FOSSIL ANGIOSPERM LEAVES: PALEOBOTANY’S DIFFICULT CHILDREN PROVE THEMSELVES
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 (leaf architectural) information but are difﬁ cult to identify because they are not attached to other plant 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, past climate change and biotic response, paleoecology, and plant-animal 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 ecology 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 plants), 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 history, 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 fruits. 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 Cretaceous 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 Evolution to Geobiology: Research Questions Driving Paleontology 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 Patagonia, 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 petiole 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; TAXONOMY 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 seeds. 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 Paleocene 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 fossils. 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, geochronology, 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 cuticles 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 (Berry, 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 life 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 vertebrates, 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 pollen 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 plant ecology 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
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 Earth 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 trees 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 arthropod 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 tissue 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. 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