A Case Study from the Late Oligocene of Ethiopia

Palaeogeography, Palaeoclimatology, Palaeoecology 309 (2011) 242–252

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Inferring ecological disturbance in the fossil record: A case study from the late Oligocene of Ethiopia

Ellen D. Currano a,⁎, Bonnie F. Jacobs b, Aaron D. Pan c, Neil J. Tabor b a Department of Geology and Environmental Earth Science, Miami University, 114 Shideler Hall, Oxford, OH 45056, USA b Roy M. Hufﬁngton Department of Earth Sciences, Southern Methodist University, P.O. Box 750395, Dallas, TX 75275, USA c Fort Worth Museum of Science and History, 1600 Gendy St., Fort Worth, TX 76107, USA article info abstract

Article history: Environmental disturbances profoundly impact the structure, composition, and diversity of modern forest Received 20 December 2010 communities. A review of modern studies demonstrates that important characteristics used to describe fossil Received in revised form 24 May 2011 angiosperm assemblages, including leaf margin type, plant form, plant diversity, insect herbivore diversity Accepted 9 June 2011 and specialization, and variation in herbivory among plant species, differ between early and late successional Available online 15 June 2011 forests. Therefore, sequences of fossil floras that include a mix of early and later successional communities may not be appropriate to study long-term temporal trends or biotic effects of climate, latitude, or other Keywords: Succession variables. Paleobotany We conducted sedimentological, paleobotanical, and insect damage analyses at two contemporaneous late Africa Oligocene (27–28 Ma) leaf localities in the Chilga Basin, northwest Ethiopia, to test the hypothesis that Chilga successional stage explains variation between the assemblages. The Guang River and Bull's Bellow fossil plant Oligocene localities are stratigraphically equivalent and only 1.5 km apart, but they have no plant species in common. – Plant insect interactions Sedimentary structures at Bull's Bellow suggest multiple episodes of deposition and a more disturbed environment than the single, featureless mudstone that composes the Guang River fossil unit. Bull's Bellow has a significantly higher percentage of plant species with toothed margins, lower plant and insect herbivore damage diversity, and less specialized herbivore damage than Guang. Furthermore, the nearest living relatives of many of the Bull's Bellow plant species are associated with early successional forests, whereas the Guang River plants are a mix of early and late successional species. Thus, the physiological and ecological attributes of the Guang flora are consistent with a more mature forest community, and the differences between the two floras emphasize the importance of collecting multiple floras from the same stratigraphic level in order to account for landscape-level ecological processes. More specifically, accurate estimates of diversity and feeding specialization in tropical, angiosperm-rich fossil assemblages are essential to address adequately the origin and persistence of relatively high species diversity in the modern tropics, and diversity differences between regions such as modern tropical Africa and South America. © 2011 Elsevier B.V. All rights reserved.

1. Introduction taxonomic differences among stages of forest recovery emphasize the importance of determining the successional stage (or stages) Disturbances like fires, hurricanes, floods, and volcanic eruptions represented by a fossil leaf assemblage. Complete sequences of forest play an integral role in structuring forest communities and may even succession are rarely preserved in the plant macrofossil record be essential to maintaining that structure (e.g. Connell, 1978; because of its limited temporal and spatial resolution (Behrensmeyer Denslow, 1987; Hubbell et al., 1999). The process of community and Hook, 1992; Burnham et al., 1992). Instead, the macrofloral recovery following a disturbance is called succession (Harper, 1977), record preserves either isolated leaf floras representing a single and forest communities often go through a series of compositional successional stage or time-averaged floras that mix early and later and structural changes following disturbances, recognized as succes- successional stages, although there are exceptions (García Massini sional stages, each with different plant and insect herbivore diversity, et al., 2010). Sampling a mix of early and later successional composition, and life habits. The fundamental structural and communities in a stratigraphic sequence may mask true long-term temporal trends, create spurious trends, or obscure correlations with climate (Cross and Taggart, 1982; Burnham, 1994), latitude, or other variables. Furthermore, extracting the deep–time record of alpha ⁎ Corresponding author. Tel.: +1 513 529 8311. E-mail addresses: [email protected] (E.D. Currano), [email protected] and beta diversity accurately, especially at tropical paleolatitudes, is (B.F. Jacobs), [email protected] (A.D. Pan), [email protected] (N.J. Tabor). critical for identifying drivers of biodiversity change through time

(e.g., Wing and Dimichele, 1995; Burnham, 2008), and is relevant to concentrations, and high rates of photosynthesis and respiration understanding modern differences between regions, for example (Wright et al., 2004), all of which make them highly palatable to insect Africa and South America. Most individual paleobotanical sites sample herbivores (Coley et al., 1985; Wright et al., 2004). Late successional at the community scale, and thus pertain to alpha diversity, which species display a much wider range of life strategies and leaf traits. must be understood in light of successional stage. Some species invest most of their energy in growth and little in anti- Spatial heterogeneity in plant composition and insect herbivory herbivore defenses, making them vulnerable to both generalist and within a forest can be assessed in the paleobotanical record through specialist herbivores. Others are adapted to maximize nutrient lateral sampling (e.g., Burnham et al., 1992; Wing et al., 1993; retention by having a long leaf lifespan, low nutrient concentrations Burnham, 1994; Davies-Vollum and Wing, 1998; DiMichele et al., in the leaves, and low photosynthetic and respiration rates (Wright 2007; Currano, 2009). Several paleobotanical studies have attributed et al., 2004). These species, which are more likely to invest in chemical abrupt taxonomic changes across a landscape or through time to post- defenses, should be less palatable to generalist herbivores and display disturbance succession (e.g., Cross and Taggart, 1982; Taggart and a high percentage of specialized damage. Cross, 1990; Frank and Bend, 2004; Samant and Mohabey, 2009; A variety of studies suggest that plant species with toothed Bashforth et al., 2010; García Massini et al., 2010; Bashforth et al., margins are more abundant in early successional forests than in later 2011). For example, Bashforth et al. (2010, 2011) demonstrated successional forests. In upper montane Costa Rican forests, about 60% succession in Carboniferous macrofossil deposits by linking sedimen- of plant species in early successional forests had toothed margins, tological data to plant taxa. Cross and Taggart's (1982) work on the versus ~50% in late successional and ~30% in primary forests Miocene Succor Creek palynofloras used analogies to nearest living (Kappelle and Leal, 1996). Subsequent studies in Ecuador, Australia, relatives to conclude that progression through distinct post-distur- and North America have demonstrated that plant species with bance successional stages caused abrupt taxonomic shifts. toothed leaves are more common in riparian habitats than distal Here, we focus on non-taxonomic approaches that can be used to floodplain or terra firma sites (Burnham, 1994; Burnham et al., 2001; recognize post-disturbance succession in angiosperm-rich fossil Kowalski and Dilcher, 2003; Greenwood, 2005; Royer et al., 2009). assemblages. We first review the ecological literature on plant and The studies referenced above have proposed three main explanations insect herbivore responses to disturbance in order to determine what for the abundance of toothed species in riparian and disturbed (and whether) structural and functional attributes characterize early habitats: increased availability of water (Bailey and Sinnott, 1915; vs. late successional angiosperm-dominated tropical forests (Table 1). Wolfe, 1993; Kowalski and Dilcher, 2003; Royer et al., 2009), higher We then apply these characters to the Oligocene fossil record of the diversity of toothed lianas (Burnham et al., 2001), and selection Chilga Basin, northwest Ethiopia. We focus on two stratigraphically against untoothed species in disturbed environments (Kappelle and equivalent paleofloras that are 1.5 km apart but have no plant species Leal, 1996; Burnham et al., 2001). Higher rates of transpiration, in common. We hypothesize that sedimentological, taxonomic, and respiration, and photosynthesis have been measured in toothed paleoecological differences between the two paleofloras will be margins than in untoothed margins (Wolfe, 1993; Royer and Wilf, consistent with communities in different, earlier and later, forest 2006), interpreted as advantageous in places where rapid leaf successional stages. This is one of the few paleobotanical studies to expansion would be beneficial. Rapid leaf growth could provide attribute physiognomical and paleoecological variations in contem- toothed pioneer and ruderal species a competitive advantage in poraneous macrofossil assemblages to succession, and the first to disturbed habitats, especially where water availability is high and can apply insect herbivore damage data to issues involving disturbance support high rates of transpiration and photosynthesis. Although the and succession. mechanism driving the pattern may vary based on geography, phylogeny, and the presence/absence of a well-defined successional sequence (Royer et al., 2009; Little et al., 2010), these data 2. Non-taxonomic approaches to recognizing disturbance in overwhelmingly support a higher percentage of toothed angiosperm modern settings species in riparian and disturbed habitats. 2.1. Plant physiology and morphology 2.2. Plant ecology The first plants to occupy an area following a disturbance generally Ecological studies of disturbance and succession in neotropical have rapid resource acquisition, high growth rates, and a life strategy ecosystems have focused on forest regeneration following timber that maximizes seed production (Grime, 1974). Their leaves often harvesting, clear-cutting, and hurricanes. Guariguata and Ostertag have low leaf mass per area, short leaf lifespan, high nutrient (2001) review the literature and propose a four stage sequence for tropical terra firma forest recovery. Initial colonization by grasses, Table 1 herbs, and ferns occurs during the first five years following the Key characters for recognizing early versus late successional tropical forests. disturbance. Years 5–20 are characterized by early forest develop- Character Early successional forest Late successional forest ment, as short-lived pioneers create a closed canopy forest. Lianas,

Leaf margin Higher percentage Lower percentage toothed shrubs, and herbs are also an important component of the forest toothed species species (Guariguata et al., 1997; Pena-Claros and De Boo, 2002; Capers et al., Plant form Abundant lianas, Abundant canopy trees and 2005). Species richness steadily increases, and age since disturbance is shrubs, herbs, and understory vegetation the best predictor of plant diversity (Aide et al., 1996; Letcher and ruderal species Chazdon, 2009). Over roughly the next hundred years, long-lived Plant diversity Lower Higher, many rare species Insect herbivore Lower Higher, echoing the higher successors replace the short-lived pioneers. Plant species richness can diversity plant taxonomic and reach pre-disturbance levels in as few as forty years (Aide et al., 1996; structural diversity Barberena-Arias and Aide, 2003), and richness in late successional Insect herbivore Lower percentage Higher percentage of forests often exceeds that in primary forests because of the mixing of specialization of specialized feeders; specialized feeders; wider niche breadth narrower niche breadth early successional, late successional, and mature forest tree species Variation in Low. Most species High. Some species have (e.g. Vandermeer et al., 2000; Urquhart, 2009). The final stage of herbivory among have a lot of damage. very little damage, whereas recovery is the return to old growth forest composition. The nature plant species others have many types and and rate of this process depends on seed bank dynamics, soil occurrences of damage. characteristics, frequency and intensity of disturbance, and distance 244 E.D. Currano et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 309 (2011) 242–252 to and characteristics of the remnant forest. Although species richness strata in the late Oligocene Chattian stage, between 27 and 28 Ma can rebound to old-growth values within a few decades after a (Kappelman et al., 2003; Jacobs et al., 2005). disturbance, it often takes hundreds of years for the species The most productive and well-preserved fossil floras in the Chilga composition to return to what it was before the disturbance Basin occur in autochthonous overbank and pond deposits. These (Guariguata and Ostertag, 2001; Urquhart, 2009). floras, which consist of leaf, fruit, seed, and flower compressions, provide a unique view of wet, tropical vegetation from the interior of the Afro-Arabian continent. They predate both the major mammalian 2.3. Insect herbivory turnover event that occurred near the Paleogene–Neogene boundary (Maglio, 1978; Bernor et al., 1987; Gagnon, 1997; Kappelman et al., Ecological disturbances should have both direct and indirect 2003; Stevens et al., 2008; Rasmussen and Gutierrez, 2009; Ducrocq effects on insect herbivore communities. Frequent disturbances and Boisserie, 2010) and Miocene rifting. The plant species found at keep insect herbivore diversity low, and most insect species have a Chilga are characteristic of lowland or submontane tropical moist short generation time, high migratory ability, high reproductive forests and represent a historical biogeographic link between the potential, and low niche specialization (Brown, 1985). Insect currently disjunct Central and West African forests and the East communities also feel the bottom-up effects of changes in the plant African coastal and Eastern Arc forests (Jacobs et al., 2005; Pan et al., community, and specialized herbivores should be most susceptible 2006; Pan, 2007; Pan and Jacobs, 2009; Pan, 2010). Similar to modern because of their dependence on one or a few closely related host African tropical forests, legumes (Fabaceae) dominate the Chilga plants. Several studies have demonstrated an increase in herbivore floras. However, the occurrence and diversity of fossil palms at Chilga specialization with plant successional stage. Brown's (1985) land- contrasts strongly with extant African tropical forests, which are mark study of Heteroptera populations showed a decline in the notably depauperate in palms (Pan et al., 2006). proportion of generalist insect species and an increase in the proportion of specialists along a gradient of early to late successional 3.2. Fieldwork and paleobotanical analyses plant communities. Similarly, Brown and Southwood (1983), using a numerical scale to express niche breadth of sap sucking insects, In this study, we compare two fossil floras that occur in the same documented a decline in breadth as succession proceeded. More facies and are stratigraphically and temporally equivalent. The Guang recently, a study of restoration plots in the Brazilian Amazon found River plant fossil horizon is exposed laterally for 60 m along the that forest age is the most important factor determining the richness Guang River, and the Bull's Bellow locality is 1.5 km to the south, along of galling insects (Fernandes et al., 2010), considered among the most the Margargaria River (Fig. 1, Table 2). Detailed lithological de- specialized of insects. scriptions were made at four different sublocalities at Bull's Bellow Published theories regarding the effects of plant succession on and at a single locality (CH40) along the Guang River (Fig. 2). Sections insect herbivore diversity are all founded on the idea that a more were dug back minimally 300 mm in order to avoid modern complex resource base can support more species than a simple weathering features. Descriptions include lithology, sedimentary resource base. Most insect species display some degree of specializa- structure, color, acid-reaction class, bed thickness and characteristics tion (Bernays and Chapman, 1994; Termonia et al., 2001; Farrell and of boundaries between sedimentary rock layers. Sediment and Sequeira, 2004), and increasing the complexity of the resource base paleosol profile colors were determined by comparison of dry samples creates more niches for insect herbivores. Resource complexity can be against Munsell® Color Chips (Munsell Color, 1975). defined taxonomically or structurally. According to the taxonomic Because the two fossil horizons are laterally extensive, we diversity hypothesis, the more taxonomically diverse a plant com- excavated and collected fossil plants from four sublocalities at munity is, the more insect species it can support (Siemann et al., 1998; Guang and seven sublocalities at Bull's Bellow to capture spatial Bröse, 2003), and a variety of studies have demonstrated a positive heterogeneity within each locality. Sublocality sites were selected correlation between plant diversity and insect diversity (Wright and based on accessibility, rock cohesiveness, and preservational quality Samways, 1998; Hawkins and Porter, 2003; e.g. Haddad et al., 2009). of plant remains. At each sublocality, the fossil-bearing layer was The structural heterogeneity hypothesis, on the other hand, states identified and the overburden removed to make a bench quarry. Every that heterogeneity in plant architecture and structure increase as a leaf fragment that had the potential to be identified was collected and forest matures, driving higher insect diversity in later successional curated at the National Museum of Ethiopia, Addis Ababa. A total of stages (Southwood et al., 1979; Bröse, 2003; Jeffries et al., 2006). 433 identifiable leaves (or leaflets in the case of compound leaves) Architectural diversity refers to the distribution of different types of were collected at Guang and 645 at Bull's Bellow. plant structure and tissues, and structural diversity to the distribution Leaf fossils were sorted into plant morphotypes using leaf of plant parts spatially above ground level. In all likelihood, both plant architectural (Ellis et al., 2009) and cuticular characters (Dilcher, taxonomic and structural diversity influence insect species diversity, 1974). Fossil cuticle was isolated from the rock matrix by first placing and higher herbivore diversity is therefore expected in a late leaf fragments in 10% HCl for half an hour, then rinsing them with successional forest than an early successional forest. distilled water, and finally immersing them in 48% HF until the cuticle was completely matrix-free (2–24 h). The specimens were then 3. Methods treated with a dilute bleach solution to further isolate the cuticle, which was then mounted on slides in glycerine jelly for light 3.1. Geologic overview microscopy. Fossil specimens were compared with extant plant collections in herbaria at the Royal Botanic Gardens, Kew, Missouri The study area is located 60 km west of Gondar in Chilga Woreda, Botanical Garden, and Botanical Research Institute of Texas. Amhara Region, northwestern Ethiopia. Massive flood basalts up to Every identifiable leaf (or leaflet) with at least half of the blade intact 2000 m thick were extruded about 30 Ma (Hofmann et al., 1997), was scored for insect herbivore damage using the Labandeira et al. followed by faulting in the middle to late Oligocene to create a basin (2007) damage type (DT) system. Insect folivory was distinguished no less than 325 and probably no greater than 1000 km2. Fossiliferous from detritivory or taphonomic alteration by the presence of plant clastic and volcaniclastic sediments interbedded with volcanic de- response tissue; consistency in the pattern, position, or type of damage; posits filled the basin (Feseha, 2002; Jacobs et al., 2005). A total of or specific micromorphological features, such as pupal chambers, 150 m of stratigraphic section containing fossil plants and animals is particular mandible bite marks, or exit slits in mines and galls exposed; radiometric dates and paleomagnetic reversals place these (Labandeira, 1998). Damage types can be divided into generalized E.D. Currano et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 309 (2011) 242–252 245

A C CH52 Hauga D CH40 River

0°

Basalt: 32.4 +/- 1.6 Ma

Hadeza Kernet River River CH41 B 36° 40° 44° 48° CH54 14° Guang, inset D 10 m Chilga Basin Bull’s Bellow, Guang River Sublocalities inset C 12° 12 30° inset E CH95 CH72 E CH90 N Tuff: 27.36+/- 0.11 Ma CH91 CH103 10° CH101

6° CH92 Guang Bull’s Bellow Sublocalities 37 03° 10 m 4° River

Fig. 1. Map of the Chilga study area, modiﬁed from Kappelman et al. (2003). (A) Location of the Chilga Basin on the Afro-Arabian continent and (B) in Ethiopia. (C) Detailed map of the Chilga area showing the location of the Guang River and Bull's Bellow fossil plant localities and dated rock samples along the Guang and Hauga Rivers. (D) Spatial separation of the sublocalities at Guang and (E) at Bull's Bellow.

DTs, made by insects whose diet typically includes many taxonomically either fossil or extant host taxa (Labandeira, 2002; Labandeira et al., unrelated plants, and specialized DTs, made by insects that typically 2007). Here, we consider DTs to be specialized if they have a host consume only one or a few closely related host plants (Wilf and specialization value of 2 or 3 on the 1–3 scale in the Labandeira et al. Labandeira, 1999; Labandeira et al., 2002; Labandeira et al., 2007). (2007) system. Specialization is recognized by similarity to extant specialized feeders, by morphologically stereotyped damage patterns, and by restricted 3.3. Quantitative analyses occurrences confined to particular host-plant species or tissue types in All analyses were performed in R version 2.9.2 (R Development Core Team, Vienna, Austria). We analyzed plant species richness, evenness, and heterogeneity for each flora. Floral richness, or the number of plant species standardized for sample size, was measured Table 2 Sampling summary, Guang River and Bull's Bellow. using analytical rarefaction, and errors were estimated using Heck et al.'s (1975) standard error. Probability of interspecificencounter Sublocality Site GPS No. No. leaf No. insect (PIE) was used to compare evenness among sublocalities and coordinates identifiable species or herbivore ⁎ leaves morphotypes DTs between Guang and Bull's Bellow. Floral heterogeneity within a locality was quantified by calculating the Bray–Curtis distance CH40 Guang N 12.5134 209 14 21 E 37.1240‡ between all pairs of sublocalities. These distances were calculated CH41 Guang N 12.5129 94 25 14 from a matrix of plant species' relative abundances. We averaged the E 37.1240 results within each locality to obtain a single value for CH52 Guang N 12.5134 74 15 12 heterogeneity. E 37.1240‡ Insect folivory was examined using three damage metrics: CH54 Guang N 12.5129 56 18 13 E 37.1239 diversity, frequency, and composition. Damage diversity, or the Guang total 433 40 32 number of DTs present at a site or on a host species, was normalized for the number of leaves sampled as in previous studies (Wilf and CH72 Bull's Bellow N 12.50890 195 22 18 Labandeira, 1999; Currano et al., 2008). Damage diversity on a per- E 037.11300 CH90 Bull's Bellow N 12.50888 126 15 9 leaf basis is a core measure of how many ecological feeding types are E 037.11288 present on a certain amount of foliage resource. Although damage CH91 Bull's Bellow N 12.50886 34 10 2 diversity is not completely analogous to insect diversity, preliminary E 037.11277 data from Panama show a good correspondence between DT diversity CH92 Bull's Bellow N 12.50873 155 14 17 and actual insect diversity (Ramírez-Carvalho et al., 2009). Damage E 037.11270 CH95 Bull's Bellow N 12.50937 75 14 6 frequency is simply the percent of leaves in a sample that are E 037.11417 damaged. Because a leaf either has damage or does not, error bars for CH101 Bull's Bellow N 12.50929 5 4 1 damage frequency are calculated using a binomial sampling distribu- E 037.11397 tion. Damage composition refers to the relative abundance of the DTs CH103 Bull's Bellow N 12.50936 55 10 10 E 037.11423 in different samples. Only DTs that occurred on two or more leaves Bull's Bellow total 645 35 27 were included in these analyses. The data were first arcsine square- root transformed to improve normality (Sokal and Rohlf, 1995). The ⁎ Damage types. ‡ “ ” CH40 and CH52 are less than 5 m apart and therefore have identical GPS metaMDS function in R was then used to perform nonmetric coordinates at this resolution. multidimensional scaling (NMS) ordinations. 246 E.D. Currano et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 309 (2011) 242–252 Bull’s Bellow Guang River CH72 CH90 CH91 CH92 CH40 5Y5/1 5Y7/3

260 5Y8/2 260 260 260 260 G24/10G G24/10G Legend 5Y6/6 250 250 250 250 250 Fossil leaves G14/N G14/N 5Y5/1 240 240 240 240 240 Fossil fragments Mud drapes 230 230 230 230 230 5Y8/3 G15/10Y G15/5Y Burrows 220 220 220 220 220 Ripple cross 5Y4/1 G24/10G lamination 210 210 210 210 210 Blocky structure G14/N 200 200 200 200 200 G15/5Y Wavy lamination 190 2.5Y6/1 190 190 190 190 Trough X-beds 180 180 5Y6/2 180 5Y4/1 180 180 Transported logs 5Y5/3 Burnt logs 170 170 170 G16/10Y 170 170 Root structures 5Y5/6 160 160 160 G15/5G 5Y5/1 160 160 Paleosol tops 5Y5/3 150 150 G14/10Y 150 5Y6/3 150 150 Sphaerosiderite 5Y7/8 concretions 140 G13/10Y 140 140 140 140 5Y5/2 130 130 & 5Y4/3 130 130 130 5Y5/2 120 120 120 120 5Y4/2 120 5Y4/2 5Y5/2 110 110 110 110 110 & 5Y4/2 G13/5GY 100 100 G14/5GY 100 100 100

90 90 90 90 90 5Y6/3 80 80 80 5Y5/2 G26/10G 80 80 5Y6/2 70 70 70 & 70 70 5Y1/1 5Y5/2 5Y6/2 60 60 5Y5/3 60 60 60 & 7.5YR5/2 50 50 50 50 5Y6/3 50 2.5Y7/3 40 40 40 40 40

30 30 30 30 30

20 20 20 20 20

10 10 10 10 10 G13/5GY

0 0 0 0 0 Cl Cl Cl Cl Cl fss fss fss fss fss ms ms ms ms ms vfss vfss vfss vfss vfss SlCl SlCl SlCl SlCl SlCl O.M. O.M. O.M. O.M. O.M.

Fig. 2. Detailed stratigraphic sections through Bull's Bellow and Guang river sublocalities. Descriptions and interpretations are in the text, Sections 4.1 and 5.1.

4. Results (Jacobs et al., 2005). The upper half to one-third of the measured sections is dominated by claystones, silty claystones and mudstones and only 4.1. Sedimentology and stratigraphy rarely preserves carbonized organic matter compressions or concretionary sphaerosiderite. At Bull's Bellow, this upper part of the stratigraphy The fossil flora stratigraphic unit considered herein was collected preserves sedimentary transport structures including plane-to-wavy from a single layer ranging in thickness from 9 to 40 cm (Fig. 2) laminations, ripple cross-lamination, small-scale (10–20 cm deep) composed of drab-colored, wavy laminated to thinly bedded, trough cross-bedding and clear examples of a scour-and-fill deposit claystone to mudstone. This single bed is correlative among all (CH90, 160–180 cm) and mud drapes (CH90, 245–260 cm). In addition, study sites based upon the authors' ability to walk this bed, and verify fallen and burnt tree trunks occur among three of the five measured its continuity, from the Guang River to Bull's Bellow collection sites. sublocality sections, and only in the beds within the fossil flora unit. The stratigraphy of the Bull's Bellow and Guang River sites is dominated by drab-colored and fine-grained lithologies (Fig. 2). The 4.2. Plant taxonomy lower half to two-thirds of each measured and described sublocality section is dominated by massive to angular blocky claystone to mudstone The Bull's Bellow flora includes numerous taxa typically associated with common, vertical to horizontal, branching organic matter com- with early successional stages of tropical forest regrowth (Fig. 3). pressionsaswellascommon(2–5% by volume) to abundant (5–15% by These consist of abundant fruit compressions representing the tribe volume) mm-sized, orange to brown, sphaerosiderite concretions Naucleeae sensu lato (Rubiaceae; Fig. 3A, B) and fossil vegetative E.D. Currano et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 309 (2011) 242–252 247

G D

F C B

Fig. 3. Bull's Bellow and Guang River disturbance plant taxa. A, B: Naucleeae (Rubiaceae) reproductive structures, scale bar — 10 mm, (A) inﬂorescence or immature infructescence, (B) infructescence; C–G: Leaf compressions, scale bar — 20 mm, (C) Cardiospermum sp., (D) African rattan (Arecaceae: Lepidocaryeae) leaﬂet fragment, (E) Euphorbiaceae, (F) Salicaceae sensu lato.

material of heliophytic vine and liana taxa including Cardiospermum 2009). The Guang River flora also consists of fossils that likely (Sapindaceae; Fig. 3C), an African rattan (Arecaceae: Lepidocaryeae; represent slow growing, canopy or emergent trees including Fig. 3D), and a morphotype that likely represents either Aristolochia- Cynometra, Afzelia (Fabaceae: Detarieae sensu lato), and two ceae or Menispermaceae. In addition, numerous toothed-leaves of Sapotaceae morphospecies (Sapoteae sp. and Chyrsophylloid sp.; Euphorbiaceae (Macaranga or a closely related euphorbiaceous taxon; (Pan, 2007; Pan et al., 2010)). While the presence of disturbance Fig. 3E) and Salicaceae sensu lato (Fig. 3F) are present and represent indicator taxa is consistent with a secondary forest community, the ruderal elements (George et al., 1993; Slik et al., 2003; LaFrankie et al., abundance of understorey and mature canopy forest groups in the 2006). Guang River flora suggest a later stage of forest regrowth capable of The Guang River flora differs from Bull's Bellow in the co- recruiting and sustaining such elements. occurrence of forest taxa that are typical of early secondary forests and those found in later successional stages of forest regrowth. Guang River fossil taxa representinggroupscommonlyassociated 4.3. Plant morphology with forest gaps, forest edges, and recolonized areas include Eremospatha (Arecaceae: Lepidocaryeae), Clausena (Rutaceae), Two out of 34 dicot species at Guang have toothed leaves, Dioscorea section Lasiophyton (Dioscoreaceae), and Strychnos compared to seven out of 35 at Bull's Bellow. Because margin type (Loganiaceae; Fig. 3G; Pan et al., 2006; Pan, 2007; Sunderland, is a binomial character, a binomial distribution was used to compute 2007; Pan, 2010), whereas genera with living relatives commonly errors on the percent of untoothed species as described by Wilf occurring as understorey, shade tolerant trees in African moist (1997).TheGuangflora, with 5.9±4.0% toothed species, has forests include Cola (Malvaceae sensu lato: Sterculiodeae), Ocotea significantly fewer toothed species than the Bull's Bellow flora, with (Lauraceae), and Eugenia (Myrtaceae; (Pan, 2007; Pan and Jacobs, 20±6.8% toothed species. 248 E.D. Currano et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 309 (2011) 242–252 A 20 40

16 30

20 8 No. morphotypes No. Morphotypes 10 4

Guang River Bull’s Bellow 0 0 7654321 189503521141310 0 100 200 300 400 500 Frequency of Occurrence, Guang River No. leaves

Fig. 4. Rarefaction curves comparing the number of angiosperm leaf morphotypes at B Guang River and Bull's Bellow. The thin lines are diversity at the sublocalities, and the 20 thick lines show total diversity at Guang and Bull's Bellow when the sublocalities from each site are lumped. The shaded area represents the standard error on the rarefaction calculated using the equations of Heck et al. (1975). 16

4.4. Plant richness and heterogeneity 8 In order to examine plant richness standardized for sample size, No. Morphotypes rarefaction curves were plotted for the Guang River and Bull's Bellow 4 sublocalities (Fig. 4). Although there is a range in rarefied species richness at sublocalities within a site, the Guang localities generally 0 have more species than those at Bull's Bellow (Table 3). When the 98754321 21887524742372322171510 fi sublocalities at each site are lumped together, Guang has signi cantly Frequency of Occurrence, Bull’s Bellow higher floral richness than Bull's Bellow. Furthermore, the lumped Bull's Bellow curve and most Bull's Bellow sublocality curves are Fig. 5. Frequency of occurrence of angiosperm leaf morphotypes at (A) Guang River and beginning to level off, indicating that we have sampled much of the (B) Bull's Bellow. Note that the x-axis is not to scale. diversity at this site. In contrast, additional collecting is needed to fully sample diversity at Guang, as illustrated by the steadily increasing rarefaction curves. Swartzieae (cf. Mildbraediodendron) composes another 13% of the Both sites are strongly dominated by a single plant species and leaves at Bull's Bellow. To examine lateral plant heterogeneity within over half of the plant species are represented by less than five leaves each locality, we calculated Bray–Curtis distances between sublocal- (Fig. 5). Thus, there is very little difference in evenness between ities (Tables 4 and 5), which measure differences based upon species Guang and Bull's Bellow at both sublocality and locality levels compositions and frequencies. The mean Bray–Curtis distance (Table 3). The most abundant species at each site are legumes. between sublocalities is 0.65 at Guang and 0.51 at Bull's Bellow. Cynometra chaka makes up 44% of the leaves at Guang, an Albizia-like This difference is significant (t=−2.78, p=0.02, df=7), indicating leaf (mimosoid sp. 1) is 34% of the total at Bull's Bellow, and that the Guang flora is more heterogeneous.

Table 3 Table 4 Floral diversity and evenness. Bray–Curtis distance, calculated using plant abundance data, for the Guang sublocalities Sublocality Shannon Probability of Rarefied arrayed from south to north. interspecific diversity at CH54 CH41 CH40 CH52 encounter 50 leaves CH54 – CH40 (G) 1.57 0.66 9.33 CH41 0.64 – CH41 (G) 2.58 0.88 17.87 CH40 0.75 0.64 – CH52 (G) 1.53 0.58 12.32 CH52 0.79 0.55 0.55 – CH54 (G) 2.53 0.91 17.11 Average of Guang River 2.05±.58 0.76±.17 14.16±4.05 sublocalities Lumped Guang River 2.32 0.78 Table 5 Bray–Curtis distance, calculated using plant abundance data, for the Bull's Bellow fi CH72 (BB) 2.3 0.81 14.71 sublocalities with at least 50 identi able leaves. Sites are ordered from west to east. CH90 (BB) 1.72 0.73 10.27 CH92 CH90 CH95 CH72 CH103 CH92 (BB) 2.07 0.85 9.33 CH95 (BB) 2 0.81 12.01 CH92 – CH103 (BB) 1.74 0.74 9.8 CH90 0.58 – Average of Bull's Bellow 1.96±.24 0.79±.05 11.35±2.08 CH95 0.47 0.44 – sublocalities, N50 leaves CH72 0.61 0.55 0.54 – Lumped Bull's Bellow 2.44 0.84 CH103 0.55 0.51 0.29 0.58 – E.D. Currano et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 309 (2011) 242–252 249 A 40 35 Guang River Guang River Bull's Bellow 30 Bull's Bellow

25 30 20

15 No. DTs 10 20

0 100 200 300 400 500 600 700 % of Le a ve s or DTO 10 B 20

15 0 % leaves, % leaves, % leaves, % DTO, % DTO, 10 total gen. spec. spec. galls damage damage damage 5 Fig. 7. Damage specialization at Guang and Bull's Bellow. DTO: Damage type occurrence. No. Specialized DTs 0 0 100 200 300 400 500 600 700 Damage frequency is signiﬁcantly higher at Guang than at Bull's C 5 Bellow (31.6 vs. 23.1% of leaves damaged, Fig. 7). The percent of leaves with specialized damage is nearly double, and the percent of leaves 4 with generalized damage is also slightly higher. Elevated specialization at Guang is also apparent when percent of damage occurrences 3 rather than percent of leaves damaged are analyzed, and it appears to be primarily driven by an increase in galling at Guang. 2 An NMS ordination of percent of leaves with each DT at each sublocality conﬁrms that there are important differences in damage

No. Mine Types 1 composition between Guang and Bull's Bellow (Fig. 8A). The Guang River sublocalities plot close to each other and are separated from 0 most of the Bull's Bellow sublocalities. The Bull's Bellow sublocalities 0 100 200 300 400 500 600 700 show more scatter, indicating greater variation in damage composi- No. Leaves tion, and Bull's Bellow sublocality CH92 plots closer to the Guang sublocalities than to other Bull's Bellow sublocalities. Fig. 8B considers Fig. 6. Resampling curves of (A) total, (B) specialized, and (C) mine damage diversity at Guang and Bull's Bellow. Shaded area represents one standard deviation above and damage composition on individual plant hosts at the two sites. The below the mean of the resamples. Guang and Bull's Bellow hosts do not form distinct groups, and show a similar amount of variation in damage composition within locality. Thus, both localities contain a mix of little damaged and highly 4.5. Insect herbivory damaged plant taxa.

We analyzed insect damage diversity, frequency, and composition at each locality for both individual host plants and the bulk flora. Total, 5. Discussion specialized, and mine damage diversity on the bulk flora are all significantly higher at Guang than at Bull's Bellow (Fig. 6). However, 5.1. Sedimentology and depositional environments when analyzing herbivory on individual host species at the two sites, only total damage diversity is higher at Guang (Table 6). Therefore, We consider the massive to angular blocky claystones to the higher damage diversities on the Guang bulk flora are most likely mudstones, which may preserve concretionary sphaerosiderites, to due to elevated plant richness at Guang. be paleosol profiles. Furthermore, we consider the branching

Table 6 Insect herbivory data.

Plant species or leaf morphotype Site Total DTs at 30 leaves Specialized DTs at 30 leaves Mine DTs at 30 leaves

Cynometra chaka Guang 5.7 ±1.6 2.0±1.2 0.2 ±0.4 Sapoteae sp. Guang 4.3 ±1.0 1.6±0.5 0 Type H Guang 7.4 ±1.0 0.9±0.3 0 Guang River average 5.8±0.4 1.5±0.5 0.05±0.2 Albizia-like (mimosoid sp. 1) Bull's Bellow 5.2 ±1.5 1.1±0.8 0 Cf. Aristolochiaceae sp. 1 Bull's Bellow 7.0 ±0.9 2.4±0.7 0 Euphorbiaceae sp. 1 Bull's Bellow 4.9 ±1.5 1.7±1.1 0 Swartzieae (cf. Mildbraediodendron) Bull's Bellow 2.7 ±1.0 1.6±0.8 0.6 ±0.5 Small tooth Bull's Bellow 5.3 ±1.2 1.4±0.6 0 Type Y Bull's Bellow 3.1 ±0.8 3.1±0.8 0 Bull's Bellow average 4.3±0.3 1.8±0.2 0.1±0.2 250 E.D. Currano et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 309 (2011) 242–252

A With the exception of CH92, all of the sublocalities inspected preserve a paleosol proﬁle directly beneath the unit containing the

0.5 fl fi 91 fossil ora. Note that scour and erosion of this paleosol pro le can be 40 quite extensive (e.g., scour of paleosol in Bull's Bellow CH90), and 54 thereforeitispossiblethatacorrelativesoilprofile at CH92 was present, but completely eroded, prior to deposition of the overlying 92 fl

0.0 41 unit containing the fossil ora. Nevertheless, the regional sedimen- 52 72 tology directly beneath this fossiliferous stratigraphic unit repre-

NMS Axis 2 sents a generally stable yet swampy landscape across this part of the 95 basin. The common feature of burnt, fallen and transported fossil tree -0.5 90 103 trunks at two of the four Bull's Bellow sublocality sections and at Guang River sublocality CH40 suggests an important ecological shift that resulted in destruction, transport, deposition, and preservation -1.0 -0.5 0.0 0.5 of large-statured plants at least in this part of the basin. It is NMS Axis 1 impossible to determine from our data the mechanism responsible for this ecological shift, but it nevertheless included ﬁre as part of the B disturbance process. However, the fossiliferous units of the Bull's Type K1 Bellow sublocalities are composed of numerous beds and lamina- Type B ACE tions, suggesting multiples episodes of deposition and a generally Mild. Fab. 3 more “disturbed” environment than the fossiliferous unit at the Type R Chrys. Guang River sublocality, which is composed of a single, featureless Sori. Sapo. Type Y Alb. mudstone that may represent a single depositional event subse- Cyno. Aris. quently overprinted by pedogenesis (Fig. 2). These differences in Euph. Clau. sedimentary structure suggest that the Guang River locality

NMS Axis 2 SmT Tri. Type H represents a more stable, relatively more quiescent and low-energy

Caes. depositional system than the Bull's Bellow locality during deposition of the fossiliferous unit.

-1.0 -0.5 0.0 0.5 5.2. Resolving fossil and depositional records -1.0 -0.5 0.0 0.5 1.0 1.5 NMS Axis 1 Basin-wide studies of the sedimentology, stratigraphy, and Fig. 8. Nonmetric multidimensional scaling (NMS) ordinations of insect folivore paleosols at Chilga indicate a heterogeneous landscape (Jacobs et al., damage (A) at each sublocality and (B) on each plant species. NMS axes 1 and 2 define 2005). A mixture of poorly-drained and well-drained paleosol types the two-dimensional ordination space that most accurately represents differences in occur within the basin, indicating that landscape heterogeneity was fi damage composition among samples. Guang samples are indicated by lled circles and likely caused by differences in water table height across space and Bull's Bellow samples by open triangles. Leaf species or morphotype abbreviations as follows: Mild. = Swartzieae (cf. Mildbraediodendron); Fab. 3 = Fabaceae sp. 3; Sori. = with time. Sedimentological analyses of stream channel and overbank Sorindeia sp.; Cyno. = Cynometra chaka; Albizia-like = Albizia-like (mimosoid sp. 1); deposits suggest that rivers had relatively shallow gradients and Sapo = Sapoteae sp.; Chry. = Chrysophylloid sp.; Aris. = cf. Aristolochiaceae sp. 1; wandered across the landscape, changing course and affecting plant Euph. = Euphorbiaceae sp. 1; SmT = Small tooth; Caes. = Caesalpinieae legume. communities via periodic flooding events (Jacobs et al., 2005). Additionally, charred tree trunks at three of five measured sections carbonized organic matter to be root compressions, and therefore also provide evidence for fires altering the landscape. In this study, we represent parts of paleosol profiles. These strata (capped by “˜” consider the consequences of this disturbance regime across space at symbols in Fig. 2) represent intervals of stability, colonization by flora a single time. and fauna, and relative quiescence with respect to deposition (e.g., Because the Guang River and Bull's Bellow floras are stratigraphi- Buol et al., 1997; Birkeland, 1999). Nevertheless, the presence of cally equivalent and only 1.5 km apart, it is surprising that the two concretionary sphaerosiderite (a ferrous Fe-mineral) and carbonized have no plant species in common. However, our stratigraphic and organic matter suggest these profiles developed as poorly drained, sedimentological data provide evidence that the Bull's Bellow site was swampy soils. a less stable, higher energy environment than the Guang River site, Sedimentary structures associated with the fossil bed at Bull's and a detailed analysis of the taxonomy, plant physiognomy, and Bellow sublocalities include plane and wavy laminations, ripple paleoecology at each site confirms that the two floras represent cross-lamination, trough cross-bedding, and scour-and-fill struc- different stages of tropical forest recovery. Bull's Bellow has a higher tures, most of which are indicative of bedload transport under low- percentage of plant species with toothed margins, and the nearest to upper-flow regimes (Fig. 2). Yet, the lithology of these strata is living relatives of many of the plant species are associated with early composed of claystone, silty claystone, and mudstone, none of which successional forests. Both plant and insect herbivore diversity are typically participate in bedload transport due to the hydrodynamic relatively low, and there is very little specialized damage. In contrast, behavior of such fine-grained materials in turbulent flow (e.g., the Guang River flora has a very low percentage of plant species with Birkeland, 1999). We suspect these fine-grained lithologies with toothed margins, and the plants are a mix of early and late suc- bed-load sedimentary transport structures reflect diagenetic alter- cessional species. Plant and insect damage diversity are significantly ation of originally labile coarse (coarse silt to fine-sand sized) higher than at Bull's Bellow, and the frequency of specialized damage volcanic grains to phyllosilicate minerals, which are the residuum of is nearly twice as high. A review of the ecological literature indicates in-situ chemical weathering that took place soon after burial. In this that these physiological and ecological attributes are consistent with a respect, portrayals of sedimentary grain sizes in Fig. 2 may be a more mature forest community (Table 1). misleading indicator of transport energies, and therefore we will Consequently, multiple biotic and abiotic proxies indicate that consider only sedimentary structures in the foregoing interpretation disturbance, succession, and other landscape-level ecological of depositional environments. processes explain variations in plant physiognomy, plant and insect E.D. 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