Palaeontologia Electronica Pleistocene Flora of Rio Puerto

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Pleistocene flora of Rio Puerto Viejo, Costa Rica

Terry A. Lott, David L. Dilcher, Sally P. Horn, Orlando Vargas, and Robert L. Sanford, Jr.

ABSTRACT

The Puerto Viejo Pleistocene megafossil flora presented here is based on fossil leaves, fruits, and seeds from the banks of Río Puerto Viejo, Costa Rica. Eleven types of plant megafossils are described in this study, including Laurophyllum, Oxandra, Pip- erites, Ingeae, Parinari, Sacoglottis, Byrsonima, and Pouteria. Detailed morphological and anatomical data are provided for each taxon. Although the Puerto Viejo site is situ- ated in the Atlantic Lowland Tropical Wet Forest today, the fossil flora suggests a relationship with nearby modern forests at slightly higher elevation, and cooler paleotemperatures than at present.

Terry A. Lott. Paleobotany and Palynology Laboratory, Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611-7800, USA. [email protected] David L. Dilcher. Department of Biology, Indiana University, Bloomington, Indiana 47401, USA. [email protected] Sally P. Horn. Department of Geography, University of Tennessee, Knoxville, Tennessee 37996, USA. [email protected] Orlando Vargas. La Selva Biological Station, Organization for Tropical Studies, Puerto Viejo de Sarapiquí, Costa Rica. [email protected] Robert L. Sanford, Jr. Department of Biological Sciences, University of Denver, Denver, Colorado 80208, USA. [email protected]

KEY WORDS: Pleistocene; Costa Rica; fossil plants; cuticle; anatomy

INTRODUCTION ous studies of the extant flora (Hartshorn and Ham- mel 1994; Wilbur 1994), along with some The lowland neotropical flora of La Selva Bio- paleoecological research focused on pollen and logical Station in Costa Rica (10°26’N, 84°00’W) is charcoal evidence of Late Quaternary vegetation predominately that of an undisturbed tropical wet and fire history (Horn and Sanford 1992; Kennedy forest. The station also includes some secondary and Horn 1997, 2008; Horn and Kennedy 2001; forest, along with areas of swamp, riparian, dis- Titiz and Sanford 2007). The plant fossil record for turbed, and managed vegetation (McDade et al. this area is relatively scarce, and records from 1994). Research at La Selva has included numer- Quaternary deposits of Costa Rica overall are pre-

PE Article Number: 14.1.5A Copyright: Palaeontological Association March 2011 Submission: 19 May 2010. Acceptance: 8 December 2010

Lott, Terry A., Dilcher, David L., Horn, Sally P., Vargas, Orlando, and Sanford, Robert L., Jr., 2011. Pleistocene flora of Rio Puerto Viejo, Costa Rica. Palaeontologia Electronica Vol. 14, Issue1; 5A:15p; http://palaeo-electronica.org/2011_1/242/index.html LOTT ET AL.: PLEISTOCENE FLORA COSTA RICA

dominately from plant microfossils. A few plant cut from the middle of the leaves, and these sec- macrofossils have been found in the Miocene tions were soaked in Jefferey’s solution (50% Nitric (Uscari sequence; Berry 1921a) and Tertiary of acid/ 50% of 10% Chromic acid) to remove the Costa Rica (Puntarenas Province; Gómez 1971, mesophyll. An insect pin mounted in a wooden 1972), but some determinations have been shown probe was used to tease apart the upper and lower to be incorrect (Graham 1987b, 1988). cuticle, and then a small paint brush with 2-3 bris- In this paper we present systematic descrip- tles was used to gently clean away the mesophyll. tions of plant megafossils from a Pleistocene The cuticle then went through an alcohol dehydra- deposit along the banks of Río Puerto Viejo, on the tion series of 50%, 95%, and 100% ethanol, northeastern edge of La Selva Biological Station in stained with 1% Safranin–O in 100% ethanol, then the canton of Sarapiquí, Heredia Province, Costa through a series of 100% ethanol, 10%Etoh/ Rica. The plant fossil assemblage is based on 90%HemoDe (or Citrisolv), and then 100% leaves, cuticle, fruits, seeds, wood, pollen, and HemoDe (or Citrisolv [Fisher Scientific, Pittsburgh, spores, and provides information on the composi- Pennsylvania]). The cuticle was then mounted in a tion of a lowland Atlantic flora during the Pleisto- drop of HSR (synthetic resin) in HemoDe (or Cit- cene of Costa Rica. Preliminary leaf identification, risolv) on a microscope slide, placed on a slide along with wood, pollen, and spore identifications warmer with a lead weight over the cover slip, and were presented in Horn et al. (2003) but without later sealed with fingernail polish. Over 100 cuticle systematic descriptions. and mesofossil slides were prepared, and the cuticle of over 100 modern leaf species were also pre- MATERIAL AND METHODS pared and examined. All cuticle parameters were determined using the Zeiss KS400, Version 3.0, The fossils presented here were collected 1999 imaging system. Five different and random- from exposed vertical banks of the Puerto Viejo ized areas within the alveoles were measured for river, on the northeastern edge of the La Selva Bio- 2 logical Station. The specific locality is called Site epidermal cell density (ED [n/mm ]) and stomatal 2 PV1 and was under clay-rich volcanic tephra up to density (SD [n/mm ]). The stomatal density was 1.4 m thick overlain by 11.8 m of alluvium, collu- then calculated using the Stomatal Index formula of vium, and modern soil. Radiocarbon analyses of SI = [stomatal density/(stomatal density + epider- wood from the deposit, and 40Ar/39Ar analysis of mal cell density)] × 100 (Salisbury 1927). plagioclase in the tephra, indicate that the flora is The fossil material is numbered with the Uni- Pleistocene in age (older than 46 ka but younger versity of Florida acronym (UF) followed by the than 915 ka; Horn et al. 2003). Sally Horn and Rob- locality number and then the specimen number ert Sanford collected fossils and bulk clay samples (e.g., UF18882–32685). Modern leaves used for in August 1992 from which the fossils were iso- comparisons are numbered in the University of lated. The sedimentology and dating of this site is Florida Modern Leaf Reference Collection accord- presented in Horn et al. (2003), along with initial ing to a consecutive numbering system (e.g., macrofossil and microfossil determinations. The UF5437). Modern leaf specimens were examined present physiognomy of the site is a tropical wet from the herbaria of the University of Florida forest in the Atlantic lowlands, about 35 m above (FLAS), Smithsonian Institution (SI), Missouri sea level. Botanical Garden (MO), and the Modern Refer- The bulk clay samples were washed at the ence Collection of the Paleobotany and Palynology Paleobotany and Palynology Laboratory, Florida Laboratory (prepared cuticle slides of nearly 5,000 Museum of Natural History, University of Florida species). All sorted and unsorted fossil samples using commercial detergent to separate the leaves are stored in the Florida Museum of Natural History and remove debris. The isolated organic material Paleobotany/Palynology Collection. Systematic was soaked in hydrofluoric acid (HF) to remove sil- description and terminology follows Dilcher (1974) icates, and then thoroughly washed with filtered and Ellis et al. (2009), and classification follows water. Specimens include fragmentary leaves, cuti- APG III (2009) and Judd et al. (2002). Terminology cle, wood, fruits, and seeds. They were photo- for stomates is as follows: the term stomata graphed with a Nikon 35 mm (Melville, New York, includes stomatal aperture plus guard cells, while USA) and a Zeiss 35 mm camera (Thornwood, stomatal complex includes stomatal aperture plus New York, USA). Specimens were also imaged guard cells plus subsidiary cells (Dilcher 1974; Ellis using a Nikon Coolpix990 and Zeiss AxioCam et al. 2009). camera. Square sections (1.0 cm x 1.0 cm) were

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SYSTEMATICS Menispermaceae have stomatal ledges and stomatal shape is not tetracytic (Krukoff and Moldenke Order PIPERALES Berchtold and Presl, 1820 1938, 1941, 1942, 1943; Krukoff and Barneby Family PIPERACEAE Giseke, 1792 1970; Barneby and Krukoff 1971; Wilkinson 1989; Genus PIPERITES Goeppert, 1854 Hong et al. 2001). Characters such as venation Piperites sp. (Figure 1.1–1.3), basal cells (Figure 1.6), epider- Figure 1.1–3, 1.5–7 mal and stomatal shape (Figure 1.5, 1.7) suggest a relationship to Piperaceae, near Piper rosei C.DC. Material: Puerto Viejo – UF18882–33585a,b, and P. novogalicianum A.J. Bornstein (Figure 1.4) 33586, 53699 (Burger 1971; Bornstein 1989). Description: Leaves petiolate. Lamina incomplete, The family Piperaceae are tropical trees, ovate, unlobed, > 4.8 cm long by 2.5 cm wide. shrubs, lianas, herbs, and sometimes epiphytic, Apex missing, base and margin fragmented. Peti- with five genera and ca. 3000 species, with Piper ole marginal, 1 cm long with scattered trichomes having around 1000 species. Due to the lack of an (Figure 1.3). Venation basal actinodromous, con- apex, fragmented base, and poorly defined sto- sisting of 5–7 primary veins, and two secondary mata, assignment of the fossil to any one species veins. Interior secondaries chevron, diverging from of Piperaceae is not advisable and is referred to primaries at 60–80º (Figure 1.1–1.2). Simple the fossil genus Piperites. Piperaceae pollen has agrophic veins, minor secondaries simple brochi- been found in the Pleistocene and Holocene of dodromous. Tertiary and quaternary veins irregular Costa Rica (Kesel 1974; Horn 1985, 1992; Hooghi- reticulate (Figure 1.2). Adaxial surface glabrous; emstra et al. 1992; Northrop and Horn 1996; Arford epidermal cells mostly pentagonal with some tet- 2001; Clement and Horn 2001; Anchukaitis and ragonal (average size ca. 23 x 32.9 µm), surface is Horn 2005; Kennedy and Horn 2008). Leaves of smooth, and cell walls mostly arcuate, some sinuo- Piperites have been reported from the Miocene of late to sinuous, or rarely sinuate (Figure 1.5). Costa Rica (Berry 1921a), and the Tertiary of Vene- Abaxial surface with numerous basal cells (aver- zuela (Berry 1936) and Indonesia (van Konijnen- age size ca. 15.8 x 22.3 µm), and occasional min- burg-van Cittert et al. 2004). ute glandular cells; epidermal cells smooth Order LAURALES Jussieu ex Berchtold and Presl, (average size ca. 24.9 x 33.6 µm) (Figure 1.6–1.7). 1820 Stomata sunken, barley visible, and tetracytic Family LAURACEAE Jussieu, 1789 (average size ca. 31.4 x 31.6 µm) (Figure 1.7). Genus LAUROPHYLLUM Goeppert emend Hill, Comments: Characters such as palmate venation 1986 and interconnecting secondary veins suggest the Laurophyllum sp. families Piperaceae, Malvaceae, Cecropiaceae, Figure 1.8–1.12 Urticaceae, and Menispermaceae. Within Urticaceae, genera such as Cecropia (Judd and Material: Puerto Viejo – UF18882–32687, 32688, Olmstead 2004; Systma et al. 2002), and Cecropi- 32689, 32690, 32692, 32693. aceae, genera such as Pourouma, venation is sim- Description: Leaves petiolate. Lamina incomplete, ilar, but the petiolar attachment is peltate in elliptic, unlobed, 6.0 cm long and 2–4.7 cm wide at Cecropia (Burger 1977; Hammel 1986), and the the middle. Apex angle acute (Figure 1.10), with deeply lobed lamina of Pourouma (Burger 1977; straight flanks, base angle acute, with cuneate Berg et al. 1990) do not match the fossil specimen. flanks (Figure 1.8). Margin entire. The petiole mar- Within the Malvaceae, genera such as Sterculia ginal, 4.0 mm long by 2.0 mm wide. Primary vena- and Theobroma are basal plinerved, with glandular tion pinnate, secondary venation cells and epidermal cell features that are similar to eucamptodromous (Figure 1.9), secondary vein the fossils, but the predominance of stellate angle of divergence near the base 30–40 (Figure trichomes are lacking in the fossil specimens 1.8), middle 35–60, and apex 30–90. Basal veins (Robyns 1964; Hussin and Sani 1998). The numer- are subopposite, remaining veins alternate; basal ous basal cells and some glandular cells, and sto- secondaries arch laterally and upward extending matal shapes appear most similar to those found in out to the margin, middle and upper secondaries the Piperaceae (Pant and Banerji 1965; Bornstein arching slightly or straight from the midvein out- 1989) and Malvaceae, but Malvaceae contain sto- ward to near margin, then an abrupt upward curve matal ledges. In Menispermaceae, the presence of to the superadjacent vein. Intersecondary veins 1– basal and glandular cells is similar to the fossil but 3 per intercosta, traversing more than ½ distance

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FIGURE 1. 1–3, 5–7, Piperites. 1, 5–7, UF18882-33585a. 1. Partial leaf with basal actinodromous venation. 2. Line drawing of partial leaf showing chevron interior secondaries, and irregular reticulate tertiary veins, UF18882-53699. 3. Petiole and basal venation, UF18882-33585b. 4. Extant leaf of Piper rosei, UF6048. 5. Adaxial surface with mostly arched epidermal cell walls. 6. Abaxial trichome base with numerous basal cells. 7. Abaxial sunken stomata. 8–12, Laurophyllum. 9, 11, 12, UF18882-32689. 8. Partial leaf with basal straight margins, UF18882-32687. 9. Line drawing of partial leaf with eucamptodromous secondary venation. 10. Partial leaf with acute apex, UF18882-32688. 11. Adaxial surface with epidermal cell walls with thin sections or knobby projections (arrows). 12. Abaxial epidermal cells also with thin sections or knobby projections (arrows). Stomates with inner ridge on the guard cell. Ridge presented as a thick black line in the stomate. Scale bar for 1–3, 8, and 10 equals 5 mm; 4 equals 1 cm; 5, 11, and 12 equals 20 µm; 6 equals 15 µm; 7 equals 30 µm; 9 equals 10 mm.

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to the margin before forking into two branches, one specimens in the organ genus Laurophyllum based joining the superadjacent secondary, and one join- on characters of entire-margined leaves, cuticular ing the subadjacent secondary (Figure 1.9). Ter- scales mentioned above, and slit like stomatal tiary venation reticulate and tertiary vein angle openings on the outer abaxial surface. Cuticular obtuse. Marginal vein present. Adaxial surface gla- characters of our specimens are similar to the dis- brous; epidermal cells tetragonal to pentagonal persed fossil cuticle organ species Piliparicutis with some hexagonal (average size ca. 8.7 x 15.5 hradekensis except the stomatal size is twice the µm), surface smooth, cell walls straight, slightly size in P. hradekensis (Schneider 2005). Venation curved to slightly sinuate with thin sections or and cuticular specimen UF18882-32689 is unique knobby projections along anticlinal walls (Figure with trichome bases limited to the abaxial surface 1.11, arrow). Abaxial surface glabrous but with a and the stomatal index is higher. Thus, there is the few trichome bases; epidermal cells pentagonal to possibility of more than one species of Laurophyl- tetragonal (average size ca. 7.5 x 15.1 µm), sur- lum. face smooth, cell walls straight, slightly curved or Lauraceae are a subtropical to tropical family slightly sinuate with thin sections or knobby projec- of woody plants, with over 50 genera and 2500– tions along the anticlinal walls (Figure 1.12, arrow). 3000 species (Rohwer 1993). Ocotea, with over Stomatal complex is random, brachyparacytic, and 300 species, are found in subtropical to tropical hemiparacytic (stomata average size ca. 9.1 x 13.6 Central America to South America, Madagascar, µm) with an inner rim scale on the guard cell, trap- Africa, and the Canary Islands. Nectandra, with ezoid in shape, and cutinized inner walls of the about 120 species, are found in subtropical to trop- subsidiary cells adjacent to the guard cell scales. ical Central to South America (Rohwer 1993). Fos- Stomatal pore is flat to round topped to slightly sil leaves and reproductive structures of Lauraceae flared, opening slit-like, stomatal index ca. 13.5– are known from mid- and Late Cretaceous locali- 16.3, and subsidiary cell size ca. 4.6–6.3 x 9.2– ties in the Northern Hemisphere, and well-pre- 16.3 µm. served leaves of Lauraceae are commonly found in Comments: Extant species of Lauraceae have Cenozoic floras of Europe, North America, and predominately simple, entire-margined leaves with Australia (Hill 1986; Carpenter et al. 2007). Within acrodromous, brochidodromous, and camptodro- the neotropics, fossil leaves of Laurophyllum are mous venation (Wolfe 1977; Christophel and found in the Miocene of Argentina (Anzótegui and Rowett 1996; Carpenter et al. 2007). Thus, the Aceñolaza 2008), and Nectandra leaves in the character of fossil leaf venation alone is not reliable Cenozoic of Central America, and South America for placement within Lauraceae. A cuticular char- (Engelhardt 1895; Berry 1921a, 1923, 1929, 1936; acter unique to Lauraceae is paracytic stomata Anzótegui and Aceñolaza 2008). The presence of with cuticular scales between the small embedded Ocotea leaves in the Pleistocene of Costa Rica guard cells and overaching subsidiary cells (Ban- (Horn et al. 2003) is now in question due to leaf dulksa 1926; Dilcher 1963; Hill 1986). The pres- similarities of Ocotea and Nectandra. ence of entire leaves with the above mention Order MAGNOLIALES Jussieu ex Berchtold and stomatal character provides a stable placement of Presl, 1820 the fossils with Lauraceae. The fossils provide Family ANNONACEAE Jussieu, 1789 numerous characters that are similar to extant spe- Genus OXANDRA Richard ex Sagra, 1841 cies of Ocotea, Nectandra, and Beilschmiedia such Oxandra sp. as overall leaf shape, size, venation (Figure 1.8– Figure 2.1–2.3. 1.10), epidermal shape, size, and stomatal type. The trapezoid-shaped inner rim scale of the guard Material: Puerto Viejo – UF18882–33609, 33610, cells (Figure 1.12) is characteristic of Ocotea 33611. (Dilcher 1963), Nectandra, and pan-tropical spe- Description: Dispersed carpels of a berry, ellip- cies Beilschmiedia (Nishida and Christophel 1999) soid, 2.4 cm long, 1.3 cm wide, and 0.8 cm high. but in Beilschmiedia the epidermal cells are highly Surface finely verrucose and glabrous, apex sinuate or knobby (buttressed) (Christophel and rounded and base narrows to 0.5 cm wide. Carpel Rowett 1996). wall is woody, 1–1.3 mm thick, black, and the pulp Due to the difficulty of distinguishing between is spongy (Figure 2.1–2.3). Ocotea and Nectandra based on leaf morphology, Comments: Carpel characters (Figure 2.1–2.3) of placement within either genus is not advisable. the fossil are very similar to Annonaceae, and in Here, we follow Hill’s (1986) advice and place our particular Oxandra xylopioides Diels (Figure 2.4)

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FIGURE 2. 1–3, carpels of Oxandra. 1. Side view, UF18882-33609. 2. Side view, UF18882-33610. 3. Sectional view showing woody wall and spongy pulp, UF18882-33611. 4. Immature carpel of extant Oxandra xylopioides, UF1152. 5–10, Parinari sp. 1. 5–7, 9, UF18882-32685. 5. Adaxial surface with epidermal cell walls that are straight to slightly curved. 6. Abaxial epidermal cells and “butterfly-shape” stomates. 7. Partial leaf with numerous regular spaced secondary veins. 8. Line drawing of partial leaf with alternate percurrent tertiary venation, UF18882-53698. 9. Abaxial surface with simple single-celled trichome (arrows). 10. Laminar and petiolar glands (arrows), UF18882-32686. 11, 12, Parinari sp. 2. 11. Side view of elliptical fruit, UF18882-33067. 12. Sectional view of fruit showing thick and bony endocarp with two locules, UF18882-33066. 13. Extant leaf of Parinari excelsa, UF5437. Scale bar for 1–4, and 8 equals 5 mm; 5, 6 equals 20 µm; 7 equals 2 cm; 9 equals 15 µm; 10 equals 0.5 mm; 11–13 equals 1 cm.

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(Diels 1927; van Setten and Koek-Noorman, smooth, cell walls straight to slightly curved (Figure 1992). 2.5). Abaxial surface with simple single celled Annonaceae are a pantropical family of trees, trichomes around sunken stomata; epidermal cells shrubs, rarely subshrubs, or climbers, with 128 mostly pentagonal with some tetragonal (average genera and ca. 2300 species (Kessler 1993). size ca. 5.1 x 6.7 µm), surface smooth, cell walls Oxandra are trees to shrubs, with around 22 spe- straight to slightly curved (Figure 2.6). Stomatal cies, and are found in the West Indies and Panama complex with cells crowded against each other and to South Brazil (Kessler 1993). Fossil seeds of stomata brachyparacytic (stomata average size ca. Annonaceae are known from the Maastrichtian of 9.5 x 11.6 µm). Subsidiary cells form a circular Nigeria, and then diversify in the Eocene London shape with each guard cell distinctly arching out- Clay flora (Doyle and Thomas 1997). Based on the ward into the center of its adjacent subsidiary cell phylogenetic analyses of Annonaceae using rbcL (sometimes referred to as “butterfly-shape” Prance and trnL-F plastid DNA sequences, Oxandra may 1972); subsidiary cell size ca. 6.7 x 10.7 µm (Fig- have originated within the Miocene (Richardson et ure 2.6). al. 2004). Leaves of Annona have been reported in Comments: Morphological characters of the fossil the Tertiary of Venezuela (Berry 1921b, 1936), such as leaf entire, elliptic to oblong shape, basil- Panama (Berry 1918), and in the Miocene of Mex- aminar and petiolar glands, simple trichomes, and ico (Berry 1923) and Costa Rica (Berry 1921a). pinnate venation are similar to Euphorbiaceae (Tet- Leaves of Guatteria are published from the Tertiary rorchiduim), Malpighiaceae (Bunchosia, Byrsonima of Panama (Berry 1918). Annonaceous pollen has [elliptic form], Heteropterys, Lophopterys, and been reported in the Pleistocene of Costa Rica Mascagnia), and Chrysobalanaceae (Parinari and (Kesel 1974). In this report, we correct the previous Licania). In Tetrorchiduim (Burger and Huft 1995), identification of Xylopia (Horn et al. 2003) to Oxan- the placement of the laminar glands, and low num- dra. ber of secondary vein pairs do not match the fossil Order MALPIGHIALES Jussieu ex Berchtold and leaf. In Bunchosia, Byrsonima [elliptic form], Het- Presl, 1820 eropteris, Lophopterys, and Mascagnia (Anderson Family CHRYSOBALANACEAE Brown ex Tuckey, 1982, 1995, 1999, 2001; Amorim 2001; Anderson 1818 and Davis 2001), the low number of secondary Genus PARINARI Aublet, 1775 vein pairs does not match the fossil. The venation Parinari sp. 1 and anatomy of the fossil leaves do suggest a Figure 2.5–2.10 (leaf) close affiliation with Parinari or Licania (Prance 1972). The basilaminar and petiolar glands are Material: Puerto Viejo – UF18882–32684, 32685, characteristic for both Parinari (Figure 2.13) and 32686, 32694, 32695, 32696, 32697, 33596, Licania, along with single celled trichomes on the 33597, 53698. petiole. Both genera have characteristic sunken Description: Leaves petiolate. Lamina incomplete, stomatal regions (Prance 1972). Whole leaf sizes elliptic to oblong, unlobed, symmetrical, 3.3–7.4 cm tend to be smaller than Licania but in the range of long by 1.2–3.5 cm wide, laminar ratio 2.1:1–2.8:1 Parinari (Figure 2.7–2.8, 2.13). The secondary vein (Figure 2.7–2.8). Apex missing, base angle acute angle of divergence resembles Licania, but the to obtuse, with cuneate to rounded flanks; 1–2 number and spacing of secondary veins per side basilaminar sessile glands present (Figure 2.7, resemble Parinari (Figure 2.7–2.8). Adaxial and 2.10). Margin entire. Petiole marginal, 6 mm long abaxial epidermal characteristics are similar and 1–2 mm wide, bearing 1–3 sessile glands and between the fossil, Parinari and Licania but abaxial simple single-celled trichomes (Figure 2.9). Pri- cell surfaces in Licania have some striations while mary venation pinnate; secondary venation Parinari tend to be smooth. Abaxial trichomes are eucamptodromous. More than 21 secondary veins similar to Parinari. The stomata for both Parinari per side, alternate to opposite, spacing regular, and Licania are brachyparacytic and the lateral angle of divergence 50–60, arching slightly from subsidiary cells extend out in a butterfly wing midvein outward to near margin, then arching shape, but stomatal and subsidiary size tends to be abruptly towards apex, unbranched (Figure 2.7, larger than observed for Licania and is in the size 2.8). Tertiary venation alternate percurrent, tertiary range observed for Parinari. When all the charac- vein angle obtuse (Figure 2.8). Adaxial surface gla- ters are considered, the fossils are best placed in brous; epidermal cells mostly pentagonal, some the genus Parinari. tetragonal (average size ca. 6.6 x 9.6 µm), surface

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Chrysobalanaceae are a lowland pantropical Burger and Zamora 1991). A recent review of family of trees and shrubs, with 17 genera and 494 Humiriaceae has determined that Schistostemon species (Prance and White 1988). Parinari is also should be a subgenus of Sacoglottis (Herrera et al. pantropical with 49 species (Prance and White 2010). 1988). The fossil history of Chrysobalanaceae is Humiriaceae are trees and shrubs with eight limited, with pollen found in the Oligocene (Muller genera and 49 species, found in the tropics of Cen- 1981) and phytoliths in the Pleistocene of Panama tral America, South America, and Western Africa. (Piperno and Jones 2003). Sacoglottis, with eight species, are found in Central Parinari sp. 2 America, South America, and Western Africa while Figure 2.11–2.12 (fruit) Schistostemon, with seven species, are found in South America (Cuatrecasas 1961). Fossil fruits of Material: Puerto Viejo – UF18882–33066, 33067. Sacoglottis have been reported from the Oligocene Description: An elliptic drupe, 3.7–5.3 cm long by and Pliocene of Colombia (Reid 1933; Cuatreca- 1.3–2.0 cm wide; tapered apically, base rounded; sas 1961; Wijninga and Kuhry 1990; Wijninga bilocular, each single seeded (Figure 2.11–2.12). 1996), and the Pliocene of Bolivia (Berry 1922). Exocarp smooth, 1 mm thick; mesocarp spongy/ Our specimens are very similar to Sacoglottis ter- fibrous, 1 mm thick; endocarp thick and bony, 3–5 tiaria Berry (1922) of Bolivia. mm thick. Locules 9 mm long by 6 mm wide, Family MALPIGHIACEAE Jussieu, 1789 smooth interior. Fibrous strands near attenuate Genus BYRSONIMA Richard ex Humboldt, Bon- end. pland, Kunth, 1821 Comments: Characters of the fossil (Figure 2.11– Byrsonima sp. 2.12) fit well with Parinari (Prance 1972; van Roos- Figure 3.3–3.5. malen 1985; Roth 1987) except extant Parinari has densely pubescent locules while the locules of the Material: Puerto Viejo – UF18882–33602, 33603, fossil lacks pubescence. The subgenus Licania, 33604, 33605, 33606, 33607. section Pulverulenta, has similar endocarp charac- Description: Fruit with endocarp preserved, non- ters but the exocarp is wrinkled to ridged, and is dehiscent. Shape is globose, apex rounded, and densely pubescent in the locules. Parinari fruits base with a shallow indentation (Figure 3.3). Aver- have been reported in the Miocene of Ethiopia (Tiff- age length 7.6 mm, average equatorial diameter ney et al. 1994), Pliocene of Colombia (Wijninga 7.0 mm. Endocarp woody with rugose surface (Fig- and Kuhry, 1990; Wijninga, 1996) and the Holo- ure 3.4), trilocular with a single seed per locule, cene of Zambia (Phillipson 1976). and vascular bundle down center of the fruit. Loc- Family HUMIRIACEAE Jussieu ex St. Hilaire et al., ules are dorsally depressed ovate and symmetri- 1829 cally arranged about the long axis of the fruit Genus SACOGLOTTIS Martius, 1827 (Figure 3.5). Sacoglottis tertiaria Berry Comments: Fossil fruit characters of shape, three Figure 3.1–3.2. woody carpels, and each carpel with a single locule are similar to the families Euphorbiaceae, Material: Puerto Viejo – UF18882–33581, 33582, Violaceae, and Malpighiaceae. Violaceae fruits are 33583, 33584, 33600, 33601. predominately capsular, dehiscent into three Description: Fruit an elliptical drupe of five valves, valves (van Roosmalen 1985), while in the fossil 2.2–3.2 cm in length by 1.5–2.5 cm in diameter specimen there is no trace of longitudinal grooves (Figure 3.1–3.2) with rounded apex and truncate indicative of capsules. In Euphorbiaceae, drupa- base. Endocarp woody, five carpels radially ceous fruits that are non-dehiscent, and trilocular arranged. Five valves with surface irregularly warty with a single seed per locule is found in Drypetes, and dotted with surface pits representing collapsed although the endocarp is hard but brittle, not evi- lacunae or resin ducts, five septa with smooth sur- dent in the fossil specimen that includes a thick faces united at the apex and base. endocarp (Berry et al. 1999). Within Malpighi- Comments: Characters of the fossil such as aceae, morphological characters of an endocarp shape, size, woody endocarp with irregular warts with a rugose surface, a shallow basal indentation, and collapsed lacunae, and carpel arrangement and locule shape and arrangement place the fossil are similar to Humiriaceae and in particular Saco- within Byrsonima (Figure 3.6–3.7) (Robertson glottis and Schistostemon (Cuatrecasas 1961; 1972, figure 1h, i; Anderson 1982, 1999, 2001; van Roosmalen 1985).

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FIGURE 3. 1–2, fruits of Sacoglottis tertiaria Berry. 1. Side view, UF18882-33584. 2. Apical view showing five valves with surface irregularly warty and dotted with pits representing collapsed lacunae or resin ducts, UF18882-33582. 3–5, fruits of Byrsonima. 3. Basal view with a shallow indentation, UF18882- 33603. 4. Side view of Figure 3.3 with rugose surface. 5. Transverse section of 3 locular, single seeded fruit, UF18882-33602. 6. Transverse section of 3 locular, single seeded fruit of extant Byrsonima lucida, UF1151. 7. Side view of Figure 3.6 before sectioned. 8–12, Ingeae leaflet, UF18882-33578. 8. Complete oblong leaflet. 9. Abaxial short trichome. 10. Marginal trichome that is unicellular and conical. 11. Adaxial surface, epidermal cell walls straight to slightly curved. 12. Abaxial epidermal cells and stomates. 13. Leguminocarpon with wall peeled away to reveal ovate seeds perpendicular to fruit length, UF18882- 33577. Scale bar for 1, 2, 6, and 7 equals 5 mm; 3–5 and 8 equals 3 mm; 9–12 equals 15 µm; 13 equals 1 cm.

9 LOTT ET AL.: PLEISTOCENE FLORA COSTA RICA

Malpighiaceae are pantropical to subtropical to the tribes Mimoseae (Acacia) and Ingeae (Albi- trees, shrubs, subshrubs, or lianas, with 66 genera zia, Pithecellobium, Calliandra, and Zapoteca) and 1200 species (Anderson 1990). Byrsonima are (Woodson and Schery 1950; Leelavathi and trees, shrubs, or subshrubs with 135 species, Ramayya 1982; Ghosh and Roy 1986; Grosso et found in S.E. Florida, the Caribbean, and from al. 1994; Ogundipe and Akinrinlade 1998). Acacia Mexico to South America. Fossil pollen of Malpighi- and Pithecellobium tend to be amphistomatic while aceae are found in the Miocene of Costa Rica Calliandra and Zapoteca are hypostomatic. Albizia (Graham 1987a, b) and leaves in the Tertiary of shows both amphistomatic and hypostomatic con- Panama (Berry 1918). Fossil pollen of Byrsonima dition, although when amphistomatic, the adaxial occurs in the Quaternary of Costa Rica (Kesel stomata are very sparse. Acacia, Albizia, Pithecel- 1974; Horn 1985; Graham and Dilcher 1995). lobium, and Calliandra tend to have both paracytic Order FABALES Bromhead, 1838 and anisocytic stomata with equal to unequal sub- Family FABACEAE Lindley, 1836 sidiary cells and unicellular hairs. Calliandra and Subfamily MIMOSOIDEAE de Candolle, 1825 Zapoteca epidermal cell walls are sinuate. Tribe INGEAE Bentham and Hooker, 1865 Although no one genus contains all the characters noted in the fossil, Ingeae seems closer in charac- Morphotype PV1-28 ter traits to the fossil. More than one specimen is Figure 3.8–3.12 (Leaflet) needed for character variability, allowing for a more Material: Puerto Viejo – UF18882–33578. precise placement within a recognized taxa, so a Description: Leaflet complete, oblong, asymmetri- temporary Morphotype category (Johnson 1989) cal, unlobed, 7–8 mm long by 2.5–3.0 mm wide, will be used. lamina ratio 2.6:1–2.8:1 (Figure 3.8). Apex angle The tribe Ingeae are trees, shrubs, or rarely acute and mucronate, with convex flanks, base climbers, found in the pantropical to subtropical angle obtuse, with concavo-convex flanks. Margin regions, with 17 genera and ~1000 species entire. Petiole missing. Primary venation pinnate; (Nielsen 1981; Herendeen et al. 1992). Ingeae pol- secondary venation brochidodromous, basal sec- len is known from the Eocene of Egypt (Herendeen ondary veins present and arching upward to mid- et al. 1992), and possible leaflets from the Eocene section of leaflet. Secondary vein spacing of Kentucky (Herendeen and Dilcher 1987) and the increasing toward base. Adaxial surface with short Tertiary of Costa Rica (Berry 1921a, Graham unicellular trichomes (average size ca. 2 x 25 µm) 1992). with an acute apex (usually broken off) and thick- Genus LEGUMINOCARPON Goeppert, 1855 ened base; epidermal cells mostly tetragonal, Leguminocarpon sp. 1 some pentagonal (average size ca. 7.4 x 13.6 µm), Figures 3.13, 4.1–4.2 (fruit) surface smooth, cell walls straight to slightly curved (Figure 3.11). Abaxial surface with short trichomes Material: Puerto Viejo – UF18882–33575, 33576, (average size ca. 3 x 40 µm) with an acute apex 33577. (usually broken off) and slightly thickened base Description: Pod fragmented, > 5.5 cm long by 1– (Figure 3.9); epidermal cells mostly tetragonal, 1.9 cm wide, linear to slightly curved, straight; some pentagonal (average size ca. 8 x 19.2 µm), rounded to short tapered apex and oblique with surface smooth, cell walls straight to arcuate (Fig- longitudinal axis of fruit; curved tapered base ure 3.9). Marginal trichomes present, unicellular, aligned with longitudinal axis of the fruit (Figures and conical (average size ca. 15 x 90 µm) (Figure 3.13, 4.1–4.2). Marginal sutures 1 mm thick, 3.10). Stomatal complex random and hypostom- medial along entire length of fruit, possibly dehis- atic, paracytic to anisocytic (stomata average size cence along one suture. Fruit non-winged, and sur- ca. 7.5 x 17 µm) with thin inner rim, stomatal index face with small papilla. Seeds 9–10 mm long by 5– 9.7; in paracytic stomata, subsidiary cells equal to 6 mm wide, ovate, perpendicular to fruit length; unequal in size, (average size ca. 4.7 x 26.1 µm) funiculus 3 mm long by 0.5 mm wide. (Figure 3.12). Comments: The fragmented nature of the pods Comments: Overall shape and size of the fossil makes it difficult to place this fossil within a sub- leaflet is similar to Zygophyllaceae except in Zygo- family status, although the papillose nature of the phyllaceae there are more basal secondary veins, fruit wall is not usually found in the subfamily Caes- and the leaflets are amphistomatic. The leaflet alpinioideae (Cowan 1981). Although a fruit that is architecture, prominent basal secondary veins, and dehiscent along one suture can be found in all trichomes of the fossil (Figure 3.8–3.9) are similar three subfamilies, the general shape of the pod,

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FIGURE 4. 1, 2, Leguminocarpon . 1. Basal section with curved tapered base, UF18882-33576. 2. Apical section with rounded apex oblique to longitudinal axis, UF18882-33575. 3–6, partial leaves, and cuticle of Pouteria. 3. Apical section with short attenuate, rounded end apex, UF18882-45285. 4. Line drawing of partial leaf with festooned brochidodromous venation, UF18882-53697. 5. Adaxial surface with sinuate epidermal cell walls, UF18882-32803. 6. Abaxial surface with sinuate epidermal cell walls, and stomata (arrow), UF18882-32803. 7. Ellipsoid seed of Pouteria with hilum covering full length of seed, UF18882- 32825. 8. Extant seed of Pouteria, UF1153. 9. Extant leaf of Pouteria torta, UF5208. 10. Line drawing of Incertae Sedis leaf with festooned brochidodromous secondary venation, and two series of unorganized exmedial loops, UF18882-53700. Scale bar for 1–3 equals 1 cm; 4, 7, 8, and 10 equals 5 mm; 5, 6 equals 20 µm; 9 equals 2.5 cm.

11 LOTT ET AL.: PLEISTOCENE FLORA COSTA RICA

base, and apex of the fossil fruits (Figures 3.13, abaxial cell walls are straight to slightly undulating 4.1–4.2) are close to Albizia and Havardia (Mimos- (UF5127, 5131, 5212; Watson and Dallwitz 1983, odieae: Nielsen 1981; Kirkbridge et al. 1999). The 1993). Although characters such as attenuate fossil fruits share characters with Albizia such as apex, festooned brochidodromous venation, lack of apex oblique to longitudinal axis and margin with a marginal vein, and a flat midrib (Pennington thickened sutural area, but again the fragmentary 1990) place the fossil leaf close to Pouteria, the nature of the fossils preclude placement within fragmentary nature of the leaves prevent a precise Albizia. Mimosites has been used for fossil legume affiliation to any one species, so we place the fossil fruits and leaves but this name should be restricted into the morphotype designation. to the tribe Mimoseae (Herendeen and Dilcher Sapotaceae are pantropical trees, shrubs, or 1990). lianas, with 53 genera and 1100 species. Pouteria Calliandra pollen has been found in the Qua- are pantropical with 325 species and are confined ternary of Panama (Barlett and Barghoorn 1973) to lowland rainforest below 1000 m altitude (Pen- and the Pliocene of Colombia (Caccavari 1996) nington 2004). Fossil pollen of Sapotaceae are while Calliandra and Acacia pollen are found in the found worldwide through the Cenozoic (Harley Pleistocene of Costa Rica (Kesel 1974). 1990) and more specifically of Pouteria in the Plio- Order ERICALES Berchtold and Presl, 1820 cene and Pleistocene of Costa Rica (Kesel 1974; Family SAPOTACEAE Jussieu, 1789 Graham and Dilcher 1998). Fossil Sapotaceous Genus POUTERIA Aublet, 1775 leaves are found in the Eocene/Miocene of Argen- tina (Berry 1938). Morphotype PV1-12 Figure 4.3–4.6 (leaf) Morphotype PV1-27 Figure 4.7 (seed) Material: Puerto Viejo – UF18882–32803, 32804, 33598, 33599, 45285, 53697. Material: Puerto Viejo – UF18882–32825. Description: Lamina incomplete, elliptic, unlobed. Description: Seed ellipsoid, 3.3 cm long by 1.4 cm Apex short attenuate, rounded end (Figure 4.3) wide, hilum adaxial covering full length of seed, and micro aristate, base fragmented but tending scar 2 mm wide at base, 8.0 mm wide at apex (Fig- convex. Margin entire. Primary venation pinnate, ure 4.7). secondary venation festooned brochidodromous Comments: Fossil seed characters of shape, and with two-three series of exmedial loops, last series hilum position and extent fits well in Sapotaceae, close against the margin (Figure 4.4). Secondary and in particular Pouteria (Figure 4.8). veins alternate, spacing irregular, angle of diver- INCERTAE SEDIS gence 50–60º. Secondaries gently curving upward and out toward the margin. Secondary attachment Morphotype PV1-16 decurrent. Intersecondary veins 1–3 per intercosta, Figure 4.10 traversing more or less one half the distance to the Material: Puerto Viejo – UF18882–53700. margin then forking into two branches and joining Description: Lamina incomplete, elliptic, unlobed, adjacent intersecondaries or secondaries. Tertiary > 2 cm long by 1.7 cm wide. Apex missing, base and quaternary veins irregular reticulate, marginal slightly cordate with rounded flanks (Figure 4.10). vein lacking, midrib flat. Adaxial surface glabrous; Margin entire. Primary venation pinnate, secondary epidermal cells mostly tetragonal (average size ca. venation festooned brochidodromous with two 12.9 x 17.6 µm), surface smooth, cell walls sinulate series of unorganized exmedial loops. Secondary to sinuate (Figure 4.5). Abaxial surface glabrous; veins alternate, spacing irregular, angle of diver- epidermal cells mostly tetragonal (average size ca. gence 52–86º. Ascendence of secondaries 12.1 x 17.0 µm), surface smooth, cell walls sinuous unequal, one side with two secondary loops reach- to sinuate (Figure 4.6). Stomata paracytic to ano- ing middle of lamina, other side with three second- mocytic (average size ca. 8.5 x 11.5 µm), stomatal ary loops reaching middle of lamina. index 10.8. Intersecondaries 1–2 per intercosta, traversing Comments: The form and venation of the fossil less than or more than one half the distance to leaves are very similar to Pouteria (Sapotaceae) margin then joining tertiary veins. Tertiary and qua- (Figure 4.9) and Macrolobium (Leguminosae). The ternary veins irregular reticulate, marginal vein adaxial and abaxial sinuate cell walls of the fossil present. are very similar to Pouteria while in Macrolobium,

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TABLE 1. Megafossil abundance for site PV1, Rio Puerto Viejo, Costa Rica.

Reproductive Taxon Organ Leaf abundance abundance Byrsonima Fruit 9.8%

Ingeae Leaflet 0.4%

Leguminocarpon Legume 2.7% Laurophyllum Leaf 1.6%

Oxandra Carpels 10.7%

Parinari Leaf 50.3% Parinari Fruit 32.1%

Piperites Leaf 0.4%

Pouteria Leaf 31.3% Pouteria Seed 5.3%

Sacoglottis Fruit 9.8%

DISCUSSION an overrepresentation of streamside plants, or dif- ferential aerial transport of more distant species The Pleistocene fossil flora collected along (MacGinitie 1953; Wolfe 1971; Spicer 1981). The the Río Puerto Viejo contains fragmentary leaves, fact that almost all the fossil leaves are small and cuticle, wood, fruits, and seeds, adequately pre- fragmentary suggests mechanical fragmentation of served to allow detailed morphological and ana- streamside plants in a fluvial setting. Further field tomical observations. This fossil flora sits within a examination needs to be done for a proper tapho- gray layer of clay-rich volcanic material, which, in nomic analysis of the leaves, such as the direction turn, is overlain by sedimentary deposits and mod- of the midvein to explore if the leaves were ori- ern soil horizon at the top of the riverbank (Horn et ented in the same direction and comparing the al. 2003). The depositional soil near Puerto Viejo is deposit with modern leaf deposits in similar envi- classified as old alluvial terraces, Pleistocene River ronments along the Rio Puerto Viejo. terraces (Sollins et al. 1994). The fossiliferous gray The Puerto Viejo Pleistocene sediments con- layer was initially described as a fluvially reworked tain macrofossils of leaves, fruits, and seeds of 43 volcanic deposit (Alvarado 1990), but subsequent morphotypes, 11 of which have been determined to lab analyses of feldspar grains and detritus in this the Tribe, Family, Genus, or Species level (see gray sediment indicated a primary airfall deposit Horn et al. 2003 for identifications of fossil wood, (Horn et al. 2003). Except for a single leaflet, all the pollen, and spores). Of the undetermined morpho- fossil leaves examined from this layer are fragmen- types, most have an abundance of less than 0.4 %. tary, and the sizes are under 8 cm long. The size Of the 11 identified taxa, five are fragmentary leaf/ range for extant species that are related to the fos- cuticle types, and six are whole fruit/seed types. sil leaves include Pouteria, up to 45 cm long (Pen- Leaves that dominate the paleoflora are Parinari nington 1990), Parinari up to 17 cm long (Prance (50.3%) and Pouteria (31.3%). Other leaves are 1972), Piper (multi-nerved species, Bornstein Laurophyllum (1.6%), Piperites (0.4%), and Ingeae 1989) up to 20 cm long, and Costa Rica species of (0.4%). Reproductive units that dominate the flora Ocotea/Nectandra up to 55 cm long (Burger and are Parinari (32.1%), followed by Oxandra (10.7%), Werff 1990). The lack of large leaves may be due Sacoglottis and Byrsonima (9.8% respectively), in part to the collection methods, which involved Pouteria (5.3%), and Legumincarpon (2.7%) (Table cutting out blocks of material that would fit in plastic 1). Fossil Parinari represents half of the leaves and bags ca. 20 cm x 20 cm in size. The condition of nearly one-third of the fruits recovered, with an the leaves in the flora may also reflect the fact that extant distribution in the lowland tropics. Although larger leaves tend to become fragmented and Parinari is lacking in the modern flora of La Selva, it destroyed in turbulent conditions (Wolfe 1971), and is present at nearby higher elevations of 500 m they do not travel very far via air currents (Roth and (Horn et al. 2003). Another extant lowland tropical Dilcher 1978). In comparison, small leaves may be species is Pouteria, with a high percentage of fossil

13 LOTT ET AL.: PLEISTOCENE FLORA COSTA RICA

Pouteria leaves in the fossil flora. Pouteria, which are fragmented suggesting a fluvial deposit but fur- grows at La Selva today, increases in abundance ther taphonomic analysis is required to confirm this from 300–600 m (Pringle et al. 1984; Lieberman et assessment. The fossil flora is similar to modern al. 1996). Sacoglottis and Byrsonima can be found Costa Rica tropical forest and shows a biogeo- living at La Selva and up to 500–1000 m (Burger graphic connection with northern South America. and Zamora 1991). The close relatives of Lauro- phyllum are found in La Selva (Nectandra) and in ACKNOWLEDGMENTS higher elevations of 2300–2600 m (Ocotea) (Wilbur The authors wish to thank K. Perkins (FLAS), 1994; Lieberman et al. 1996). Oxandra seems to G. Russell (SI), and J.C. Solomon (MO) for access be lacking in La Selva and higher elevations near to herbarium specimens; M. Baranova and C. Jef- La Selva. Pentaclethra macroloba dominates the frey (Komarov Botanical Institute, Russia) for cuti- extant primary lowland forest of La Selva (35–150 cle preparation techniques; S. Manchester m), is not dominant at 300 m (Pringle et al. 1984) (FLMNH) for help in fruit and seed identification and is lacking in the fossil flora. The preceding dis- and manuscript suggestions; and H. Wang tributions suggest that the fossil flora has some (FLMNH), D. Christophel (Denver University), B. connection to a slightly higher elevation tropical Hammel (MO), R. Burnham (Michigan), C. Jara- forest of present-day Braulio Carrillo National Park millo (STRI), and one anonymous reviewer for (Hartshorn and Hammel 1994; Lieberman et al. helpful comments. This is the University of Florida 1996), just south of La Selva. The Quaternary Contribution to Paleobiology publication number period included 18–20 glacial-interglacial cycles 555. (Johnson 1982; Davis 1983). In the mountains of Costa Rica, cooling during Quaternary glacial inter- REFERENCES vals resulted in altitudinal shifts downward in species ranges and vegetation belts (Martin 1964; Alvarado I., G.E. 1990. Características geológicas de la Hooghiemstra et al. 1992; Islebe et al. 1995; Islebe Estación Biológica La Selva. Tecnologia en Marcha, and Hooghiemstra 1997). Extrapolating from mod- 10:11–22. ern ranges of the preceding species and surface Amorim, A.M. 2001. Two new species of Heteropteris temperature lapse rates (Horn et al. 2003), the (Malpighiaceae) from southeastern Brazil. Contribu- tions from the University of Michigan Herbarium, macrofossil flora of La Selva suggests paleotem- 23:29–34. peratures 2.5–3.1°C cooler than at present, which Anchukaitis, K.J. and Horn, S.P. 2005. A 2000-year may coincide with fluctuations in the Quaternary reconstruction of forest disturbance from southern climate. The fossil flora is similar to the modern Pacific Costa Rica. Palaeogeography, Palaeoclima- Costa Rican tropical forest, which has a biogeo- tology, Palaeoecology, 221:35–54. graphic connection with tropical forest of Northern Anderson, W.R. 1982. Notes on Neotropical Malpighi- South America (Gentry 1990). This biogeographic aceae-I. Contributions from the University of Michi- connection shows up in the fossil record of Central gan Herbarium, 15:93–136. and Northern South America (Burnham and Gra- Anderson, W.R. 1990. The origin of the Malpighiaceae – ham 1999). Genera and families in common with the evidence from morphology. Memoirs of the New previous reports of the fossil flora of Costa Rica York Botanical Gardens, 64:210–224. Anderson, W.R. 1995. Notes on Neotropical Malpighi- and Northern South America include Parinari, aceae-V. Contributions from the University of Michi- Sacoglottis, Piperaceae, and Annonaceae gan Herbarium, 20:15–36. (Engelhardt 1895; Berry 1921a, b, 1922, 1923, Anderson, W.R. 1999. Notes on Neotropical Malpighi- 1936; Wijninga and Kuhry 1990; Wijninga 1996). aceae-VII. Contributions from the University of Michi- gan Herbarium, 22:1–19. CONCLUSIONS Anderson, W.R. 2001. Notes on Neotropical Malpighi- aceae-VIII. Contributions from the University of Mich- Plant species identified in the Rio Puerto Viejo igan Herbarium, 23:63–81. deposit lived in a lowland neotropical forest of Anderson, W.R. and Davis, C.C. 2001. Monograph of Northeastern Costa Rica during the Pleistocene Lophopterys (Malpighiaceae). Contributions from the (younger than 915 ka), with cooler paleotempera- University of Michigan Herbarium, 23:83–105. tures than at present. Sedimentary analysis of the Anzótegui, L.M. and Aceñolaza, P.G. 2008. Macrofloristic gray layer from which the fossils were found sug- assemblage of the Paraná Formation (Middle-Upper gests a fluvially reworked volcanic or primary airfall Miocene) in the Entre Ríos (Argentina). Neues deposit. Except for a single leaflet, all the leaves Jahrbuch fur Geologie und Palaontologie Abhandlun- gen, 248:159–170.

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