PETER WILF Department of Geosciences Pennsylvania State University 537 Deike Building University Park, PA 16802

Abstract—The great bulk of the angiosperm fossil record consists of isolated fossil leaves that preserve abun- dant shape and venation ( architectural) information but are diffi cult to identify because they are not attached to other organs. Thus, poor taxonomic knowledge has tempered the tremendous potential of fossil leaves for constructing fi nely resolved records of biodiversity through time, extinction and recovery, change and biotic response, , and plant- associations. Moreover, paleoecological and paleo- climatic interpretations of fossil leaves are in great need of new approaches. Recent work is rapidly increasing the scientifi c value of fossil angiosperm leaves through advances in traditional paleobotanical reconstruction, phylogenetic understanding of both leaf architecture and the response of leaf shape to climate, quantitative plant using measurable, correlatable leaf traits, and improved understanding of insect leaf-feeding damage. These emerging areas offer many novel opportunities to link paleoecology and neoecology. Increased collabo- ration across traditionally separate research areas is critical to continued success.

INTRODUCTION 1982). For these and other reasons, the broader fi eld of paleobotany tends to avoid the angiosperm leaf re- Leaves, the most visible plant organs, are by far cord, paleobotany courses typically “run out of time” the most abundant type of plant fossil. However, fos- before the topic arrives, and the most voluminous sil leaves, especially those of angiosperms (fl ower- source of potential data that paleobotany has to of- ing ), are notoriously diffi cult to identify. They fer is generally kept out of sight or considered mostly are often found in isolation and without preservation decorative. of organic material (i.e., as impressions). A fossil Despite this diffi cult , fossil fl oras domi- leaf considered “excellent” on the outcrop due to its nated by isolated angiosperm leaves are somehow beauty and apparent completeness (Fig. 1) typically providing data for a large number of recent publica- preserves only a size, a shape, and a venation pattern. tions in respectable journals, especially paleoecologi- Less often, organic materials with additional charac- cal and paleoclimatic studies related to past climate ters are present, such as cuticular remains, or attach- change and extinction. How can this be? I focus here ments to other leaves or leafl ets are preserved. Very on a selection of developing research areas where fos- rarely, leaves may be attached to diagnostic fl owers sil angiosperm leaves play a central role. I fi rst discuss or . These problems are especially acute for the the legacy issues mentioned above and how overcom- angiosperms, due to their high diversity, abundance, ing them is an important and interesting research goal, and phenotypic plasticity from to Recent. combining subdisciplines that often work separately. Early angiosperm paleobotanists, though deserving I then give an overview of recent developments, in great credit as scientifi c pioneers, fi lled the literature plant functional ecology, paleoclimate, and plant-ani- with an apparently intractable legacy: thousands of in- mal interactions, that have much potential to provide correct assignments to extant genera based on super- important new links between paleoecology and neo- fi cial comparisons (discussed in Dilcher, 1974; Hill, ecology.

In From to : Research Questions Driving at the Start of a New Century, Paleontolog- ical Society Short Course, October 4, 2008. Paleontological Society Papers, Volume 14, Patricia H. Kelley and Richard K. Bambach. (Eds.). Copyright © 2008 The Paleontological Society. 320 PETER WILF

Figure 1—A typical ‘problem child’ from the Laguna del Hunco fl ora, early Eocene of , Argentina (Museo Paleontológico Egidio Feruglio, MPEF-PB 979; note 1 cm scale bar). This cosmetically attractive, three-lobed leaf is one of 109 specimens of this morphotype in the fl ora; the morphotype has not been found attached to other plant organs and also apparently lacks organic preservation. The distinctively regular primary veins originating from a single point at the base, along with other features, allow placement in the large family Malvaceae s.l. (> 240 genera, > 4200 species). Further taxonomic placement is unlikely, although there are sim- ilarities to the genus Brachychiton. Leaf shape in the morphotype, known currently as “Malvaceae sp. TY23,” shows wide variation in lobe incision and width as well as leaf size, though placement in a single morphotype is aided by the large sample size, which allows observation of the continuum of variation. Consistent features across the sample include palmate lobation with three (sometimes two) lobes and primary veins originating from a single point; the lobes convex-sided, with pointed acute apices; the lobe sinuses rounded, incised up to >50% to >80% of the distance to midvein; the leaf margin typically untoothed; and the secondary veins brochi- dodromous (prominently looped) apically but interior (joining the primary veins together) basally. Malvaceae sp. TY23 is a good example of the many types of data fossil leaves typically provide; its presence contributes to the high estimated plant richness of this fl ora (over 150 leaf morphotypes), its relative abundance to paleo- ecological data and diversity analyses, its stratigraphic positions to the timing of paleoenvironmental events, its lack of teeth to a warm paleotemperature estimate from the whole fl ora (16.6 ± 2.0 deg. C; interestingly, there are teeth on a single specimen), its generally large leaf area (reconstructed as 5344 mm2 on this specimen) to a moist paleoprecipitation estimate from the whole fl ora (114 +49.1, -34.3 cm/y), its area and width (2.5 mm on this specimen) to estimated leaf mass per area (for this specimen: 89 g/m2, 95% prediction range 68 to 117 g/m2), and its abundant and diverse associated insect damage, found on many other plant hosts in the fl ora as well, to interpretations of elevated plant-animal associations and ecosystem diversity in Eocene Patagonia (Wilf et al. 2003a, 2005a, 2005b). Insect damage on this specimen includes, from top to bottom arrow, poly- lobate hole feeding (damage type 3 of Labandeira et al. 2007), deeply incised margin feeding (DT15), surface feeding (DT29), and curvilinear hole feeding (DT7, bottom two arrows), all of which are generalist damage types conceivably made by a single feeding insect. FOSSIL ANGIOSPERM LEAVES 321

THE LEAF MORPHOTYPE - guide to character distribution across the angiosperms; DIALECTIC two useful contributions have come from tropical plant identifi cation guides that make extensive use of leaf When anatomical and epidermal features are not architecture (Gentry, 1993; Keller, 2004). Thus, fossil preserved, fossil angiosperm leaves are most often leaf identifi cation requires great fi rst-hand knowledge, reliably assigned using attachments, which are rare derived from personal experience of cleared-leaf col- (Crane and Stockey, 1985; Manchester et al., 1986; lections (available in very few institutions), herbaria, Boucher et al., 2003; Zamaloa et al., 2006), or repeated and living specimens, of immensely complex visual co-occurrence (Wing and Hickey, 1984; Manchester patterns and their distributions among the world’s and Hickey, 2007) with other organs considered diag- plants. The need for this broad geographic knowledge nostic, most often fl owers, fruits, and . This ap- is greatest for Cretaceous and Paleogene fl oras (and proach attains high botanical precision but usually for many Neogene, especially Miocene assemblages), a small minority of the leaf species inferred to be pres- which typically have little compositional relationship ent. Thus most leaf fl oras, including many with high to that of the modern site, or even to the continent apparent richness, remain poorly known taxonomi- where they are found. cally. There are exceptions: sustained efforts by S.R. A great opportunity now exists to re-evaluate Manchester and colleagues on the typically low-diver- angiosperm leaf architecture within the overhauled sity fl oras of the Western Interior USA have phylogenetic context offered by molecular data (An- deciphered a large percentage of leaf taxa (e.g., Crane giosperm Phylogeny Group, 2003). The phylogenetic et al., 1991; Manchester et al., 1999; Manchester and signal, homoplasy, and character evolution of leaf ar- Hickey, 2007). One signifi cant outcome of botanical chitecture can be investigated quantitatively, and this reconstructions, underscoring the hazards of identify- will eventually lead to greater confi dence in the phylo- ing isolated fossil leaves, is the frequent recognition genetic signifi cance of particular characters when they of extinct genera. These often incorporate specimens are found in . Preliminary work already shows previously diagnosed to extant genera before attach- phylogenetic signal and evolutionary patterns across ment or associational evidence emerged (Manchester, the angiosperms in broad traits such as vein organiza- 1989, 2001; Manchester et al., 1998). tion, leaf shape, and major venation category (Doyle, For leaves without recognized attachments, co- 2007; Green and Little, 2007), as well as confi rmation associations, organic material, or anatomy, i.e., the and possibility of refi nement for many of the patterns great majority of the record, we turn to the leaf im- noted by Hickey and Wolfe (1975). Phylogenetic sig- pressions themselves, where we typically fi nd a great nal also emerges in leaf shape variables, long assumed deal of data on shape and the fi ne details of venation to be convergent, that are signifi cant for paleoclimate (leaf architecture). These features are highly variable estimates (Little et al., 2008, discussed below). Within and quite subtle among living plants, and it is here plant lineages, leaf architectural characters are increas- that early fossil workers made many mistakes. Widely ingly used in cladistic evolutionary studies, including used, detailed descriptive terminology now exists for characters selected for investigation precisely because leaf architecture (e.g., Hickey, 1973; Ash et al., 1999; they are often preserved in fossil leaves (Doyle and Ellis et al., 2009), which has been studied for several Endress, 2000; Eklund et al., 2004; Fuller and Hickey, extant groups (e.g., Carr et al., 1986; Keating and Ran- 2005; Scharaschkin and Doyle, 2005; Manos et al., drianasolo, 1988; Hickey and Taylor, 1991; Todzia 2007). and Keating, 1991; Gandolfo and Romero, 1992; Liu, Although advancement of phylogenetic leaf archi- 1996; Premoli, 1996; González et al., 2004; Fuller and tecture will greatly improve hypotheses about the bo- Hickey, 2005; Martínez-Millán and Cevallos-Ferriz, tanical affi nities of many fossil angiosperm leaves, the 2005). However, since a major overview paper by bulk of taxa, especially from older (Cretaceous and Hickey and Wolfe (1975), which showed systematic Paleogene) fl oras will remain unidentifi ed for some signal in leaf architecture with great utility for identi- time to come, especially because the discovery rate fying fossils (e.g., Hickey, 1977; Wolfe, 1977; Wolfe of new forms remains high. In addition to taxonomy, and Wehr, 1987), there has been no detailed or updated there is a strong need to estimate the total number of 322 PETER WILF

species in a fl ora and analyze their characteristics, as tion and proper illustration of all the morphotypes in a major data source that can be tied to robust stratig- a fl ora is essential, even as a parataxonomy, though raphy, , and paleoclimate records. Leaf this rarely occurs (e.g., Hill, 1982; Crane et al., 1990; architecture allows the discrimination of morphologi- Dilcher and Lott, 2005; Danehy et al., 2007). Con- cally discrete sets of species-like entities, called mor- versely, collections made in pursuit of a small number photypes, within fossil (and extant) fl oras (Johnson et of targeted botanical entities are much more valuable al., 1989; Ash et al., 1999). Morphotypes are highly if a full suite of associated taxa and organs is collected, defensible compared to the old practice of assigning including leaves, and more so yet if abundance data all fossils, no matter how fragmentary and question- are captured. These statements are easily made, but in able, to extant genera. They derive from vouchered practice it can be quite diffi cult in the fi eld to broaden specimens and are subject to review by later investi- one’s search image and resource investment beyond gators. Leaf morphotypes may or may not be equiva- the initial target that motivated the fi eld work. Linking lent to named entities; if not, when they are eventually morphotyping and systematics from the start of a proj- taxonomically assigned they carry no nomenclatural ect is therefore a robust recipe for diverse successes. baggage. An example of this type of collaboration is a cur- The major advantage of morphotypes is that they rent project on latest Cretaceous and Paleogene fossil can comprise a parataxonomy for an entire fossil fl ora, fl oras of Patagonia, Argentina. We have collected more usually associated with abundance, paleoecological, than 12,000 plant fossils with precise stratigraphic and stratigraphic data. They make possible important control, including more than 400 leaf morphotypes, to treatments of whole-fl ora ecology, diversity, climate answer a set of initial questions about plant diversity, analysis, and many other topics, as well as illustra- plant-insect associations, paleoclimate, and geochro- tions and descriptions that are free of taxonomic er- nology (Wilf et al., 2003a, 2005a, 2005b; Iglesias et rors. For example, leaf morphotypes play a major role al., 2007, 2008a). At the same time, the collections al- in many studies of regional biodiversity through time, low systematic delineation of many important botani- including extinction, recovery, and response to climate cal entities, usually based on leaves with or at- change (Wolfe and Upchurch, 1986; Johnson et al., tached or associated reproductive structures (Zamaloa 1989; Wing et al., 1995; Wilf, 2000). Their obvious et al., 2006; Gandolfo et al., 2006, 2007; González et disadvantage is that they are to various degrees un- known as botanical entities, and their widespread use al., 2007; Wilf et al., 2007, 2008), as well as new ich- in high-profi le publications perhaps sends a message notaxonomic entities from fossilized insect folivory to students that taxonomy doesn’t matter very much. (Sarzetti et al., 2008). Thus, simultaneous advances in Thus, leaf morphotypes generate reproducible science geological and ecological as well as systematic aspects that has greatly increased the profi le of paleobotany of paleobotany are being made in a large and produc- in diverse fi elds such as climate change and paleocli- tive fi eld area, little investigated since the 1920s and matology, geochemistry, stratigraphy, ecology, and 1930s (, 1925, 1937, 1938). The morphotypes the other major branches of paleontology. At the same create a stable organizational substrate for hundreds time, they are “diffi cult children” that often cause un- of species represented by thousands of specimens, ease among botanists and paleobotanists. from which taxonomic entities can be recognized and The resolution to this dialectic is collaboration, large-scale questions of pattern can be asked. Less cooperation, and diversifi cation of interests. Leaf formal cooperation also yields results: bulk collec- morphotypers typically pursue large sample sizes tions of late Paleocene leaves in Wyoming that were and statistical signifi cance to test large-scale patterns, used in a study of insect damage through time (Wilf and some of the largest and stratigraphically best- et al. 2006) included well-preserved fossil fruits that constrained fossil plant collections in the world are contributed to resolving an associated Paleocene leaf the result. However, these collections must be made species long considered enigmatic (now Browniea with great attention to the relatively rare fossil fl ow- serrata, Nyssaceae: Manchester and Hickey, 2007). In ers, seeds, fruits, cuticles, and attachments that allow addition, prospecting for fossil plants in the area led to systematics to be done. In addition, eventual publica- the discovery of an important, 40Ar-39Ar dated volca- FOSSIL ANGIOSPERM LEAVES 323 nic ash that precisely constrains the fl oras, including Swenson and Enquist, 2007), using straightforward the Browniea occurrences (Secord et al., 2006). metrics such as R2 and p, to reveal how the constituent I note in passing the great potential for reinvestigat- species of a community vary in resource deployment ing leaf fossils with epifl uorescence microscopy (e.g., and strategy. Traits that typically have high vari- Friedrich and Schaarschmidt, 1979; Schaarschmidt, ance within a community are especially informative 1982; Kerp and Krings, 1999), which allows rapid for interpreting ecology at the species level. However, scanning of numerous specimens to reveal detailed, it is challenging to identify traits that can be measured informative features on an overlooked few that may in fossils or estimated by proxy. For fossil , have appeared only to be impressions or coalifi cations body size has a long history of ecological interpreta- under conventional light microscopy. The technique tion from fossils via scaling from tooth dimensions has been highly productive in our lab. For example, (e.g., Alroy, 1998). in-situ grains in fossil fl owers may fl uoresce For plants, leaf mass per area has emerged from a brightly but be invisible under SEM because they are wealth of recent literature in as centrally located just under the matrix surface (Iglesias et al., important in defi ning communities along resource gra- 2008b). Leaf cuticles too fragile to isolate safely with dients (Reich et al., 1991, 1997, 1999; Ackerly and chemicals, and so thin as to be nearly undetectable un- Reich, 1999; Wright et al., 2004, 2005a, 2005b). Leaf der ordinary light, can be investigated in-situ and non- mass per area (which is also the inverse of specifi c leaf destructively (Wilf et al., 2008; Iglesias et al., 2008a). area) varies signifi cantly within sites and correlates signifi cantly with related traits including leaf lifes- pan (+), leaf toughness (+) and thickness (+), nitrogen FUNCTIONAL LEAF TRAITS: A content (-), and photosynthetic capacity (-). In turn, QUANTITATIVE LINK FROM these intercorrelated traits also correlate with plant PALEOECOLOGY TO NEOECOLOGY defense and palatability to herbivores; for example, leaves with high leaf mass per area tend to have low Fossil plant deposits contain a vast reserve of un- concentrations of nitrogen and are thus demonstrably dertapped, diverse ecological information (recently less palatable to insects (Coley, 1983; Coley and Bar- reviewed comprehensively by DiMichele and Gastal- one, 1996). do, 2008). Deep-time paleoecology, in general, con- A recent collaboration of 16 ecologists and paleo- tinues to be dominated by the production of diversity botanists produced an easily-applied, well-calibrated and turnover metrics and relative abundance curves proxy for fossil leaf mass per area based on the biome- via taxon counting, and by interpretations of tapho- chanical scaling relationship between leaf mass and nomy and depositional environments. Direct quan- petiole dimensions, normalized to leaf (blade) area titative links to neoecological data remain weak but (Royer et al., 2007; Fig. 2). Specifi cally, petiole width fundamental for testing which current ecological ob- is used because it is much more commonly preserved servations have temporal generality, and how current than full petiole length, and when squared, petiole ecosystems evolved. Adding to the paleoecologist’s width scales to the petiole’s cross-sectional area that diffi culty is a plethora of contending neoecological supports the leaf mass. Thus, all that is needed from theories that are diffi cult or impossible to test with fossil leaves (or leafl ets if compound leaves) is petiole fossils, a prominent example being Hubbell’s (2001) (petiolule) width and estimated leaf area. The calibra- neutral theory of biodiversity. tion was based on angiosperms, but importantly for Quantitative trait ecology is one of the most prom- deep-time fossil applications, preliminary gymno- ising avenues for new breakthroughs in paleoecology sperm data fi t the angiosperm calibration well (Royer because it is built from measurements, usually contin- et al., 2007). uous, of critical functional variables that are strongly Royer et al. (2007) quantifi ed fossil leaf mass per tied to the performance and environmental tolerances area for two well-sampled, taxonomically well under- of organisms (e.g., McGill et al., 2006). Trait values stood (MacGinitie, 1969; Wolfe and Wehr, 1987) Eo- can then be correlated to each other and to variables cene lake fl oras with insect-herbivory data: Republic representing ecological gradients (Wright et al., 2004; (early Eocene, Washington, humid warm temperate) 324 PETER WILF

1000 -2


Leaf mass per area, g m 10 0.00010.001 0.01 0.1 (Petiole width)2 / (leaf area) Figure 2—Scaling between petiole width2 (mm2) and leaf dry mass (g), normalized by leaf area (mm2 and m2, respectively), for 667 species-site pairs of extant woody angiosperms from 65 globally distributed sites, re- drawn from Royer et al. (2007). Note that the vertical axis shows the desired trait variable, leaf mass per area (g m-2), and that the only input needed from fossil leaves is petiole (petiolule for compound leaves) width and leaf (leafl et) area (horizontal axis). Dots represent the species-site pairs, and triangles represent the site means for sites where ten or more species were sampled. The black and gray lines are the linear regressions for species and sites, respectively (see Royer et al. 2007 for details). Dashed lines represent 95% prediction intervals for the species data.

and Green River (middle Eocene Bonanza site, Utah, on less understood fossil fl oras (for an application to seasonally dry subtropical). From modern observa- past climate change and herbivory, see Currano et al., tions of how leaf mass per area and plant-insect ecol- 2008). The results also indicate a higher likely rate of ogy vary with climate (Coley, 1983; summarized in nutrient recycling, which increases at lower leaf mass Wilf et al., 2001), Royer et al. predicted, and found, per area, among woody angiosperms at Republic than a greater variance of both leaf mass per area and her- at Green River. bivory for the seasonally dry Green River fl ora than This example from paleobotany brings together at Republic, as well as an overall negative correla- both plant trait ecology and plant-insect ecology into tion of herbivory and leaf mass per area. These results a straightforward predictive framework for paleoecol- showed the Green River sample to contain a mixture ogy. More importantly, it demonstrates the potential of lake-margin species (of Platanaceae and Salica- for trait ecology to allow direct, productive compari- ceae) with high resource availability, presumed fast son of fossil and extant communities in terms of niche growth strategy, and high palatability (low leaf mass ecology, climate gradients, plant-animal interactions, per area), versus the presumably drought-tolerant, and nutrient recycling (see also Royer, 2008). slow-growing, and unpalatable species occupying the rest of the landscape (high leaf mass per area). This study quantitatively confi rmed a previous character- PALEOCLIMATE FROM LEAF ization of the variance within Green River plant and FOSSILS: WHICH WAY FORWARD? plant-insect community ecology based on traditional, qualitative interpretation of fossil plant growth strat- I am fairly certain that “paleoclimate estimates” egy and herbivory in modern analog environments would be the top response to any poll of geologists (Wilf et al., 2001). Thus, the approach is ready to use asked the question: “what good are fossil leaves?” FOSSIL ANGIOSPERM LEAVES 325

Indeed, quantitative paleoclimate estimates are in all signals in CLAMP are statistical byproducts of the likelihood paleobotany’s most frequent export to other modern correlation of temperature and temperature fi elds. “How warm was it there?” and “how fast and seasonality (Jordan, 1996) and that leaf sizes are sig- how much did it cool here?” are core questions for un- nifi cantly biased towards small leaves in the CLAMP derstanding history, and fossil plants have long database, particularly affecting rainfall estimates by been major contributors to paleoclimate reconstruc- infl ating them (Wilf et al., 1998, 1999). I note here that tions, fossil biome interpretations, intercontinental mi- the leaf-size bias in the calibration data is also very gration hypotheses, climate simulation constraints, etc. likely to distort paleoaltitude estimates using CLAMP, The leaf data have come in two principal forms: analy- which use fossil leaves to estimate differences in mean sis of the climatic tolerances of nearest living relatives annual enthalpy between coeval coastal reference and (e.g., Mosbrugger and Utescher, 1997), which relies inland target fl oras (e.g., Wolfe et al., 1997, 1998). on correct taxonomic placement of fossils, and analy- This is because enthalpy (which has a specifi c humid- sis of leaf size and shape variables (i.e., leaf physiog- ity component that correlates with leaf size) will be nomy; starting with Bailey and Sinnott, 1915), which overestimated more for the coastal reference fl ora, due does not, and is therefore a common use of leaf mor- to its larger leaves, than for the targeted inland fl ora, photypes. Many paleotemperature trends quantifi ed infl ating the enthalpy difference and thus the paleoel- from fossil leaf physiognomy, especially leaf-margin evation estimate for the inland site. analysis (the robust linear correlation of mean annual Seeking an alternative to CLAMP, I began a new temperature with the percentage of woody dicot spe- project to improve multivariate leaf physiognomy and cies in a mesic fl ora that have untoothed leaf margins: to recover the additional climate signal that Wolfe Bailey and Sinnott, 1915; Wolfe, 1979), have been fi rst identifi ed in the CLAMP project. Two signifi cant validated by marine isotopic and other independent problems to overcome were fi rst, that CLAMP relied data for important intervals of global warming and on discrete character states rather than continuous cooling near the Cretaceous-Paleogene, Paleocene- measurements, and second, that after observing many Eocene, and Eocene-Oligocene boundaries (Wolfe and colleagues scoring leaves, it was clear that different Poore, 1982; Wolfe, 1992; Wing et al., 2000, 2005; investigators were not likely to score the same leaf Wilf et al. 2003b). This general topic, its rich history, the same way using Wolfe’s instructions (Wilf, 1997). and many associated issues have been reviewed ex- Rapid, computerized measurement of leaf outlines on haustively elsewhere, most recently and effectively by ordinary desktop computers had just (ca. 2000) be- Greenwood (2007), and I concentrate here on a few come possible and seemed to be an excellent proce- directions I consider most productive. dure for solving both problems. The fi rst is the future of multivariate leaf physiog- Working with two undergraduates (Huff et al., nomy. In a major breakthrough, Wolfe (1993, 1995) 2003), I developed a set of computer-assisted, highly showed the signifi cant contribution to climate signal in reproducible, continuous measurements including var- extant fl oras that comes not only from the among-spe- ious combinations and ratios of area, perimeter, tooth cies mean of leaf margin state (toothed or untoothed, count, and tooth area measurements, and showed that i.e., leaf-margin analysis) at a site but also from 28 these varied in the predicted way between one wet other shape characters, and he developed a method tropical site (Panama) and two temperate (Pennsylva- for using this signal in paleoclimate estimates known nia) extant sites: the tropical site’s leaves (or leafl ets as CLAMP (climate leaf analysis multivariate pro- when compound) were, by among-species mean, more gram). In my fi rst paper (Wilf, 1997), I found that the circular and less dissected, with smaller and fewer additional characters, unfortunately, did not improve teeth. Due to the central role of digital leaf images, we temperature estimates in extant fl oras over leaf-mar- coined the method “digital leaf physiognomy” (Huff gin analysis, despite requiring many times more work. et al., 2003). A major follow-up paper using leaf col- This straightforward conclusion has been repeatedly lections by E.A. Kowalski and D.L. Dilcher examined validated (see Greenwood, 2007 for review), and no these and 14 additional sites from the Eastern USA, defense of CLAMP has emerged that has refuted it. fi nding signifi cant linear correlations between most Other work has shown that temperature seasonality of the digital leaf physiognomy characters and mean 326 PETER WILF

annual temperature (Royer et al. 2005). Importantly, climate estimates for fossil fl oras with no modern re- several correlations passed digital fragmentation tests gional analogs. The Little et al. initial results are also and showed promise for use in fossil fl oras. Another validated by the work mentioned above that showed benefi t of the method is that it appears to dampen an phylogenetic signal in leaf-shape data mapped on important bias, whereby species near bodies of water (Doyle, 2007; Green and Little, 2007). analogous to depocenters are more often toothed than Leaf physiognomy science is entering a new phase those in adjacent forest from the same climate (Burn- wherein high reproducibility of measurements and ham et al., 2001). However, additions of a few fl oras improved phylogenetic context both allow signifi cant from outside the Eastern USA altered the correlations improvements in characterizing the taxonomy, paleo- somewhat (Cariglino, 2007), and it is clear that a great climate, and ecology of fossil fl oras. This is a far more deal of additional calibration data from more regions productive and interesting route forward than the con- will be needed before major applications can be made tinuing proliferation of papers on “equation-testing” to fossil fl oras (D.L. Royer et al., work in progress). and revisitation of old arguments about CLAMP (for Moreover, the amount of labor needed to measure review see Greenwood, 2007). A broad approach is the new variables from imperfectly preserved fossil also more likely to keep leaf physiognomy involved in leaves exceeds CLAMP (Cariglino, 2007), and thus relevant and diverse science while geochemical paleo- future acceptance of the method depends on whether climate proxies for the terrestrial realm advance quick- the labor is justifi ed with signifi cantly improved cli- ly (Weijers et al., 2007; Snell et al. 2007; Schouten et mate estimates. al., 2008). The digital leaf physiognomy project has had many synergistic outcomes, currently in very early stages, that are at least as interesting for future investi- CALIBRATING INSECT-DAMAGE RICHNESS gations as the initial climatic correlations and applica- FOR PALEOECOLOGY AND NEOECOLOGY tions because they provide new, explicit, and quantita- tive links between paleoecology and neoecology. The Clearly one of the most productive contributions wealth of continuously measured, novel leaf-shape of fossil leaves is their uniquely diverse and abundant data that is emerging has high statistical signifi cance preservation of insect-feeding damage. No other type and ecological importance (Royer et al., 2008). The data can be placed on phylogenetic trees to measure of fossil preserves such rich, direct evidence of two historical effects, and they can also be correlated to levels of the food web in a single specimen, often com- other vegetational traits (Royer et al., 2005, and see bined with the full stratigraphic context, high sample above). size, and other contextual data offered by fossil leaf Preliminary work (Little et al., 2008) shows that collections such as paleoclimate data, leaf trait data nearly all of the leaf traits used in leaf-margin analy- (see above), and host-plant abundance and phylogeny. sis and digital leaf physiognomy, and presumably in Thus, fossil insect damage offers a tremendous oppor- CLAMP as well (including tooth traits), have slight tunity to study and time the response of plant-insect to strong, signifi cant historical (phylogenetic) signal. feeding associations to major environmental stresses Thus, Little et al. are demonstrating that the core as- and climate change (Labandeira et al., 2002a; Wilf et sumptions underlying leaf-physiognomic methods al., 2006; Currano et al., 2008). This topic, with ob- need overhaul: that leaf shape is primarily controlled vious relevance to today’s changing ecosystems, has by climate, that phylogeny is insignifi cant, and there- been extensively reviewed recently (Labandeira, 2005; fore that the species at a site can be treated as statis- Wilf, 2008), and the example of Eocene herbivory in tically independent entities. Continued investigation the context of leaf mass per area and climate (Royer et along these lines is likely to help explain the much-de- al., 2007) is given above. Here, I briefl y discuss some bated “regional differences” in leaf-climate responses important aspects of the bedrock data source, insect (e.g., Greenwood et al., 2004; Aizen and Ezcurra, damage types (DTs) that occur on fossil leaves (a few 2008) and to allow phylogenetic adjustments of paleo- examples shown in Fig. 1), what is needed to under- FOSSIL ANGIOSPERM LEAVES 327 stand them better, and their potential as a strong link over, calibration should make possible an alternative to neoecology. measure of past diversity through time and Ecologists have living herbivores available for enable this conspicuous data source to be used for eco- counting, and they have not needed a system for quan- logical studies in living forests. For example, insect tifying richness of insect damage (but see below). In- feeding richness can be monitored for its response to stead, insect damage is usually quantifi ed as a rate: current climate change, a natural and relevant exten- amount of leaf removed per unit time. Recog- sion of results from the deep-time fossil record, pro- nition of insect damage types originated to quantify jected to neoecology. the full richness of insect feeding on Paleocene and Eocene fl oras from Wyoming (Wilf and Labandeira, 1999). The fossil DTs have since been expanded, il- ACKNOWLEDGMENTS lustrated, and described using several fossil fl oras (e.g., Labandeira, 2002; Labandeira et al., 2002b). The I especially thank these current and former mem- working catalog of fossil DTs, now numbering more bers of my lab group for their many stimulating con- than 150, is maintained in an open-access, fully illus- tributions: Stefan Little, Dana Royer, Ellen Currano, trated, continuously updated, printable Internet guide Bárbara Cariglino, Ari Iglesias, Daniel Danehy, and (Labandeira et al., 2007). David Janesko. Many colleagues, whose work is cited, The DTs parallel leaf morphotypes in many ways have strongly infl uenced my thinking. Richard Bam- in terms of taxonomic issues. They are informal, op- bach, Rebecca Horwitt, Dana Royer, and two anony- erational units that represent the insect-feeding rich- mous reviewers provided helpful comments. For recent ness on a fl ora. Although some may fi nd the inherent fi nancial support of some of the research discussed concept of “morphotypes on morphotypes” unsettling, here, I thank the National Science Foundation (grant this allows characterization of the full spectrum of DEB-0345750), the David and Lucile Packard Foun- damage richness on all the host plants in a fl ora. As for dation, the Petroleum Research Fund (grant 40546- leaf morphotypes, the eventual incorporation of DTs AC8), the Ryan Family Foundation, and the ARC-NZ into formal taxonomic entities is essential, especially Research Network for Vegetation Function, supported for those that can be linked to a well-defi ned culprit by the Australian Research Council (to Mark Westoby, (Wilf et al., 2000; Sarzetti et al., 2008), but the discov- for the meetings leading to Royer et al. 2007). ery rate is much higher than the description rate. A ma- jor difference from leaf morphotypes, which usually correspond to inferred species entities, is that the cor- REFERENCES respondence of DTs to real herbivore species is highly variable, and for the most part unquantifi ed. Whereas ACKERLY, D. D. and P. B. REICH. 1999. Conver- the mine, gall, and other “specialized” damage types gence and correlations among leaf size and func- on a particular plant host typically each represent one tion in plants: a comparative test using inde- or only a few herbivore species (Johnson and Lyon, pendent contrasts. American Journal of , 1991; Russo, 2007), generalized feeding, such as most 86:1272-1281. external foliage feeding, is much harder to pinpoint. A AIZEN, M. A. and C. EZCURRA. 2008. Do leaf mar- few herbivore species at a site may make many kinds gins of the temperate forest fl ora of southern South of damage on many plant species (Basset and Höft, America refl ect a warmer past? Global Ecology 1994). and , 17:164-174. Therefore, a major effort is needed in living for- ALROY, J. 1998. Cope’s Rule and the dynamics of ests to calibrate the insect damage types to the number body mass evolution in North American fossil of herbivore species that make them. This work, un- mammals. Science, 280:731-734. derway in a pilot project, will lead to more informed ANGIOSPERM PHYLOGENY GROUP. 2003. An interpretations of fossil damage occurrences and will update of the Angiosperm Phylogeny Group clas- also produce important natural history data. More- sifi cation for the orders and families of fl owering 328 PETER WILF

plants: APG II. Botanical Journal of the Linnean COLEY, P. D., and J. A. BARONE. 1996. Herbivory Society, 141:399-436. and plant defenses in tropical forests. Annual Re- ASH, A. W., B. ELLIS, L. J. HICKEY, K. R. JOHN- view of Ecology and Systematics, 27:305-335. SON, P. WILF, and S. L. WING. 1999. Manual of CRANE, P. R. and R. A. STOCKEY. 1985. Growth Leaf Architecture: Morphological Description and and reproductive biology of Joffrea speirsii gen. et Categorization of Dicotyledonous and Net-Veined sp. nov., a Cercidiphyllum-like plant from the Late Monocotyledonous Angiosperms. Smithsonian In- Paleocene of Alberta, Canada. Canadian Journal of stitution, Washington, D.C., www.peabody.yale. Botany, 63:340-364. edu/collections/pb/MLA.pdf CRANE, P. R., S. R. MANCHESTER, and D. L. BAILEY, I. W. and E. W. SINNOTT. 1915. A botani- DILCHER. 1990. A preliminary survey of fossil cal index of Cretaceous and Tertiary . Sci- leaves and well-preserved reproductive structures ence, 41:831-834. from the Sentinel Butte Formation (Paleocene) BASSET, Y. and R. HÖFT. 1994. Can apparent leaf near Almont, North Dakota. Fieldiana , damage in tropical trees be predicted by herbivore 20:1-63. load or host-related variables? A case study in Pap- CRANE, P. R., S. R. MANCHESTER, and D. L. ua New Guinea. Selbyana, 15:3-13. DILCHER. 1991. Reproductive and vegetative BERRY, E. W. 1925. A Miocene fl ora from Patago- structure of Nordenskioldia (Trochodendraceae), nia. Johns Hopkins University Studies in Geology, a vesselless dicotyledon from the Early Tertiary 6:183-251. of the Northern Hemisphere. American Journal of BERRY, E. W. 1937. A Paleocene fl ora from Patago- Botany, 78:1311-1334. nia. Johns Hopkins University Studies in Geology, CURRANO, E. D., P. WILF, S. L. WING, C. C. 12:33-50. LABANDEIRA, E. C. LOVELOCK, and D. L. BERRY, E. W. 1938. Tertiary fl ora from the Río Pi- ROYER. 2008. Sharply increased insect herbivory chileufú, Argentina. Geological Society of America during the Paleocene-Eocene thermal maximum. Special Paper, 12:1-149. Proceedings of the National Academy of Sciences BOUCHER, L. D., S. R. MANCHESTER, and W. S. USA, 105:1960-1964. JUDD. 2003. An extinct genus of Salicaceae based DANEHY, D. R., P. WILF, and S. A. LITTLE. 2007. on twigs with attached fl owers, fruits, and foliage Early Eocene macrofl ora from the Red Hot Truck from the Eocene of Utah Stop locality (Meridian, Mississippi, USA). Palae- and Colorado, USA. American Journal of Botany, ontologia Electronica 10:article 10.3.17A, palaeo- 90:1389-1399. electronica.org/2007_3/132/index.html. BURNHAM, R. J., N. C. A. PITMAN, K. R. JOHN- DILCHER, D. L. 1974. Approaches to the identifi ca- SON, and P. WILF. 2001. Habitat-related error in tion of angiosperm leaf remains. Botanical Review, estimating temperatures from leaf margins in a hu- 40:1-157. mid tropical forest. American Journal of Botany, DILCHER, D. L. and T. A. LOTT. 2005. A middle 88:1096-1102. Eocene fossil plant assemblage (Powers Clay Pit) CARIGLINO, B. 2007. Paleoclimatic analysis of the from western Tennessee. Florida Museum of Natu- Eocene Laguna del Hunco, Green River, and Re- ral History Bulletin, 45:1-43. public fl oras using digital leaf physiognomy. M.S. DIMICHELE, W. A. and R. A. GASTALDO. 2008. thesis, Pennsylvania State University, 104 p. Plant paleoecology in deep time. Annals of the CARR, D. J., S. G. M. CARR, and J. R. LENZ. 1986. Missouri Botanical Garden, 95:144-198. Leaf venation in Eucalyptus and other genera of DOYLE, J. A. 2007. Systematic value and evolution Myrtaceae: implications for systems of classifi - of leaf architecture across the angiosperms in light cation of venation. Australian Journal of Botany, of molecular phylogenetic analyses. Courier Forsc- 34:53-62. hungsinstitut Senckenberg, 258:37. COLEY, P. D. 1983. Herbivory and defensive charac- DOYLE, J. A. and P. K. ENDRESS. 2000. Morpho- teristics of species in a lowland tropical forest. logical phylogenetic analysis of basal angiosperms: Ecological Monographs, 53:209-233. comparison and combination with molecular data. FOSSIL ANGIOSPERM LEAVES 329

International Journal of Plant Sciences, 161:S121- testing the utility of Compendium Index Categories S153. for taxonomic identifi cation and phylogenetic anal- EKLUND, H., J. A. DOYLE, and P. S. HERENDEEN. ysis of modern cleared leaves. Botanical Society of 2004. Morphological phylogenetic analysis of liv- America Annual Meeting, Chicago, abstract 2165. ing and fossil Chloranthaceae. International Jour- GREENWOOD, D. R. 2007. Fossil angiosperm leaves nal of Plant Sciences 165:107-151. and climate: from Wolfe and Dilcher to Burnham ELLIS, B., D. DALY, L. J. HICKEY, K. R. JOHN- and Wilf. Courier Forschungsinstitut Senckenberg, SON, J. MITCHELL, P. WILF, and S. L. WING. 258:95-108. 2009. Manual of Leaf Architecture. Cornell Uni- GREENWOOD, D. R., P. WILF, S. L. WING, and D. versity Press, Ithaca, in press. C. CHRISTOPHEL. 2004. Paleotemperature esti- FRIEDRICH, W. L. and F. SCHAARSCHMIDT. mation using leaf-margin analysis: is Australia dif- 1979. Epi fl uorescence of fossil plants. Zeiss-infor- ferent? Palaios, 19:129-142. mation 24:16-18. HICKEY, L. J. 1973. Classifi cation of the architec- FULLER, D. Q. and L. J. HICKEY. 2005. Systematics ture of dicotyledonous leaves. American Journal of and leaf architecture of the Gunneraceae. Botanical Botany, 60:17-33. Review, 71:295-353. HICKEY, L. J. 1977. Stratigraphy and paleobotany GANDOLFO, M. A. and E. J. ROMERO. 1992. Leaf of the (Early Tertiary) of morphology and a key to species of Nothofagus Bl. western North Dakota. GSA Memoir, 150:1-183. Bulletin of the Torrey Botanical Club, 119:152- HICKEY, L. J. and D. W. TAYLOR. 1991. The leaf 166. architecture of Ticodendron and the application GANDOLFO, M. A., C. C. GONZÁLEZ, M. C. ZA- of foliar characters in discerning its relationships. MALOA, N. R. CÚNEO, and P. WILF. 2006. Eu- Annals of the Missouri Botanical Garden, 78:105- calyptus (Myrtaceae) from the early 130. Eocene of Patagonia, Argentina. Botanical Society HICKEY, L. J. and J. A. WOLFE. 1975. The bases of America Annual Meeting, Chico, CA, abstract of angiosperm phylogeny: vegetative morphology. 473. Annals of the Missouri Botanical Garden, 62:538- GANDOLFO, M. A., M. C. ZAMALOA, C. C. 589. GONZÁLEZ, N. R. CÚNEO, P. WILF, and K. R. HILL, R. S. 1982. The Eocene megafossil fl ora of JOHNSON. 2007. Bixaceae: a tropical component Nerriga, New South Wales, Australia. Palaeonto- of the early Eocene Laguna del Hunco paleofl ora, graphica Abteilung B: Palaeophytologie, 181:44- Chubut, Patagonia, Argentina. Geological Society 77. of America Abstracts with Programs, 39:585. HUBBELL, S. P. 2001. The Unifi ed Neutral Theory of GENTRY, A. H. 1993. A fi eld guide to the families Biodiversity and Biogeography. Princeton Univer- and genera of woody plants of northwest South sity Press, Princeton, 396 p. America (Colombia, Ecuador, Peru), with supple- HUFF, P. M., P. WILF, and E. J. AZUMAH. 2003. mentary notes on herbaceous taxa. Conservation Digital future for paleoclimate estimation from International, Washington, DC. fossil leaves? Preliminary results. Palaios 18:266- GONZÁLEZ, C. C., M. A. GANDOLFO, and N. 274. R. CÚNEO. 2004. Leaf architecture and epider- IGLESIAS, A., P. WILF, K. R. JOHNSON, A. B. ZA- mal characters of the Argentinean species of Pro- MUNER, N. R. CÚNEO, S. D. MATHEOS, and teaceae. International Journal of Plant Sciences, B. S. SINGER. 2007. A Paleocene lowland mac- 165:521-526. rofl ora from Patagonia reveals signifi cantly greater GONZÁLEZ, C. C., M. A. GANDOLFO, N. R. CÚ- richness than North American analogs. Geology, NEO, P. WILF, and K. R. JOHNSON. 2007. Revi- 35:947-950. sion of the Proteaceae record from Pa- IGLESIAS, A., P. WILF, M. A. GANDOLFO, S. A. tagonia, Argentina. Botanical Review, 73:235-266. LITTLE, K. R. JOHNSON, A. ZAMUNER, C. C. GREEN, W. A. and S. A. LITTLE. 2007. Leaf char- LABANDEIRA, and N. R. CÚNEO. 2008a. Paleo- acters across families and orders of angiosperms: cene Patagonian fl oras: in situ cuticles complement 330 PETER WILF

architectural data from leaf compressions of Podo- logical Society of America Special Paper 361:297- carpaceae, , and Nothofagaceae. Botani- 327. cal Society of America Annual Meeting, Vancou- LABANDEIRA, C. C., P. WILF, K. R. JOHNSON, ver, abstract 449. and F. MARSH. 2007. Guide to Insect (and oth- IGLESIAS, A., S. A. LITTLE, P. WILF, and M. A. er) Damage Types on Compressed Plant Fossils. GANDOLFO. 2008b. An early Paleocene fl ower Version 3.0. Smithsonian Institution, Washington, related to Resedaceae (Brassicales) bearing in situ D.C., .si.edu/insects/index.html. pollen and from Patagonia, Argentina. Inter- LITTLE, S. A., S. KEMBEL, P. WILF, and D. L. national Organization of Paleobotany, VIIIth Qua- ROYER. 2008. Phylogenetic signal in leaf traits drennial Conference, Bonn, Germany, Abstracts. and its infl uence on leaf-climate correlations. Bo- JOHNSON, K. R., D. J. NICHOLS, M. ATTREP, Jr., tanical Society of America Annual Meeting, Van- and C. J. ORTH. 1989. High-resolution leaf-fossil couver, abstract 626. record spanning the Cretaceous-Tertiary boundary. LIU, Y. 1996. Foliar architecture of Betulaceae and a Nature, 340:708-711. revision of Chinese betulaceous megafossils. Pa- JOHNSON, W. T. and H. H. LYON. 1991. Insects that laeontographica Abteilung B: Palaeophytologie, Feed on Trees and , 2 ed. Cornell University 239:23-57. Press, Ithaca, 560 p. MACGINITIE, H. D. 1969. The Eocene Green River JORDAN, G. J. 1996. Eocene continental climates fl ora of northwestern Colorado and northeastern and latitudinal temperature gradients: Comment. Utah. University of California Publications in Geo- Geology, 24:1054. logical Sciences, 83:1-140. KEATING, R. C. and V. RANDRIANASOLO. 1988. MANCHESTER, S. R. 1989. Attached reproductive The contribution of leaf architecture and and vegetative remains of the extinct American- anatomy to classifi cation of the Rhizophoraceae European genus Cedrelospermum (Ulmaceae) from and Anisophylleaceae. Annals of the Missouri Bo- the early Tertiary of Utah and Colorado. American tanical Garden, 75:1343-1368. Journal of Botany, 76:256-276. KELLER, R. 2004. Identifi cation of Tropical Woody MANCHESTER, S. R. 2001. Update on the megafos- Plants in the Absence of : a Field Guide, 2 sil fl ora of Florissant, Colorado. Proceedings of ed. Birkhäuser Verlag, Basel, 294 p. the Denver Museum of Nature & Science, Series KERP, H. and M. KRINGS. 1999. Light microscopy 4 1:137-162. of cuticles. p. 52-56. In T. P. Jones and N. P. Rowe, MANCHESTER, S. R., D. L. DILCHER, and W. D. eds., Fossil plants and : modern techniques. TIDWELL. 1986. Interconnected reproductive and Geological Society, London. vegetative remains of Populus (Salicaceae) from LABANDEIRA, C. C. 2002. Paleobiology of middle the middle Eocene Green River Formation, north- Eocene plant-insect associations from the Pacifi c eastern Utah. American Journal of Botany, 73:156- Northwest: a preliminary report. Rocky Mountain 160. Geology, 37:31-59. MANCHESTER, S. R., D. L. DILCHER, and S. L. LABANDEIRA, C. C. 2005. The fossil record of in- WING. 1998. Attached leaves and fruits of myrta- sect extinction: new approaches and future direc- ceous affi nity from the middle Eocene of Colorado. tions. American Entomologist, 51:10-25. Review of Palaeobotany and , 102:153- LABANDEIRA, C. C., K. R. JOHNSON, and P. 163. WILF. 2002a. Impact of the terminal Cretaceous MANCHESTER, S. R., P. R. CRANE, and L. B. GO- event on plant-insect associations. Proceedings of LOVNEVA. 1999. An extinct genus with affi ni- the National Academy of Sciences USA, 99:2061- ties to extant Davidia and Camptotheca (Cornales) 2066. from the Paleocene of North America and east- LABANDEIRA, C. C., K. R. JOHNSON, and P. ern Asia. International Journal of Plant Sciences, LANG. 2002b. Preliminary assessment of insect 160:188-207. herbivory across the Cretaceous-Tertiary bound- MANCHESTER, S. R. and L. J. HICKEY. 2007. ary: major extinction and minimum rebound. Geo- Reproductive and vegetative organs of Browniea FOSSIL ANGIOSPERM LEAVES 331

gen. n. (Nyssaceae) from the Paleocene of North ROYER, D. L., L. SACK, P. WILF, C. H. LUSK, G. America. International Journal of Plant Sciences, J. JORDAN, Ü. NIINEMETS, I. J. WRIGHT, M. 168:229-249. WESTOBY, B. CARIGLINO, P. D. COLEY, A. D. MANOS, P. S., P. S. SOLTIS, D. E. SOLTIS, S. R. CUTTER, K. R. JOHNSON, C. C. LABANDEI- MANCHESTER, S. H. OH, C. D. BELL, D. L. RA, A. T. MOLES, M. B. PALMER, and F. VAL- DILCHER, and D. E. STONE. 2007. Phylogeny of LADARES. 2007. Fossil leaf economics quantifi ed: extant and fossil Juglandaceae inferred from the in- calibration, Eocene case study, and implications. tegration of molecular and morphological data sets. Paleobiology, 33:574-589. Systematic Biology, 56:412-430. ROYER, D. L., J. C. MCELWAIN, J. M. ADAMS, and MARTÍNEZ-MILLÁN, M. and S. R. S. CEVALLOS- P. WILF. 2008. Sensitivity of leaf size and shape to FERRIZ. 2005. Arquitectura foliar de Anacardia- climate within Acer rubrum and Quercus kelloggii. ceae. Revista Mexicana de Biodiversidad, 76:137- New Phytologist, 179: 808-817. 190. RUSSO, R. 2007. Field Guide to Plant Galls of Cali- MCGILL, B. J., B. J. ENQUIST, E. WEIHER, and M. fornia and other Western States. University of Cali- WESTOBY. 2006. Rebuilding community ecology fornia Press, Berkeley, 400 p. from functional traits. Trends in Ecology & Evolu- SARZETTI, L., C. C. LABANDEIRA, and J. GE- tion, 21:178-185. NISE. 2008. A leafcutter bee from the MOSBRUGGER, V. and T. UTESCHER. 1997. The middle Eocene of Patagonia, Argentina, and a re- coexistence approach - a method for quantitative view of megachilid (Hymenoptera) ichnology. Pal- reconstructions of Tertiary terrestrial palaeoclimate aeontology 51:933-941. SCHAARSCHMIDT, F. 1982. Präparation und Unter- data using plant fossils. , Palaeo- suchung der Eozänen Pfl anzenfossilen von Messel climatology, Palaeoecology, 134:61-86. bei Darmstadt. Courier Forschungsinstitut Senck- PREMOLI, A. C. 1996. Leaf architecture of South enberg, 56:59-77. American Nothofagus (Nothofagaceae) using tradi- SCHARASCHKIN, T. and J. A. DOYLE. 2005. Phy- tional and new methods in morphometrics. Botani- logeny and historical biogeography of Anaxagorea cal Journal of the Linnean Society, 121:25-40. (Annonaceae) using morphology and non-cod- REICH, P. B., C. UHL, M. B. WALTERS, and D. S. ing sequence data. Systematic Botany, ELLSWORTH. 1991. Leaf lifespan as a determi- 30:712-735. nant of leaf structure and function among 23 Ama- SCHOUTEN, S., J. ELDRETT, D. R. GREENWOOD, zonian tree species. Oecologia, 86:16-24. I. HARDING, M. BAAS, and J. S. S. DAMSTÉ. REICH, P. B., M. B. WALTERS, and D. S. ELLS- 2008. Onset of long-term cooling of Greenland WORTH. 1997. From tropics to tundra: Global near the Eocene-Oligocene boundary as revealed convergence in plant functioning. Proceedings of by branched tetraether lipids. Geology, 36:147- the National Academy of Sciences USA, 94:13730- 150. 13734. SECORD, R., P. D. GINGERICH, M. E. SMITH, W. REICH, P. B., D. S. ELLSWORTH, M. B. WALTERS, C. CLYDE, P. WILF, and B. S. SINGER. 2006. J. M. VOSE, C. GRESHAM, J. C. VOLIN, and Geochronology and mammalian W. D. BOWMAN. 1999. Generality of leaf trait of middle and upper Paleocene continental strata, relationships: a test across six biomes. Ecology, Bighorn Basin, Wyoming. American Journal of 80:1955-1969. Science, 306:211-245. ROYER, D. L. 2008. Nutrient turnover rates in ancient SNELL, K. E., J. M. EILER, D. DETTMAN, and P. L. terrestrial ecosystems. Palaios, 23:421-423. KOCH. 2007. Continental temperatures from the ROYER, D. L., P. WILF, D. A. JANESKO, E. A. Paleocene-Eocene boundary in the Big Horn Basin, KOWALSKI, and D. L. DILCHER. 2005. Cor- WY from carbonate clumped isotope thermometry. relations of climate and plant ecology to leaf size Geochimica et Cosmochimica Acta, 71:A950. and shape: potential proxies for the fossil record. SWENSON, N. G. and B. J. ENQUIST. 2007. Ecolog- American Journal of Botany, 92:1141-1151. ical and evolutionary determinants of a key plant 332 PETER WILF

functional trait: wood density and its community- WILF, P., K. R. JOHNSON, and B. T. HUBER. wide variation across latitude and elevation. Amer- 2003b. Correlated terrestrial and marine evidence ican Journal of Botany, 94:451-459. for global climate changes before mass extinction TODZIA, C. A. and R. C. KEATING. 1991. Leaf at the Cretaceous-Paleogene boundary. Proceed- architecture of the Chloranthaceae. Annals of the ings of the National Academy of Sciences USA, Missouri Botanical Garden, 78:476-496. 100:599-604. WEIJERS, J. W. H., S. SCHOUTEN, A. SLUIJS, H. WILF, P., K. R. JOHNSON, N. R. CÚNEO, M. E. BRINKHUIS, and J. S. S. DAMSTÉ. 2007. Warm SMITH, B. S. SINGER, and M. A. GANDOLFO. Arctic continents during the Palaeocene-Eocene 2005a. Eocene plant diversity at Laguna del Hunco thermal maximum. Earth and Planetary Science and Río Pichileufú, Patagonia, Argentina. Ameri- Letters, 261:230-238. can Naturalist, 165:634-650. WILF, P. 1997. When are leaves good thermometers? WILF, P., C. C. LABANDEIRA, K. R. JOHNSON, A new case for Leaf Margin Analysis. Paleobiol- and N. R. CÚNEO. 2005b. Richness of plant-in- ogy, 23:373-390. sect associations in Eocene Patagonia: a legacy for WILF, P. 2000. Late Paleocene-early Eocene climate South American biodiversity. Proceedings of the changes in southwestern Wyoming: paleobotanical National Academy of Sciences USA, 102:8944- analysis. Geological Society of America Bulletin, 8948. 112:292-307. WILF, P., C. C. LABANDEIRA, K. R. JOHNSON, WILF, P. 2008. Insect-damaged fossil leaves record and B. ELLIS. 2006. Decoupled plant and insect food web response to ancient climate change and diversity after the end-Cretaceous extinction. Sci- extinction. New Phytologist, 178:486-502. ence, 313:1112-1115. WILF, P. and C. C. LABANDEIRA. 1999. Response WILF, P., M. A. GANDOLFO, K. R. JOHNSON, and of plant-insect associations to Paleocene-Eocene N. R. CÚNEO. 2007. Biogeographic signifi cance warming. Science, 284:2153-2156. of the Laguna del Hunco fl ora, early Eocene of Pa- WILF, P., S. L. WING, D. R. GREENWOOD, and C. tagonia, Argentina. Geological Society of America L. GREENWOOD. 1998. Using fossil leaves as Abstracts with Programs, 39:585. paleoprecipitation indicators: an Eocene example. WILF, P., S. A. LITTLE, A. IGLESIAS, M. C. ZA- Geology, 26:203-206. MALOA, M. A. GANDOLFO, K. R. JOHNSON, WILF, P., S. L. WING, D. R. GREENWOOD, and C. and N. R. CÚNEO. 2008. Discovery of Papuace- L. GREENWOOD. 1999. Using fossil leaves as drus (Cupressaceae, Libocedrinae) in Eocene Pa- paleoprecipitation indicators: An Eocene example: tagonia clarifi es the Southern Rainforest enigma. Reply. Geology, 27:92. Botanical Society of America Annual Meeting, WILF, P., C. C. LABANDEIRA, W. J. KRESS, C. L. Vancouver, abstract 391. STAINES, D. M. WINDSOR, A. L. ALLEN, and WING, S. L. and L. J. HICKEY. 1984. The Platycarya K. R. JOHNSON. 2000. Timing the radiations of perplex and the evolution of the Juglandaceae. leaf beetles: hispines on gingers from latest Creta- American Journal of Botany, 71:388-411. ceous to Recent. Science, 289:291-294. WING, S. L., J. ALROY, and L. J. HICKEY. 1995. WILF, P., C. C. LABANDEIRA, K. R. JOHNSON, P. Plant and mammal diversity in the Paleocene to D. COLEY, and A. D. CUTTER. 2001. Insect her- early Eocene of the Bighorn Basin. Palaeogeogra- bivory, plant defense, and early Cenozoic climate phy, Palaeoclimatology, Palaeoecology, 115:117- change. Proceedings of the National Academy of 155. Sciences USA, 98:6221-6226. WING, S. L., H. BAO, and P. L. KOCH. 2000. An WILF, P., N. R. CÚNEO, K. R. JOHNSON, J. F. early Eocene cool period? Evidence for continental HICKS, S. L. WING, and J. D. OBRADOV- cooling during the warmest part of the Cenozoic. ICH. 2003a. High plant diversity in Eocene South p. 197-237. In B. T. Huber, K. MacLeod, and S. L. America: evidence from Patagonia. Science, Wing, eds., Warm Climates in Earth History. Cam- 300:122-125. bridge University Press, Cambridge. FOSSIL ANGIOSPERM LEAVES 333

WING, S. L., G. J. HARRINGTON, F. A. SMITH, J. altitudes in Nevada during the Miocene. Science, I. BLOCH, D. M. BOYER, and K. H. FREEMAN. 276:1672-1675. 2005. Transient fl oral change and rapid global WOLFE, J. A., C. E. FOREST, and P. MOLNAR. warming at the Paleocene-Eocene boundary. Sci- 1998. Paleobotanical evidence of Eocene and Oli- ence, 310:993-996. gocene paleoaltitudes in midlatitude western North WOLFE, J. A. 1977. Paleogene fl oras from the Gulf America. Geological Society of America Bulletin, of Alaska region. U.S. Geological Survey Profes- 110:664-678. sional Paper, 997:1-108. WRIGHT, I. J., P. B. REICH, J. H. C. CORNELIS- WOLFE, J. A 1979. Temperature parameters of humid SEN, D. S. FALSTER, E. GARNIER, K. HIKO- to mesic forests of Eastern Asia and relation to for- SAKA, B. B. LAMONT, W. LEE, J. OLEKSYN, ests of other regions of the Northern Hemisphere N. OSADA, H. POORTER, R. VILLAR, D. I. and Australasia. U.S. Geological Survey Profes- WARTON, and M. WESTOBY. 2005a. Assessing sional Paper, 1106:1-37. the generality of global leaf trait relationships. New WOLFE, J. A. 1992. Climatic, fl oristic, and vegeta- Phytologist, 166:485-496. tional changes near the Eocene/Oligocene bound- WRIGHT, I. J., P. B. REICH, J. H. C. CORNELIS- ary in North America, p. 421-436. In D. R. Prothero SEN, D. S. FALSTER, P. K. GROOM, K. HIKO- SAKA, W. LEE, C. H. LUSK, Ü. NIINEMETS, and W. A. Berggren, eds., Eocene-Oligocene Cli- J. OLEKSYN, N. OSADA, H. POORTER, D. I. matic and Biotic Evolution. Princeton University WARTON, and M. WESTOBY. 2005b. Modula- Press, Princeton, New Jersey. tion of leaf economic traits and trait relationships WOLFE, J. A. 1993. A method of obtaining climatic by climate. Global Ecology and Biogeography, parameters from leaf assemblages. U.S. Geological 14:411-421. Survey Bulletin, 2040:1-71. WRIGHT, I. J., P. B. REICH, M. WESTOBY, D. D. WOLFE, J. A. 1995. Paleoclimatic estimates from ACKERLY, Z. BARUCH, F. BONGERS, J. CAV- Tertiary leaf assemblages. Annual Review of Earth ENDER-BARES, T. CHAPIN, J. H. C. CORNE- and Planetary Sciences, 23:119-142. LISSEN, M. DIEMER, J. FLEXAS, E. GARNIER, WOLFE, J. A. and R. Z. POORE. 1982. Tertiary ma- P. K. GROOM, J. GULIAS, K. HIKOSAKA, B. rine and nonmarine climatic trends, p. 154-158. In B. LAMONT, T. LEE, W. LEE, C. LUSK, J. J. Climate in Earth History. National Academy Press, MIDGLEY, M.-L. NAVAS, Ü. NIINEMETS, J. Washington, DC. OLEKSYN, N. OSADA, H. POORTER, P. POOT, WOLFE, J. A. and G. R. UPCHURCH. 1986. Vegeta- L. PRIOR, V. I. PYANKOV, C. ROUMET, S. C. tion, climatic and fl oral changes at the Cretaceous- THOMAS, M. G. TJOELKER, E. J. VENEK- Tertiary boundary. Nature, 324:148-152. LAAS, and R. VILLAR. 2004. The worldwide leaf WOLFE, J. A. and W. C. WEHR. 1987. Middle Eo- economics spectrum. Nature, 428:821-827. cene dicotyledonous plants from Republic, north- ZAMALOA, M. C., M. A. GANDOLFO, C. C. eastern Washington. U.S. Geological Survey Bul- GONZÁLEZ, E. J. ROMERO, N. R. CÚNEO, and letin, 1597:1-25. P. WILF. 2006. Casuarinaceae from the Eocene of WOLFE, J. A., H. E. SCHORN, C. E. FOREST, and P. Patagonia, Argentina. International Journal of Plant MOLNAR. 1997. Paleobotanical evidence for high Sciences, 167:1279-1289.