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Confirmation of Romer’s Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization

Peter Ward*†, Conrad Labandeira‡§, Michel Laurin¶, and Robert A. Berner†ʈ

*Department of Biology, University of Washington, Seattle, WA 98195; ‡Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012; §Department of Entomology, University of Maryland, College Park, MD 20742; ¶Formations de Recherche en E´ volution 2696, Centre National de la Recherche Scientifique, Universite´Paris 6–Pierre et Marie Curie, Two Place Jussieu, Case 7077, 75005 Paris, France; and ʈDepartment of Geology and Geophysics, Yale University, New Haven, CT 06520-8109

Contributed by Robert A. Berner, September 12, 2006 The first terrestrialization of species that evolved from previously alians disappeared soon thereafter, followed rapidly by rare aquatic taxa was a seminal event in evolutionary history. For appearances of limbed vertebrates. This temporal gap has long vertebrates, one of the most important terrestrialized groups, this been called Romer’s Gap, and until recently it was unknown event was interrupted by a time interval known as Romer’s Gap, whether this hiatus was due to a combination of unfavorable for which, until recently, few fossils were known. Here, we argue taphonomic conditions and collection failure or whether it that geochronologic range data of terrestrial arthropods show a represented an interval of intrinsically low diversity and an pattern similar to that of vertebrates. Thus, Romer’s Gap is real, abundance of limbed vertebrates. Romer’s Gap separates occupied an interval from 360 million years before present (MYBP) occurrences of the earliest (Late ) aquatic stego- to 345 MYBP, and occurred when environmental conditions were cephalians from a much larger adaptive radiation that included unfavorable for air-breathing, terrestrial . These model the first terrestrial vertebrates that commenced during the results suggest that atmospheric oxygen levels were the major Visean stage of the Early . Although new col- driver of successful terrestrialization, and a low-oxygen interval lections have partly filled Romer’s Gap (9), including the accounts for Romer’s Gap. Results also show that terrestrialization discovery of the early limbed vertebrate Pederpes, our recent among members of arthropod and vertebrate clades occurred in findings suggest that it is not collection failure that has resulted two distinct phases. The first phase was a 65-million-year (My) in this near absence of limbed vertebrate occurrences. Here, interval from 425 to 360 MYBP, representing an earlier, prolonged we test the hypothesis that Romer’s Gap is accounted for by event of complete arthropod terrestrialization of smaller-sized environmental factors by examining the ranges of terrestrial forms (425–385 MYBP) and a subsequent, modest, and briefer arthropods over the same time interval. event of incipient terrestrialization of larger-sized, aquatic verte- Until now there has been little attention to whether terrestrial brates (385–360 MYBP). The second phase began at 345 MYBP, arthropods also show an equivalent of Romer’s Gap. Romer’s characterized by numerous new terrestrial species emerging in Gap (10, 11) was a time designation heretofore applied only to both major clades. The first and second terrestrialization phases the fossil record of stegocephalians, whose original definition is bracket Romer’s Gap, which represents a depauperate spectrum of the one used herein. However, arthropodan data can provide major arthropod and vertebrate taxa before a major Late Paleozoic new information and insight into environmental conditions colonization of terrestrial habitats. during the Devonian to Carboniferous time interval. Results atmospheric O2 ͉ Paleozoic ͉ The first terrestrialized macroscopic eumetazoans can be used to estimate standing diversity from 425 MYBP, just before the he pattern of terrestrialization by animals as recorded in Ϸ Tthe fossil record (1) indicates that arthropods, with species earliest arthropod fossils (2), to 280 MYBP (Fig. 1), the latter interpreted as fully land-based before 400 million years before a time of recognized high diversity in both arthropods and present (MYBP) (2), preceded vertebrates onto land by tens of terrestrial vertebrates (12, 13). For this interval we plotted the millions of years. The first body fossils identified as stego- geochronologic ranges and standing diversities of major, ter- cephalians (limbed vertebrates) are known from strata Ϸ370 restrialized early arthropod and vertebrate clades (Figs. 1 and MYBP, such that the appearance of the limb with digits, the 2). Clades for arthropods consisted of myriapods, arachnids loss of the opercular apparatus, and the development of other and hexapods, whereas those for vertebrates comprised stego- characters that subsequently allowed a terrestrial lifestyle, cephalians. Because of a great abundance of arthropod taxa, presumably occurred during the 25-My interval between 385 the origination rate of arthropod orders additionally was and 360 MYBP (3, 4). Most of our understanding about these determined, based on taxonomic orders (Fig. 2). Also docu- crucial vertebrate events comes from only a few freshwater mented during this interval are wide fluctuations in atmo- deposits from Euramerican localities, with outcrops in Green- spheric O2 levels, shown in Fig. 1, that are defined in greater land producing the most prolific stegocephalian remains. detail in Fig. 2. Elginerpeton and Obruchevichthys were first, between 385 and A plot of the recently computed atmospheric O2 levels against diversity data for major clades of arthropods and limbed verte- 375 MYBP, followed several million years later by a modest radiation that included Ventastega, Ichythostega, Acanthostega, Tulerpeton, Metaxygnathus, and Hynerpeton. Although most of Author contributions: P.W. designed research; P.W., C.L., M.L., and R.A.B. performed these taxa possessed limbs (although this is not certain for research; and P.W., C.L., M.L., and R.A.B. wrote the paper. Elginerpeton and Obruchevichthys), all of these taxa have been The authors declare no conflict of interest. interpreted as fully aquatic, rather than terrestrial (5–7). Their Abbreviations: MYBP, million years before present; My, million years. respiratory systems are poorly known, but osteology suggests †To whom correspondence may be addressed. E-mail: [email protected] or robert. that they were able to derive some amount of O2 from water [email protected]. instead of being entirely air breathing (8). These stegoceph- © 2006 by The National Academy of Sciences of the USA

16818–16822 ͉ PNAS ͉ November 7, 2006 ͉ vol. 103 ͉ no. 45 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0607824103 Downloaded by guest on September 23, 2021 Weigeltisauridae Prolacertiformes "Romer's Therapsida Gap" Lysorophia Seymourimorpha Varanopidae Limbed Vertebrates Araeoscelidia Edaphosauridae Diadectomorpha Gephyrostegidae Protothyrididae Nectridea "Microsaurs" Embolomeri Aistopoda Adelogyrinidae Baphetidae Whatcheeriidae Colosteidae Hynerpeton Densignathus Acanthostega Ichthyostega Tulerpeton Ventastega + Metaxygnathus Elginerpetontidae

Geophilomorpha Spirostrepida Sphaerotheriida Callipodida Polyzoniida Pleurojulida Amynilyspedida Euphoberiida

Myriapods Arthropleurida Anthracodesmus Scolopendromorpha Microdecemplicida Devonobiomorpha Archidesmida Julida Lithobiomorpha Xyloiuloidea Paleodesmus Eoarthropleurida Scutigeromorpha Zosterogrammida Cowiedesmida O 2

Amblypygi Phalangotarbida Solifugi Uropygi

Arachnids Ricinulei Mesothelae Opiliones Haptopoda Actinotrichida Pseudoscorpionida Attercopus Xenarachne Actinedina Scorpionida Trigonotarbida

Grylloblattida

Psocoptera GEOLOGY Permothemistida Odonata Land Colonizations: Protelytroptera Phase 1A Lophioneurida Phase 1B Glosselytrodea Phase 2 Planipennia Coleloptera Plecoptera Hexapods Hemiptera Miomoptera “Hypoperlida” Orthoptera Caloneurodea Diplura Megasecoptera “Protoperlaria” EVOLUTION Ephemeroptera Geroptera “Protoblattodea” Protodonata Palaeodictyoptera Diaphanopterodea Archaeognatha Collembola Rhyniognatha Ordo Devonian Carboniferous Penn. Late Early LM Early Mid Late Early Middle LEML Lower 440 420 400 380 360 340 320 300 280

Fig. 1. Geochronologic range data, using the range-through method (31), for terrestrial arthropod and vertebrate clades over the study interval. Romer’s Gap is shown in green. Major arthropod clades (Myriapoda, Arachnida, and Hexapoda) are divided into subclades at the ordinal or approximately equivalent rank; limbed vertebrates are subdivided into clades mostly of lesser rank. Two separate colonizations onto land are present. Phase 1 (425–360 MYBP) involved an earlier event consisting of arthropods (Phase 1A; 425–385 MYBP; yellow field), and a subsequent event by vertebrates (Phase 1B; 385–360 MYBP; tan field), consisting of the first aquatic to perhaps semiterrestrial limbed vertebrates. The colonization event of Phase 2 (345 MYBP to Early Permian; brown field) comprises new major originations and radiations of terrestrialized arthropods and limbed vertebrates. Values for atmospheric O2 are given as midpoints for 10-My bins (see Fig. 2); increasing O2 level is toward the top, with the present atmospheric level of 21.0% indicated by a horizontal dotted line. Ordo, ; Penn, ; E, Early; M, Middle; L, Late. Taxa in quotation marks are probably not monophyletic; geochronologic scale is from ref. 37. For documentation of vertebrate taxa, see the Appendix, which is published as supporting information on the PNAS web site.

Ward et al. PNAS ͉ November 7, 2006 ͉ vol. 103 ͉ no. 45 ͉ 16819 Downloaded by guest on September 23, 2021 New Arthropod Orders Oxygen Arthropods Limbed (per 10 million years) Ma Vertebrates

290 – Present 300 – Oxygen Level 310 –

320 –

330 –

340 –

350 – "Romer's Gap" 360 –

370 –

380 –

390 –

400 –

410 –

420 –

430 –

440 –

450 –

0 5 10 15 10 15 20 25 30 0 10 20 30 40 0 25 50 75 100 Percent Atmospheric Oxygen Orders Species

Fig. 2. Ordinal-level diversity data for arthropods from Fig. 1, shown in 10-My bins, plotted against atmospheric O2 levels as computed with the GEOCARBSULF model and Ϯ3% error margins. Over the study interval O2 levels rise significantly above 21% (present level), then subside to Ͻ15%, before a subsequent and sustained increase. The first event of Phase 1 land colonization by arthropods apparently is tied to rising atmospheric O2 with a slight time lag. Although both arthropod and limbed vertebrate clades survive the low-O2 interval, they do so at low standing diversity, are composed of long-lived taxa, and are significantly supplemented by the emergence of minimally terrestrialized vertebrate clades in the second event of Phase 1 (from Fig. 1). Most revealing is that no new arthropod and very few stegocephalian taxa originate during the low-O2 interval. A more dramatic Phase 2 of land colonization is linked to a second, more elevated rise in atmospheric O2. Data are plotted as midpoints within 10-My bins.

brate taxa (Fig. 2) indicates that an increase in origination rate from 425 to 400 MYBP, although the diversification of more of new arthropod orders lagged Ϸ10 My behind a significant rise crownward vascular plant lineages continued into the mid- in maximal O2 levels (Ͼ20%) during Ϸ435–400 MYBP. No Devonian to Ϸ370 MYBP (17, 18). Arthropod of terrestrialization of arthropods occurred before O2 levels reach- these tracheophyte producers (19) as well as their trophically ing 20%, slightly less than the present level. The subsequent drop superjacent consumers consisted of three major arthropod in O2 was followed by extinction of major arthropod clades, with clades that originated approximately at the same time and all survivors belonging to long-lived lineages. No new clades forever structured terrestrial ecosystems (2). These clades are appeared during the O2 minimum, the interval that largely myriapods, arachnids, and hexapods, although fungi also con- coincides with Romer’s Gap. This interval of 360–345 MYBP tributed a major role by providing intimate saprobic associa- was preceded by the significant Frasnian to Fammenian (Late tions with both plants and arthropods (13, 20). Among initially Devonian) mass extinction (375 MYBP), long interpreted to radiating myriapods were diverse centiped, milliped, and have been accompanied by (or perhaps caused by) periods of arthropleurid clades, some of uncertain affinities (21, 22). oceanic anoxia (14). These O2 data indicate that this interval of Arachnid clades prominently included aerially respiring scor- time also showed significantly lower levels of atmospheric O2 pions, trigonotarbids, pseudoscorpions, two mite lineages, and than occur today or was present earlier. Further evidence of the earliest spiders (23), representing a broad spectrum of these lower levels is shown by independent calculations based on high-ranked taxa. By contrast, there is minimal evidence for a rock abundance (15). Subsequently, diversification of terrestrial hexapod radiation, consisting of only collembolans and bristle- arthropods and vertebrates, also reflected in the appearance of tails (2), albeit there is indirect evidence that perhaps winged new taxa, became associated with an increase in O2 commencing insects were present (24). Based on Late Silurian to Middle Ϸ380 MYBP. This O2 increase exceeded the present level of 21% Devonian fossil occurrences and cladistic sister-group rela- at Ϸ335 MYBP and reached a subsequent peak of diversity, tionships with extant taxa, these four major groups of organ- which coincided with maximum O2 levels often associated with isms, tracheophyte plants, myriapods, arachnids, and hexa- arthropod gigantism (16). pods, indicate the early establishment of major body plans assignable to terrestrial taxa and thus an early arthropod event Discussion (425–385 MYBP) within Phase 1 of land colonization by The earliest macroscopic bryophyte-like and tracheophyte macroscopic but relatively small-sized animals. Currently, plants are assignable to taxa found from a relatively con- there is minimal evidence for a robust pattern of early strained Late Silurian to Early Devonian interval centered diversification for hexapods. Ecological data also is supportive

16820 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0607824103 Ward et al. Downloaded by guest on September 23, 2021 by documenting an early event of initial arthropod herbivory during the Late Silurian to Early Devonian; for larger-sized on spores and stems soon after these organs originated on vertebrates, the origin of amphibious structures immediately several host-plant lineages (19, 25). However, there is no before Romer’s Gap; and for both groups, the subsequent and evidence for truly terrestrial vertebrates during this first phase attendant consequences for occupying new land-based habitats of colonization. by large-sized taxa during the Middle Mississippian to Lower The second, more modest event (385–360 MYBP) within Permian. Phase 1 of colonization occurs immediately before Romer’s We conclude that terrestrialization of macroscopic Paleo- Gap and is illustrated by the first appearance of larger-sized zoic animals took place during two phases. Additionally, major stegocephalian vertebrates exhibiting amphibious features, arthropod origination and diversification occurred during both mentioned previously, and also monilophyte (‘‘fern’’) plant phases, whereas vertebrate expansion on land coincided with clades as well as a few stem-group seed-plant clades (26) the second phase. This pattern is partly attributable to signif- toward the end of the interval (18). Immediately at the end of icant changes in atmospheric O2 and toward achieving opti- Romer’s Gap and continuing into the Early Permian is Phase mality of respiratory organs in air. While mass extinc- 2, comprising an elevated number of terrestrialized arthropod tion and recovery, accommodation to new habitats, and body- taxa. During this event (345 MYBP; carboniferous), 18 major plan modernization have all been factors in the evolution of land arachnid and myriapod taxa appeared, but more dramatic life, atmospheric O2 level also has been a major, if underap- was the geochronologically delayed and sudden appearance of preciated, driver in the major features of life’s history. These 8 insect clades and soon thereafter an additional 4 clades by the features include origination, diversity levels, and probably end of the subperiod. This diversification event of modest- to absolute size increases through time. This phenomenon has larger-sized arthropods included all major trophic groups, been demonstrated for other time intervals (29, 30) and now carnivory and detritivory (heavily represented during the first is shown for the period representing the first colonizations of phase), but especially the varied life habits within herbivory, land by macroscopic organisms. One implication for animal including the consumption of live tissues of roots, leaves, and response to increasing O2 levels, herein tested by replicates seeds and wood (13, 19, 25). Specifically, herbivores parti- representing four major independently terrestrialized animal tioned live plant tissue based on functional feeding group clades, is whether a critical, minimal threshold level of atmo- throughout the Pennsylvanian Subperiod, during which exter- spheric O2 content must be realized for animal life of a given nal foliage feeders, piercer-and-suckers, gallers, pith borers, size range before colonization of land is possible. and palynivores appeared (19, 25). The presence of two separate phases of arthropod diversifi- Methods cation on either side of Romer’s Gap, but with long-ranging taxa Establishing Arthropod and Vertebrate Diversity. Our procedure common to both intervals, argues against the gap being a initially was to divide the 165-My interval from 425 My ago taphonomic artifact or period of undersampling. New data from (Ma) (Middle Silurian: Wenlock) to 280 Ma (later Early herbivory, such as the earliest example of insect folivory from the Permian: mid-) into 10-My bins. Global occurrences Late Mississippian preceding a reasonably ascribed culprit by 6 of monophyletic arthropod clades at the ordinal or approxi- My (25), supports the inference from taxonomic range data that mately equivalent rank, as well as vertebrate clades occurring arthropods were present, but at low diversities, rather than at lower rank (typically families and monotypic genera), were representing a sampling artifact from an inadequate fossil extracted from the literature and then allocated to appropriate record. bins (Fig. 1). The range-through method (31) was used to Romer’s Gap ends with a significant radiation of new land establish geochronologic lineage durations throughout inter- plant, arthropod, and stegocephalian taxa beginning Ϸ345 vals bracketed by first occurrences and last appearances, the MYBP but undergoing its highest rate of new species appear- latter including the end- cut-off for our data. Ar- ances after 335 MYBP. As in the first event of early arthropod thropod and vertebrate standing diversities and arthropod diversification during Phase 1, the second diversification took origination values were plotted as interval midpoints per GEOLOGY place soon after a steady and significant rise in O2 beginning Ϸ80 10-My bins in Fig. 2. Calculated atmospheric O2 values were MYBP but not reaching present-day levels until immediately plotted in the same manner, given as means in Fig. 1 and with after 340 MYBP. This second and larger diversification of Ϯ3% error margins in Fig. 2. increasingly larger-bodied arthropods accompanies the rise of O2 when it again exceeds the 20% level. Truly terrestrial Calculation of Atmospheric O2 Levels. Models based on analyses of vertebrates also diversify at this time, with both groups reaching the isotopic composition of carbon and sulfur (32, 33) or on the maximal diversity in our study (orders or equivalent taxa of relative abundance of different rock types (15) suggest that arthropods and species of stegocephalians) at Ϸ295 MYBP. atmospheric O2 concentrations varied throughout the Pha- EVOLUTION What caused these biphasic terrestrial radiations separated by nerozoic, with a maximum at Ϸ290 MYBP, a minimum at Ϸ15 My? Here we propose that atmospheric O2 levels were the Ϸ200 MYBP, and an overall rise from Ϸ200 MYBP to present. major determinant of the observed evolutionary pattern. Our These models suggest that that since the , O2 levels data indicate that the 20% O2 level represents an evolutionary (in terms of mass) have varied by a factor of three. The threshold for both arthropods and vertebrates. In the Paleozoic GEOCARBSULF model (34) is a combination of earlier transition to land, both arthropods from several lineages (refs. 13 GEOCARB models for CO2 and the isotope mass balance and 27, but see also ref. 28) and vertebrates (7) replaced gills with model for O2. GEOCARBSULF is a computer model that tracheae and lungs. This transition surely involved primitive takes account of the major factors thought to influence lungs or analogous structures (27) that may have been inefficient atmospheric O2 and CO2. These models account for ‘‘forc- for sufficient O2 extraction at levels lower than present. This ings,’’ which are processes that affect the levels of these gases, suboptimality of respiratory structures in air may explain why used in our calculations. Principal forcings for O2 are burial of vertebrates did not become land dwellers before Romer’s Gap. organic matter and pyrite (FeS2) in sediments, their weather- Problems included not only acquiring O2, but the consequential ing on the continents, and rates of metamorphic and volcanic problem of eliminating of CO2, a process more difficult in air degassing of reduced carbon and sulfur-containing volcanic than in water. However, benefits would have included an op- gases, such as sulfur dioxide. Thus, for our estimates, a major portunity for greater body-size increases, perhaps modulated by factor significantly affecting these rates during the Paleozoic the 10-My lag behind an atmospheric O2 rise for arthropods was the colonization of land by plants and their subsequent

Ward et al. PNAS ͉ November 7, 2006 ͉ vol. 103 ͉ no. 45 ͉ 16821 Downloaded by guest on September 23, 2021 evolution providing a vastly increased rate of organic matter significant drop in oxygen found in an earlier study (15) has burial in the form of biologically resistant lignin (35). In- been reconfirmed. creased organic burial, reflecting augmented net photosyn- thesis (photosynthesis minus respiration), caused an increase We thank D. Ehlert and F. Marsh for drafting the figures and M. Carrano in atmospheric O2 during the mid-to-late Paleozoic (36). for commentary. This work was supported by the National Aeronautics Recently, new carbon isotope data has become available (34), and Space Administration (NASA) Astrobiology Institute (P.W.) and results of which have allowed refinements of previous model the Department of Energy (R.A.B.). This article is contribution 153 of findings, especially for the early Paleozoic through Mesozoic the Evolution of Terrestrial Ecosystems Consortium at the National interval. Most crucially for the work reported here, the Museum of Natural History, Washington, DC.

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