Rainforest collapse triggered diversifi cation in Euramerica

Sarda Sahney1, Michael J. Benton1, and Howard J. Falcon-Lang2* 1Department of Sciences, University of Bristol, Bristol BS8 1RJ, UK 2Department of Earth Sciences, Royal Holloway, University of London, Surrey TW20 0EX, UK

ABSTRACT islands exerted a major impact on tetra- Abrupt collapse of the tropical rainforest biome ( ) drove rapid diversifi cation pod diversity, ecology, and the development of of Carboniferous ( and ) in Euramerica. This fi nding is based on endemism. In doing so, we draw on the theory analysis of global and alpha diversity databases in a precise geologic context. From Visean to of island biogeography (MacArthur and Wilson, Moscovian time, both diversity measures steadily increased, but following rainforest collapse 1967), which was developed to explain pat- in earliest time (ca. 305 Ma), tetrapod extinction rate peaked, alpha diversity terns of diversifi cation in oceanic islands, but is imploded, and endemism developed for the fi rst time. Analysis of ecological diversity shows equally applicable to other kinds of islands, e.g., that rainforest collapse was also accompanied by acquisition of new feeding strategies (preda- rainforest refugia. tors, herbivores), consistent with tetrapod adaptation to the effects of habitat fragmentation and resource restriction. Effects on amphibians were particularly devastating, while METHODS: LATE (‘reptiles’) fared better, being ecologically adapted to the drier conditions that followed. Our TETRAPOD DATABASE results demonstrate, for the fi rst time, that fragmentation infl uenced profoundly In order to detect changes in tetrapod diver- the ecology and of terrestrial fauna in tropical Euramerica, and illustrate the tight sity across the Moscovian-Kasimovian inter- coupling that existed between vegetation, climate, and trophic webs. val, we constructed two late Paleozoic tetra- pod databases, comprising records of global INTRODUCTION that show that dropped to its one of and alpha diversity over nine global stages During the latter part of the Carboniferous its lowest levels in the entire , if (Visean, , , Mosco- (318–299 Ma), Europe and not its lowest level (Heckel, 1991, 2008), pre- vian, Kasimovian, , , Sak- (Euramerica) were positioned over the equator, cisely coincident with the most abrupt phase marian, and ) ranging from 346 to and were covered, at times, by humid tropical of vegetation change (DiMichele et al., 2009). 270 Ma. We chose to restrict the analysis to this rainforest (DiMichele et al., 2007). This biome, An alternative hypothesis is that medium-term time span because the bracketing colloquially referred to as the Coal Forests, greenhouse warming drove aridifi cation, as and stages were times of very low comprised a heterogeneous vegetation mosaic supported by far-fi eld records in diversity, which have been interpreted as mass (Gastaldo et al., 2004) inhabited by a rich ter- (Fielding et al., 2008) and evaporites in high- extinctions or gaps in the record, i.e., Romer’s restrial fauna (Falcon-Lang et al., 2006). As cli- stand deposits in western Euramerica (Bishop gap and/or bottleneck (Ward et al., 2006) and mate aridifi ed through the later Paleozoic, these et al., 2010). However, regardless of what Olson’s gap and/or extinction, respectively rainforests collapsed, eventually being replaced caused aridifi cation, the consensus is that this (Sahney and Benton, 2008). by seasonally dry biomes (Montañez et climate shift led to the fragmentation of the al., 2007). Collapse occurred through a of Coal Forests into isolated rainforest islands Global Diversity Database step changes. First there was a gradual rise in the surrounded by xerophytic scrub (Falcon-Lang, Initially 67 families from 163 tetrapod sites frequency of opportunistic in late Mosco- 2004; Falcon-Lang et al., 2009; Falcon-Lang worldwide were tabulated to create the global vian time (Pfefferkorn and Thomson, 1982). and DiMichele, 2010). diversity database. Analysis was run with all This was followed in the earliest Kasimovian At the time of peak levels of rainforest die- of the families and then was repeated after (cyclothem-calibrated of 305.4 Ma; Heckel, back in the earliest Kasimovian, terrestrial removing 14 monotypic families, those repre- 2008) by a major, abrupt extinction of the domi- faunas had already become highly diversifi ed, sented by only a single species. The inclusion nant K-selected lycopsids and a switch to - composing sophisticated interconnected com- or exclusion of singletons made no difference dominance (DiMichele and Phillips, 1996). munities (Falcon-Lang et al., 2006). Detritivory to the results as they are randomly distributed In latest Kasimovian time, rainforests vanished was the most common primary feeding strategy through the time bins and the overall diver- (DiMichele et al., 2006). utilized by , molluscs, and , sity patterns remained the same. Stratigraphic The nature and cause of late Moscovian- including the giant litter-splitting arthropleu- ranges were assigned to each family and the Kasimovian rainforest collapse have been the rids (Shear and Kukaloveck, 1990; Labandeira, associated dates were correlated with the subjects of intense investigation. In cratonic 2006). However, some had addition- Davydov et al. (2010) time . areas of North America (where the effects of ally evolved herbivorous and predatory forms Each family was also given an ecological tectonics can be excluded), an abrupt shift to (Labandeira and Sepkoski, 1993; Grimaldi and assignment based on size (snout-vent length; more arid climates has been linked to rainforest Engel, 2005). Terrestrial (tetrapods), small: <0.15 m, medium: 0.15–1.50 m, large: collapse (DiMichele et al., 2009, 2010), though which included amphibians and amniotes >1.50 m) and diet (fi sh, insects, tetrapods, the exact causal mechanism remains uncer- (‘reptiles’), were mostly piscivores, refl ecting ), resulting in 12 ecological niches. Diet tain. One hypothesis is that aridifi cation was their dominantly waterside habitats, but some was inferred from jaw and tooth structure, pat- triggered by a short-term but intense glacial forms also had evolved insectivory (Benton, terns of tooth wear, body size, and whether the phase. This is supported by earliest Kasimo- 2005; Coates et al., 2008). Here we analyze the animal was adapted for a predominantly aquatic vian paleosols in the Lost Branch cyclothem effects of rainforest collapse on tetrapod com- or terrestrial lifestyle (Benton, 1996). Occasion- munities. Specifi cally we test the hypothesis ally, direct evidence in the form of gut contents *E-mail: [email protected] that population constriction into isolated rain- was available, e.g., and pteridosperm

© 2010 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or [email protected] GEOLOGY,Geology, December December 2010; 2010 v. 38; no. 12; p. 1079–1082; doi: 10.1130/G31182.1; 3 fi gures; 1 table. 1079 ovules in the Permian , (sometimes termed beta diversity, BD). Ende- (Munk and Sues, 1992). mism is calculated by dividing global diversity

(Tt) by mean alpha diversity (T) (BD = Tt / T; Alpha Diversity Database Sepkoski, 1988). Community data, compiled in the alpha diversity database, were constructed as a subset RESULTS: TETRAPOD of the global database, containing the most com- DIVERSIFICATION PATTERNS plete tetrapod assemblages available. Individual Several patterns emerge from our analysis. assemblages were selected based on the occur- First, global diversity steadily rose through the rence of >100 partial skeletons at a given site study interval from 6 to 7 families in the Visean and, where possible, collector curves were used and Serpukhovian to 39 families in the Artin- to assess completeness of these assemblages. skian (Fig. 2A). However, while alpha diver- After fi ltering, the database contained 22 well- sity closely tracked global diversity until the sampled assemblages. late Moscovian (i.e., Nyrany and Linton alpha Although variably time averaged, we assumed sites), the two curves dramatically diverged that each assemblage was representative of a local across the Moscovian-Kasimovian boundary as community (sensu Begon et al., 2005). The num- alpha diversity collapsed from 20 families to 7 ber of families represented in each community families (Fig. 2A). was tabulated, based on published assignments Analysis of the rates of alpha and global (supplemental databases: global diversity data- diversifi cation helps explain this divergence. base—http://www.fossilrecord.net/fossilrecord/ Although the global diversifi cation rate slowed download.html; alpha diversity database—http:// across the Moscovian-Kasimovian boundary, the palaeo.gly.bris.ac.uk/Sahney/pub/index.html) as rate became strongly negative at the alpha (com- a proxy for alpha (community) diversity. Com- munity) level, the only time when either rate of munities were binned by , and assigned an diversifi cation became negative in the nine stages, average age (based on Davydov et al., 2010), to refl ecting the fact that communities shrank in construct an alpha diversity curve. size, i.e., an “alpha implosion” (Fig. 2B). There is only one way to reconcile such a rise Data Distribution and Analysis in global diversity at a time when alpha diversity Figure 2. Tetrapod diversifi cation patterns The global (n = 163) and alpha (n = 22) was falling: the degree of endemism must have from Visean (346 Ma) to Artinskian (270 Ma). data sets were plotted on a Kasimovian paleo- risen markedly between the Moscovian and A: Global diversity of tetrapods and alpha geographic map, demonstrating that ~97% of Kasimovian-Gzhelian intervals. Calculations diversity. B: Alpha and global diversifi cation records derived from the paleoequatorial zone confi rm that this is the case. The development rates measured as fi rst derivative of values in A. C: Endemism measured as global di- and therefore intensively sample a single region. of endemism peaked in Kasimovian-Gzhelian versity (Tt) divided by mean alpha diversity Stratigraphic analysis shows that data sets are time, with the highest levels of endemism occur- (T) (Sepkoski, 1988). Vertical dotted line evenly spread through the study interval, and for ring in the following Asselian stage, before fall- highlights Moscovian-Kasimovian bound- each time bin, data sets are evenly distributed ing back to mid-Carboniferous levels by the ary. Time scale after Davydov et al. (2010). Abbreviations as in Figure 1. west and east of the Appalachians that divided Artinskian (Fig. 2C). the paleoequatorial zone (Fig. 1). A complementary picture of diversifi cation is Global and alpha curves were plotted to expressed by the ecological diversity data. The by the Asselian and, although piscivores and analyze the separate diversifi cation patterns number of ecological niches occupied by tetra- insectivores of most sizes were diverse in pre- as well as to calculate the degree of endemism pods increased from four in the Visean to nine Kasimovian strata, there were no confi rmed car- nivores or herbivores. Following the Moscovian- Kasimovian boundary, a diversity of medium and large carnivores (9%) and herbivores (5%) evolved, resulting in a more modern proportion- ing of diet ratios (Fig. 3A). Ecological diversi- fi cation was especially marked among reptiles, which occupied eight niches, seven of which were gained after the implosion, compared to only one gained by amphibians (Table 1).

DISCUSSION: RAINFOREST COLLAPSE AND TETRAPOD EVOLUTION It is now well established that climate fl uc- tuations profoundly infl uenced Carboniferous Coal Forests (Montañez et al., 2007). In earli- est Kasimovian time, an extreme glacial phase (Heckel, 1991) or greenhouse warming (Bishop Figure 1. Data distribution. A: By paleogeography (300 Ma; after Scotese and McKerrow, 1990). B: By stratigraphy. Open circles are global data and closed circles are alpha data. et al., 2010) led to hyperconstriction of the VIS—Visean; SPK—Serpukhovian, BSH—Bashkirian, MOS—Moscovian, K—Kasimovian, Coal Forests and fragmentation into rain forest G—Gzhelian, A—Asselian, SAK—, ART—Artinskian, Apps—Appalachians. islands, a state from which they never fully

1080 GEOLOGY, December 2010 ian groups that had evolved in the there were still 28 families compared (Benton, 2005; Coates et al., 2008). Key taxa to 11 reptile families), the ecological diversity of included temnospondyls (small- to large-sized reptiles was much greater, with some families fi sh eaters with broad, fl at skulls), lepospondyls occupying multiple niches (Table 1). Amphib- (small, aquatic nectrideans and terrestrial micro- ians maximally occupied six ecological niches saurs, some of which fed on insects), and reptili- after the alpha implosion, while reptiles occu- omorphs (mostly terrestrial anthracosaurs). In pied eight, seven of which were gained after the Bashkirian time, this latter clade also gave rise implosion, compared to only one by amphibians. to the fi rst amniotes (‘reptiles’). This ecological shift was primarily related to The abrupt alpha implosion in the Kasimo- diet. Pre-Kasimovian amphibians and reptiles vian-Gzhelian interval (Fig. 2) appears to have largely fed on fi sh (~70%), presumably refl ect- been selective, with amphibians hardest hit. ing the aquatic origin of tetrapods, while the Globally, amphibians that became extinct at the proportion of insectivores gradually increased Figure 3. Global ecological diversity of tet- Moscovian-Kasimovian boundary included the through this interval, refl ecting greater rapods from Visean (346 Ma) to Artinskian (270 Ma). Time scale after Davydov et al. basal tetrapod families Baphetidae and Colos- abundance, size, and diversity. However, fol- (2010). Abbreviations as in Figure 1. teidae, the microsaur families Microbrachidae, lowing rainforest collapse, diet ratios changed Hyloplesiontidae, and Odonterpetontidae, the markedly. While amphibians continued to feed temnospondyl family Dendrerpetontidae, and on fi sh and insects, reptiles began exploring recovered (DiMichele et al., 2009). By the end the reptiliomorph families Gephyrostegidae, two new food types, tetrapods (carnivory), and of the Kasimovian, Coal Forest remnants were Anthracosauridae, and Solenodonsauridae. later, plants (herbivory). This ecological diver- restricted to tiny wet spots in a seasonally dry Although three of these families were rep- sifi cation refl ected adaptations by tetrapods to landscape (DiMichele et al., 2006). Patterns resented by a single taxon, the other six were maximize acquisition of limited resources in a of tetrapod diversity identifi ed here are best more diverse. Origination of 10 new amphibian fragmented habitat. explained in terms of a population response to families in the Kasimovian-Gzhelian interval, Carnivory was a natural transition from insec- this habitat fragmentation. including the temnospondyl families , tivory for medium and large tetrapods, and it The impact of habitat fragmentation on diver- Trematopidae, and Trimerorhachidae, balanced required minimal adaptation. In contrast, a com- sifi cation was fi rst highlighted by MacArthur these losses, but the distribution of new taxa was plex set of adaptations was necessary for feed- and Wilson’s (1967) theory of oceanic island endemic, not cosmopolitan, as earlier. ing on highly fi brous materials, requiring biogeography. However, this concept can be By contrast, amniotes underwent no loss of structural modifi cations to the teeth, jaws, and extended to explain any ecosystem surrounded families, continuing to diversify into the Art- digestive tract as well as formation of endo- by differing ecosystems, whether it comprises inskian. In particular, the , symbiotic relationships with microbes to aid in rainforest refugia or landscapes altered by and related basal families, dominated digestion (Sues and Reisz, 1998). Only a small (e.g., traffi c island biogeography; Whit- Early Permian terrestrial red bed assemblages. proportion of extant tetrapods are obligate her- more et al., 2002). The initial impact of frag- The relative success of amniotes following bivores. Many extant carnivores also consume mentation is usually devastating, with most life rainforest collapse probably refl ects their two low-fi ber plant material as well as insects and rapidly dying out from restrictions on resources. unique adaptations, i.e., hard-shelled eggs that fi sh (e.g., ), so it could be that early tet- Then, as animals reestablish themselves, they could be laid on dry land and protective scales rapods made the transition to fully fl edged her- adapt to their restricted environment to take that helped retain moisture; these key adapta- bivory by way of omnivory. advantage of the new allotment of resources. tions freed them from the aquatic habitats to Kasimovian-Gzhelian tetrapods that fed on Thus, our data, which show elevated extinc- which amphibians were tied and gave them eco- high-fi ber plants include and Eda- tion rates, increased endemism, and ecological logic advantage in the widespread drylands that phosaurus. In Early Permian time, several dis- diversifi cation, apparently represent a classic developed, beginning in late Pennsylvanian time tantly related lineages of amniotes were com- community-response to habitat fragmentation, (Falcon-Lang et al., 2007). pletely herbivorous, including the as discussed in the following. and the widespread . Herbivory Tetrapod Ecological Diversity and Diet emerged independently in several lineages in Tetrapod Taxonomic Diversity The marked ecological diversifi cation follow- the Kasimovian-Gzhelian and Permian (Sues Taxonomic analysis of our data reveals ing rainforest collapse was also highly selec- and Reisz, 1998), which is consistent with con- important subtleties not evident from inspec- tive, with reptiles preferentially moving into vergent evolution within a fragmented habitat. tion of diversity curves alone. Ecosystems that new niches. Although global familial diversity A similarly marked increase in the incidence of developed prior to rainforest collapse were of amphibians was several times larger than for herbivory is also seen among arthropods in the highly cosmopolitan and dominated by amphib- reptiles (by the Artinskian this gap was less, but Kasimovian-Gzhelian, and an additional factor governing this change may have been the rise to dominance by tree ferns, which were relatively TABLE 1. NICHES, A COMBINATION OF DIET AND BODY SIZE OCCUPIED BY AMPHIBIANS AND “REPTILES” BEFORE AND AFTER THE ALPHA IMPLOSION cheaply constructed and therefore more digest- ible (Labandeira, 2006). Piscivores Insectivores Browsers Predators Total Total niches families SML SML SML SML Paleoenvironmental Data BAS-MOS amphibians Y Y Y Y Y 5 23 Our hypothesis that Coal Forest collapse K-G amphibians Y Y Y Y Y Y 6 24 drove tetrapod diversifi cation is confi rmed by BAS-MOS reptiles Y 1 2 facies analysis of tetrapod-bearing sites. The K-G reptiles Y Y Y Y Y Y Y Y 8 5 most complete assemblages preceding the Note: S—small; M—medium; L—large; BAS-MOS—Bashkirian-Moscovian; K-G—Kasimovian-Gzhelia. earliest Kasimovian event (, Jarrow,

GEOLOGY, December 2010 1081 Newsham, Linton, and Nyrany) are all associ- Carboniferous elements in Early Permian trop- the late Paleozoic in time and space: ated with coal-bearing successions. Specifi cally, ical fl oras, in Greb, S.F., and DiMichele, W.A., Geological Society of America Special Paper all occur in sedimentary deposits formed under eds., through time: Geological Soci- 441, p. 275–289, doi: 10.1130/2008.2441(19) . ety of America Special Paper 399, p. 223–248, Labandeira, C.C., 2006, The four phases of plant- humid interglacial climates when Coal Forests doi: 10.1130/2006.2399(11) . associations in deep time: Geológica were at their maximum areal extent (Falcon- DiMichele, W.A., Falcon-Lang, H.J., Nelson, J., El- Acta, v. 4, p. 409–438. Lang and DiMichele, 2010), comprising a new rick, S., and Ames, P., 2007, Ecological gradi- Labandeira, C.C., and Sepkoski, J.J., Jr., 1993, Insect continuous belt from to . 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W.A., Frank, T.D., Fielding, C.R., Isbell, J.L., DiMichele, W.A., Cecil, B., Montanez, I.P., and Birgenheier, L.P., and Rygel, M.C., 2007, CO2- ian environments comprised even more wide- Falcon-Lang, H.J., 2010, Cyclic changes in forced climate and vegetation instability during spread seasonally dry areas with highly frag- Pennsylvanian paleoclimate and it effects on late Paleozoic deglaciation: Science, v. 315, mentary habitats in which communities were fl oristic dynamics in tropical : Interna- p. 87–91, doi: 10.1126/science.1134207. restricted to small isolated wet spots (DiMichele tional Journal of Coal Geology, doi: 10.1016/j Munk, W., and Sues, H.-D., 1992, Gut contents of .coal.2010.01.007 (in press). Parasaurus (Pareiasauria) and Protorosaurus et al., 2006). Falcon-Lang, H.J., 2004, Pennsylvanian tropical () from the rainforests responded to glacial-interglacial (Upper Permian) of Hessen, Germany: Paläon- ACKNOWLEDGMENTS rhythms: Geology, v. 32, p. 689–692, doi: 10.1130/ tologische Zeitschift, v. 67, p. 169–176. Sahney appreciates Paul Ferry’s continued techni- G20523.1. Pfefferkorn, H.W., and Thomson, M.C., 1982, Changes cal support. Benton is supported by Natural Environ- Falcon-Lang, H.J., and DiMichele, W.A., 2010, in dominance patterns in Upper Carbonifer- ment Research Council (NERC) grant NE⁄C518973/1, What happened to the Coal Forests during ous plant fossil assemblages: Geology, v. 10, and Falcon-Lang by NERC Advanced Postdoctoral glacial phases?: Palaios, v. 25, doi: 10.2110/ p. 641–644, doi:10.1130/0091-7613(1982)10<641 Fellowship NE/F014120/2. palo.2009.p09-153r (in press). :CIDPIU>2.0.CO;2. 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