The delayed resurgence of equatorial forests after the Permian–Triassic ecologic crisis C. V. Looy*†, W. A. Brugman*, D. L. Dilcher‡, and H. Visscher* *Laboratory of Palaeobotany and Palynology, Utrecht University, Budapestlaan 4, 3584 CD Utrecht, The Netherlands; and ‡Paleobotany Laboratory, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611 Contributed by D. L. Dilcher, September 22, 1999 In conjunction with the Permian–Triassic ecologic crisis Ϸ250 mil- the Olenekian and Anisian Stages. In Europe, a continuous lion years ago, massive dieback of coniferous vegetation resulted shallow marine Olenekian–Anisian transition sequence is par- in a degradation of terrestrial ecosystems in Europe. A 4- to ticularly well developed in the Transdanubian Central Range in 5-million-year period of lycopsid dominance followed, and re- Hungary (20, 21). The boundary approximates the transition newed proliferation of conifers did not occur before the transition between the marls and limestones of the Csopak Marl Formation between Early and Middle Triassic. We document this delayed and the lagoonal dolomites and marls of the Aso´fo˝ Dolomite re-establishment of equatorial forests on the basis of palynological Formation. In outcrops, the Csopak Marl Formation yields the data. The reconstructed pattern of vegetational change suggests Tirolites ammonoid fauna, indicative of the Spathian Substage of that habitat restoration, migration, and evolutionary processes acted the Olenekian. Continuously cored exploration wells have en- synergistically, setting the stage for successional replacement of abled detailed biostratigraphic analysis of marine and land- lycopsid dominants by conifers within a period of Ϸ0.5 million years. derived palynomorphs (20–23). Quantitative distribution pat- terns of spore and pollen types (Fig. 1) are obtained from nderstanding of patterns and processes of past ecologic samples of borehole Bakonyszu˝cs-3. Information on the botan- Ucrises is no longer a matter of purely academic interest. ical affinity of the types is summarized in Table 1. Studies of biotic and biogeochemical change related to mass Immediately apparent is the overwhelming abundance of extinction events may substantially contribute to a prediction of Densoisporites nejburgii in the lower part of the Csopak Marl ECOLOGY the long-term consequences of current man-induced environ- Formation, indicative of the Pleuromeia monocultures known mental deterioration and its associated biodiversity decline (1, from Olenekian megafossil records in Europe. Selaginellales and 2). In making such a contribution, we should focus on the other pteridophytes are subordinate elements. In the upper part potential of high-resolution analysis of distinctive survival and of the Csopak Marl Formation, gradual shifts in relative abun- recovery phases after episodes of global ecosystem collapse (3). dances give a straightforward picture of the sequence of the At present, conceptual models of survival and recovery are gymnosperm invasions. Initial invasion was by the conifer Yuc- notably constrained by a variety of marine paleoecologic records cites, as reflected by the coming and proliferation of Voltziace- (3–6). However, because of its role in global biomass storage and aesporites heteromorphus. Additional elements followed, includ- its sensitivity to environmental change, land vegetation is one of ing the possibly ullmanniaceous conifer that produced Jugas- the most obvious biota to be investigated for patterns of survival porites conmilvinus. The lycopsid component declines drastically and recovery. Notably, the aftermath of the unrivaled Permian– and disappears from the record in the basal part of the Aso´fo˝ Triassic (P–Tr) crisis (7, 8) should serve as a valuable field of Dolomite Formation. The decrease in Voltziaceaesporites and botanical inquiry. Jugasporites, and a simultaneous increase in Triadispora and At the very end of the Permian, dieback of woody vegetation other coniferous pollen, mark the onset of the Voltzia-dominant dramatically affected terrestrial ecosystems (9–12). In the north- climax vegetation of the Anisian. ern and southern humid climatic zones of Pangaea, it resulted in The general trend observed in compositional change between Densoisporites-dominant and Triadispora-dominant assemblages the widespread disappearance of peat forests (13, 14). In the is consistent with coeval (semi) quantitative palynological semi-arid equatorial region, the dominant conifer taxa of the records from outcrops and boreholes in many parts of Europe, Late Permian Euramerican floral realm became extinct at, or northern Africa, and Israel (Fig. 2). The pollen and spore close to, the P–Tr junction (15). Among the surviving plants, assemblages originate from both terrestrial (lacustrine, fluvia- lycopsids played a central role in repopulating the initial eco- tile) and shallow marine sequences. They are invariably domi- logical desert. Subsequent radiation and expansion among nated by allochthonous elements, thus reflecting changes in Isoetales (16) resulted in dense populations of the succulent regional vegetation. Because of long-distance (wind, river) dis- quillwort Pleuromeia sternbergii (17). persal, the assemblages include a regionally derived mixture of Throughout Europe, plant megafossil information indicates pollen and spore types originating from both lowland and upland that ecosystem recovery to precrisis levels of structure and communities (24). The most complete comparative records are function did not occur before the transition between the Early from boreholes in Poland (25, 26). and Middle Triassic. A replacement of the Pleuromeia vegetation Despite the difference in temporal scale, the unidirectional Voltzia by coniferous forests is evidenced by the -dominant Early to Middle Triassic vegetation change in Europe mimics communities that characterize the early part of the Middle patterns of plant succession that occurred in response to the climate Triassic (17–19). In contrast to the discontinuous and qualitative amelioration at the beginning of the Holocene approximately plant megafossil record, successive pollen and spore assemblages 11,000 years ago. In both cases, palynological data indicate can provide the sample size and stratigraphic spacing needed to resolve the temporal pathway of plant succession during this recovery phase. Here, we document and discuss the delayed Abbreviations: P–Tr, Permian–Triassic; Ma, million years. return of woody plants in Europe on the basis of quantitative See commentary on page 13597. palynological data from an Early–Middle Triassic transition †To whom reprint requests should be addressed. E-mail: [email protected]. sequence in Hungary. The publication costs of this article were defrayed in part by page charge payment. This In current chronostratigraphic classification, the Early– article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. Middle Triassic junction corresponds to the boundary between §1734 solely to indicate this fact. PNAS ͉ November 23, 1999 ͉ vol. 96 ͉ no. 24 ͉ 13857–13862 Downloaded by guest on September 26, 2021 Fig. 1. Quantitative distribution patterns of selected spore and pollen types from the Early to Middle Triassic (Olenekian–Anisian) transition sequence in the Transdanubian Central Range, Hungary (borehole Bakonyszu˝cs-3, 6 km east of the town of Pa´pa; for location, see ref. 21). The diagram reflects the successional replacement of lycopsid-dominant by conifer-dominant vegetation. Horizontal lines represent samples. Relative abundances are expressed as percentages of total spore and pollen assemblage, and plus signs indicate rare, isolated occurrences. that the re-establishment of climax forests proceeds through representatives, both lycopsids and bryophytes could have been phases, in which herbs and shrubs are important functional preadapted to oligotrophic conditions. Earliest lycopsid pioneers members of the community. However, although rapid Holocene may have included both Selaginellales and Isoetales. Because of plant succession is notably regulated by habitat restoration and their successful radiation and expansion after P–Tr extinctions, migration (27), it is conceivable that the long-term pattern of the Isoetales may be classified as crisis progenitors (3–6), spe- Early to Middle Triassic succession is also influenced by evolu- cifically adapted to stressed environments of the Early Triassic tionary processes. Significant influences of climate change are survival phase. At least in Europe and other semi-arid regions, unlikely. Throughout the Late Permian, Early Triassic and such as northern China (29), the resulting widespread vegeta- Middle Triassic, terrestrial sedimentation in Europe is consis- tion, characterized by the relatively large succulent Pleuromeia tently dominated by the ‘‘Buntsandstein’’ redbed facies, indica- sternbergii, remained stable for a longer period of time. This tive of warm, semi-arid conditions. prolonged ecologic success of heterosporous lycopsids is remark- Under the prevailing semi-arid conditions, massive dieback of able and needs further investigation. Because of the unisexual woody vegetation in Europe is likely to have resulted in extensive gametophytes, free-sporing heterospory cannot be regarded as soil erosion. Early Triassic palynological data (Fig. 3) confirm an effective long-distance dispersal strategy in the water-limited the pioneering role for surviving lycopsids. Evidenced by the environments