler et al., 2002; Waters and Craw, 2006; Knapp et al., 2007; Lee et al., 2007; Biffin et al., 2010; Crisp and Cook, 2011; Sharma and Wheeler, 2013). Our results show, first, that modern-aspect Agathis was present long before the Oligocene, over a vast area of Gondwana before its final breakup. Thus, putative survival in situ was possible in that the genus had certainly evolved by that time, but whether Agathis was really in New Zealand during the Oligocene is not fully understood despite many possible fossils (Pole, 2008). Second, the large past distribution of Agathis revealed here shows that many areas of Gondwana, not just Australia (as thought based on the previous fossil record), could have been the source for New Zealand in a dispersal scenario. This situation is similar to that of New Zealand’s endemic tuatara lizard (Sphenodon), for which there is a global record of related fossil forms during the Jurassic, and now an especially tuatara-like fossil is known from the Campanian–Maastrichtian of Patagonia (Apesteguía and Jones, 2012). Third, A. zamunerae is the only fossil Agathis that can be well compared to living species because of its preservation of a large suite of characters from multiple organs, and in all probability it is not closely related to A. australis (see Comparisons to extant species). Therefore, there is still no reliable fossil evidence, from New Zealand or elsewhere, concerning the origins of the A. australis lineage.

Agathis zamunerae is the oldest example of a modern-aspect Agathis, but at the same time it is significantly younger than the oldest Araucaria (Middle Jurassic), in line with the abundant molecular data that show Araucaria to be sister to Agathis plus Wollemia, and the relatively late (Turonian) appearance of Wollemia-type pollen (Dilwynites; Macphail et al., 1995; Macphail and Carpenter, 2013). Early Paleocene vegetative and fertile macrofossils from the San Jorge Basin in Chubut of a probable stem taxon of Agathis, currently under study, corroborate the idea of a Paleogene crown for Agathis and show an even older ex-Australasian distribution for the Agathis lineage (I. H. Escapa et al., unpublished data). Conclusions— Agathis zamunerae sp. nov. shows a large suite of character states that are all found in living Agathis and demonstrates that the lineage was present by the early Eocene, in turn helping to validate the Australian early Cenozoic record of the genus. The presence of Agathis in both Australia and Patagonia just prior to and during the middle Eocene terminal breakup of Gondwana clearly indicates that its range during the globally warm Eocene was vast and must have included Antarctica, as is true of other fossil taxa that were previously shown to have had similar past distributions and that are also frequently associated with Agathis today. The new species was a dominant component of the ancient Patagonian rainforest biome, as indicated by its relatively high leaf abundance. Assuming that A. zamunerae of Patagonia was similar to living Agathis in having large stature, long life span, and keystone ecological roles, its extinction was an important contributor to the ecosystem transformation process in Patagonia from the ancient, high-diversity rainforests, eventually leading to its modern-day, carbon-poor steppe and species-poor temperate rainforest biomes. This natural process took many millions of years, but in its present range, many thousands of kilometers distant from Patagonia, the rapid loss of Agathis forest is having comparable impacts, several orders of magnitude more rapidly. As in the past, the present loss of Agathis is correlated with massive ecosystem disturbances and may well portend a threshold event, whereas success in conserving the genus seems likely to be correlated with many aspects of improved ecosystem health and biodiversity. LITERATURE CITED APESTEGUÍA, S., AND M. E. H. JONES. 2012. A Late Cretaceous “tuatara” (Lepidosauria: Sphenodontinae) from South America. Cretaceous Research 34: 154–160. 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 4: 475–507. AXSMITH, B. J., T. N. TAYLOR, AND E. L. TAYLOR. 1998. Anatomically preserved leaves of the conifer Notophytum krauselii (Podocarpaceae) from the Triassic of Antarctica. American Journal of Botany 85: 704–713. BALETE, D. S., L. R. HEANEY, M. JOSEFA VELUZ, AND E. A. RICKART. 2009. Diversity patterns of small mammals in the Zambales Mts., Luzon, Philippines. Mammalian Biology 74: 456–466. BARRETT, W. H. 1998. Gymnospermae. In M. N. Correa [ed.], Flora Patagonica, parte I, 370–384. Instituto Nacional de Tecnología Agropecuaria, Buenos Aires, Argentina.

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First fossil record of Discocephalinae (Insecta, Pentatomidae): a new genus from the middle Eocene of Río Pichileufú, Patagonia, Argentina.

Ceratopetalum (Cunoniaceae) fruits of Australasian affinity from the early Eocene Laguna del Hunco flora, Patagonia, Argentina.

A new Frenguelliidae (Insecta: Odonata) from the early Eocene of Laguna del Hunco, Patagonia, Argentina.

Kelp and dolphin gulls cause perineal wounds in South American fur seal pups (Arctocephalus australis) at Guafo Island, Chilean Patagonia.

Eocene Podocarpium (Leguminosae) from South China and its biogeographic implications.

Stars of South American science.

The first South American sandownid turtle from the Lower Cretaceous of Colombia.

Analysis of admixture and genetic structure of two Native American groups of Southern Argentinean Patagonia.

Student life--South American challenge.

Eocene primates of South America and the African origins of New World monkeys.

Mycorrhizal compatibility and symbiotic reproduction of Gavilea australis, an endangered terrestrial orchid from south Patagonia.

Oral manifestations of paracoccidioidomycosis (South American blastomycosis).

Radiologic appearance of pulmonary South American blastomycosis.

Corrigendum: Eocene Podocarpium (Leguminosae) from South China and its biogeographic implications.

First skulls of the early Eocene primate Shoshonius cooperi and the anthropoid-tarsier dichotomy.

First record of eocene bony fishes and crocodyliforms from Canada's Western Arctic.

South American legal perspective on professional nursing.

Esterase D in South American Indians.

First DNA Barcode Reference Library for the Identification of South American Freshwater Fish from the Lower Paraná River.

First complete mitochondrial genome of the South American annual fish Austrolebias charrua (Cyprinodontiformes: Rivulidae): peculiar features among cyprinodontiforms mitogenomes.

Contaminants in the southern tip of South America: Analysis of organochlorine compounds in feathers of avian scavengers from Argentinean Patagonia.

South American blastomycosis of the maxilla: report of a case.

American orthopedic surgery: the first 200 years.

Contributions of South American research centers to Carbohydrate Research.