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Examples of normal pollen grains in comparison with the range of malformation types observed in each of the 14 conifer species studied. Scales for each species represent 20 μm. For accession and specimen information notation see Supplementary Table 2. All specimens and specimen slides are housed in the University of California Museum of Paleontology in Berkeley, California, USA. Afrocarpus gracilior (Pilg.) Page: (1) normal, (2) fused sacci, (3) asaccate, (4) trisaccate, (5) conjoined dyad. Nageia nagi: (6) normal, (7) fused sacci, (8) asaccate, (9) trisaccate. Podocarpus totara: (10) normal, (11) fused sacci, (12) trisaccate, (13) tetrasaccate, (14) conjoined dyad. Dacrycarpus dacrydioides: (15) normal, (16) fused sacci, (17) asaccate, (18) tetrasaccate, (19) conjoined dyad, (20) unseparated triad, (21) conjoined tetrad. Phyllocladus trichomanoides: (22) normal, (23) asaccate, (24) tetrasaccate, (25) conjoined dyad, (26) conjoined triad, (27) unseparated tetrad. Prumnopitys andina: (28) normal, (29) fused sacci, (30) asaccate, (31) trisaccate, (32) unseparated dyad, (33) unseparated triad. Lagarostrobos franklinii: (34) normal, (35) asaccate, (36) unseparated dyad, (37) unseparated triad. Manoao colensoi (Hook.) Molloy: (38) normal, (39) fused sacci, (40) asaccate, (41) conjoined dyad. Picea orientalis (L.) Link: (42) normal, (43) conjoined dyad. Cathaya argyrophylla: (44) normal, (45) fused sacci, (46) asaccate, (47) trisaccate, (48) unseparated dyad. Pinus parviflora Siebold & Zucc.: (49) normal, (50) fused sacci, (51) asaccate. Cedrus libani: (52) normal, (53) fused sacci, (54) unseparated dyad. Keteleeria evelyniana: (55) normal, (56) fused sacci, (57) trisaccate, (58) unseparated triad. Abies koreana: (59) normal, (60) fused sacci, (61) tetrasaccate, (62) unseparated triad, (63) unseparated tetrad.
Source publication
Pollen malformations have been proposed as a paleoenvironmental stress proxy. However, the frequency and variability of pollen malformations under near-optimal conditions and environmental stress, as well as their developmental origins, remain unclear. To bridge these gaps, we compared pollen malformation frequencies and assemblages of 14 extant co...
Context in source publication
Context 1
... distribution of pollen malformations in the different categories compared varies between genera. However, there is little discernible phylogenetic pattern in trait prevalence between genera within and between Pinaceae and Podocarpaceae, both qualitatively (Fig. 4) and quantitatively through comparing malformation assemblages in terms of relative abundance of malformation types (Fig. ...
Citations
... This condition can arguably make the parent plants more tolerant to external environmental stress (Levin, 1983), which may have secured the continued success and ecological resilience of the Cheirolepidiaceae during environmental perturbation (Kürschner et al., 2013;Gravendyck et al., 2020). Nevertheless, currently there is still no consensus about the real presence of a polyploid advantage as many recently formed polyploid species have higher extinction rates in response to recent environmental stress than their diploid relatives (Arrigo and Barker, 2012;Bencha et al., 2022). ...
The Early Jurassic Jenkyns Event (or Toarcian Oceanic Anoxic Event T-OAE) was an episode of global warming and C-cycle perturbation that affected both marine and terrestrial ecosystems, but the interplay between climate change and vegetation is not established in detail from sections outside of Europe. Here, abundance changes in spore-pollen assemblages from the lacustrine Anya succession in the Ordos Basin (North China) reveal a unique record of vegetation dynamics during the Jenkyns Event. Plant communities responded to the event with biodiversity losses and the reorganization of gymnosperm-dominated forests. Community-level shifts are observed from the Pliensbachian–Toarcian boundary, but the onset of the negative carbon excursion (NCIE) that marks the event is coeval with the most significant turnover: a switch from a high-diversity vegetation with conifers, seed ferns, cycads, bennettites and ferns to drought-adapted low-diversity flora with Cheirolepidiaceae. The demise of forests and lowland mire biomes resulted in deforestation with increased weathering and soil erosion that exacerbated the terrestrial ecosystem crisis already under stress from rising temperatures. Terrestrial recovery was initiated before the end of the Jenkyns Event with the resurgence of pioneer ferns and lycopsids that colonized disturbed habitats. Plant assemblages signal aridification at the onset of the event with frequent climatic oscillations and extreme weather patterns during the event itself. The main NCIE phase was preceded by a short-lived cooling phase in the earliest Toarcian. In the aftermath of the NCIE, Cheirolepidiaceae forests declined and a more stable biome developed with seed ferns and various conifers. This was contemporaneous with delta development and shallowing of the lake surrounded by lowland mires with ferns, clubmosses and horsetails. Comparison of floral patterns across the Jenkyns Event show that, although Cheirolepidiaceae dominated the event globally, there were differences in vegetation response between coastal and inland areas, and recovery patterns might differ regionally.
... It is conceivable that the specific mix can indicate different causes, such as hybridisation or environmental stress. Experimental results regarding malformations in modern conifer pollen also suggest the existence of such a signal (Benca et al., 2022). ...
... We infer that the abundance of aberrant Ricciisporites-type grains dispersed in upper Rhaetian strata of Eurasia was probably linked to physiological and reproductive changes in the peltasperm parent plant shortly before its extinction. Overall, various genetic, environmental, physiological, and pathological factors can contribute to the production of infertile or damaged pollen by tapetal cells (Tretyakova and Noskova, 2004;Benca et al., 2018Benca et al., , 2022Vajda et al., 2023). All these underlying causes of abnormal pollen production are plausible and possibly induced by the dramatic environmental upheavals around the close of the Triassic. ...
... There are numerous cases of pollen polymorphism or teratologies in fossil and extant gymnosperm and angiosperm microsporangiate organs (e.g., van Konijnenburg-van Cittert, 1971;Audran and Masure, 1978;Chen et al., 1989;Skvarla et al., 2005;Lindström et al., 1997;Dreyer and Van Wyk, 1998;Foster and Afonin, 2005;Kürschner et al., 2013; van de Fig. 5. Schematic reconstruction of a branch bearing Lepidopteris ottonis leaves, Antevsia zeilleri microsporophylls, and the 'normal' and 'aberrant' developmental pathways producing Cycadopites-and Ricciisporites-type pollen grains, respectively. Schootbrugge and Wignall, 2016;Benca et al., 2018Benca et al., , 2022Kvaček and Mendes, 2020;Baranyi et al., 2023;Zavattieri and Gutiérrez, 2023). Such variation is normally evident in the form of differences in pollen size, shape, wall thickness, ornamentation and development of sacci, but can also be expressed in striking dissimilarities in exine stratification. ...
... During the Smithian-Spathian boundary event (a late Early Triassic crisis in the wake of the end-Permian event), ~50% of spores and pollen were "malformed" across the negative δ 13 C org shift of this event in Pakistan (Galasso et al. 2022); and during the end-Permian crisis, 40% of the total assemblage co-occurring with the onset of the negative δ 13 C org shift were considered abnormal, indicating that the reproductive ability of the parent plants was inhibited (Hochuli et al. 2017). Spore/pollen mutagenesis during LIP events could have been caused by increased and lethal UV-B radiation as a result of stratospheric ozone depletion by halocarbon and aerosol emissions from LIP magmatism (Benca et al. 2018(Benca et al. , 2022, volcanic induced Hg-toxicity (or other heavy metals) (Lindström et al. 2019), and possibly acid rain (SO 2 ) and soil acidification (Hochuli et al. 2017;van de Schootbrugge et al. 2009) in addition to general environmental stress. ...
Terrestrial ecosystems are integral components of global carbon budgets and modulators of Earth’s climate. Emplacement of large igneous provinces (LIPs) is implicated in almost every mass extinction and smaller biotic crises in Earth’s history, but the effects of these and other large-scale magmatic events on terrestrial ecosystems are poorly understood. Palynology, the study of fossilized pollen and spores, offer a means to robustly reconstruct the types and abundance of plants growing on the landscape and their response to Earth crises, permitting predictions of the response of terrestrial vegetation to future perturbations. We review existing palynological literature to explore the direct and cumulative impacts of large-scale magmatism, such as LIP-forming events, on terrestrial vegetation composition and dynamics over geological time.
... Further, a wide range of factors are known to induce tapetal cells of modern plants to secrete excessive sporopollenin, resulting in orbicule formation and, in some cases, fusion of pollen into permanent tetrads (Gómez et al., 2015). These unusual levels of sporopollenin secretion may result from abnormal hormonal instructions to the tapetum, and such signals can be induced by environmental stresses, such as elevated levels of metabolically harmful chemicals, dust, UV light, or excessively high or low temperatures (Benca et al., 2022). ...
... Aberrant palynomorphs have been systematically observed in intervals of severe biotic crisis, e.g., at the Devonian-Carboniferous, Permian-Triassic, and Triassic-Jurassic boundaries (e.g., Visscher et al., 2004;Kürschner et al., 2013;Lindström et al., 2019;Marshall et al., 2020). Teratology can be the proxy for many stress factors, e.g., heat, drought (Bazhina et al., 2007;Noskova et al., 2009), ozone loss, increased ultraviolet-B (UV-B) radiation (Visscher et al., 2004;Benca et al., 2022), or heavy metal pollution (Mičieta and Murín, 1996;Hochuli et al., 2017;Lindström et al., 2019). Numerous heavy metals are toxic to the metabolic activity of plants and can damage their reproductive cycle, resulting in malformed sporomorphs and disturbed growth (Nagajyoti et al., 2010). ...
... While aberrant sporomorphs occur naturally, a heightened frequency of malformation is linked to external stress (Foster and Afonin, 2005). The natural baseline of aberrancy can be different for each taxon (Benca et al., 2022), but based on observation of living and fossil plants, exceedance of a 3%-5% benchmark is generally accepted as an indication of stressed conditions (Foster and Afonin, 2005). At Anya, asymmetrical Classopollis tetrads reach 6%-7% of the total Classopollis counts, and dwarfed spores reach up to a maximum of 23% of spores. ...
... Mutagenesis can be related to water and temperature stress (Bazhina et al., 2007;Noskova et al., 2009), high UV-B radiation (Benca et al., 2022), or heavy metal pollution (Mičieta and Murín, 1996). As ozone is rapidly replenished into the atmosphere (Black et al., 2014), UV-B radiation causing long-term disturbance of mutated sporomorphs over the 900-1500 k.y. ...
The Early Jurassic Toarcian oceanic anoxic event (T-OAE, ca. 183 Ma) was accompanied by a major biotic turnover in the oceans and substantial vegetation change on land. The marine biotic crisis has been attributed to several triggers, e.g., anoxia, warming, ocean acidification, yet the processes underlying the collapse of the terrestrial ecosystem are poorly understood. New high-resolution geochemical and palynological data across the T-OAE from a lacustrine succession in North China reveal elevated occurrences of spore dwarfism, asymmetrical Classopollis tetrads, and aberrant spores coeval with increases in heavy metal (Hg, Cu, Cr, Cd, Pb, As) abundances. The occurrence of teratological spores and pollen in multiple plant groups suggests overall vegetation-scale ecological pressure. Our data indicate that the combination of a widespread floral crisis with higher terrestrial organic matter oxidation and decomposition, enhanced hydrological cycle, and coeval large-scale volcanism resulted in higher concentrations of toxic heavy metals in terrestrial ecosystems. These heavy metals could poison plants, causing mutations and disrupting their reproductive cycle, and making them more vulnerable to secondary stresses such as climatic extremes and/or habitat shifts, eventually leading to widespread collapse across all terrestrial trophic levels.
... En esta contribución documentamos la primera evidencia clara de rasgos teratológicos desarrollados independientemente en diferentes linajes de plantas y posiblemente algas, coincidiendo sincrónicamente con el intenso vulcanismo explosivo dentro de la misma región en el Triásico Medio. Foster & Afonin, 2005;Bazhina et al., 2007;De Storme & Geelen, 2013;Benca et al., 2018Benca et al., , 2022Lindström et al., 2019;Chu et al., 2021;Looy et al., 2021). Several studies have shown that volcanism is a critical factor for long-term climate change, and global warming is widely regarded to have contributed to numerous past biotic crises (Sun et al., 2012;Payne & Egan, 2019;Chen & Xu, 2019). ...
... Phytotoxic volcanic emissions and radiation stress can cause abnormalities in plants and malformed spores and pollen (sporomorphs), and tetrad formation (Mičieta & Murín, 1996;Visscher et al., 2004Visscher et al., , 2011Foster & Afonin, 2005;Yin et al., 2014;Hochuli et al., 2017;Benca et al., 2018Benca et al., , 2022Benton, 2018;Lindström et al., 2019;Grasby et al., 2020;Chu et al., 2021). Multiple malformations have been shown to be associated with environmental stress. ...
... Malformation traits can be produced through meiotic deviations 120 (mutations) and deviations later in the sporogenesis process (tetrad/free spore stage). Both of these traits can occur within sporomorphs, and some give clues into which developmental processes were disrupted" (e.g., Benca et al., 2022). Recent works have shown that elevated UV-B radiation increases malformations in pine pollen and that the resulting teratology has the same characteristics as those recorded in gymnosperm bisaccate pollen during the end-Permian (Benca et al., 2022, and references therein). ...
... This peculiar characteristic, though, could be the result of a taphonomic artefact rather than environmental stress; therefore, further studies are needed to validate this external trait. The few occurrences of spore dyads and tetrads were less than 1% on average and, therefore, below the baseline frequency of 3-5% above which environmental influence on spore and pollen morphology can be assumed 1,8,12,72 . They reflect the natural variation of spore and pollen morphology (e.g. ...
The Cenomanian/Turonian boundary interval is associated with an oceanic anoxic event (OAE 2, 94.0 Ma) during one of the warmest episodes in the Mesozoic. To date, plant responses to these climatic conditions are known only from the northern mid-latitudinal succession in Cassis, France. There, conifer-dominated and angiosperm-dominated vegetation types alternate. However, whether the exceptional environmental conditions had an impact on plant reproduction is unknown to date. We applied a new environmental proxy based on spore and pollen teratology on palynological samples from the Cassis succession, to explore if this phenomenon also occurs across the OAE 2. The observed frequencies of<1% malformed spores and pollen grains suggest that plant reproduction was not affected during the Cenomanian/Turonian boundary interval. While the effects of continental Large Igneous Province(s) on plant reproduction have shown to produce abnormal spore or pollen morphologies as evidence for severe environmental pollution, by contrast the effects of oceanic LIP(s) seems to be inconsequential.
... Teratology is the science of malformation that occurs during the development of an organism. Spores and pollen are also known to show teratomorph morphologies, sometimes in frequencies exceeding the background values of plants grown under present-day natural conditions 1 . In palaeopalynology, teratomorphic spores and pollen have been successfully employed as a proxy for increased environmental disturbance. ...
... This peculiar characteristic, though, could be the result of a taphonomic artefact rather than environmental stress; therefore, further studies are needed to validate this external trait. The few occurrences of spore dyads and tetrads were less than 1% on average and, therefore, below the baseline frequency of 3-5% above which environmental influence on spore and pollen morphology can be assumed 1,8,12,63 . They reflect the natural variation of spore and pollen morphology (e.g., 64,65 ). ...
The Cenomanian/Turonian boundary interval is associated with an oceanic anoxic event (OAE 2, 94.0 Ma) during one of the warmest episodes in the Mesozoic. To date, plant responses to these climatic conditions are known only from the northernmid-latitudinal succession in Cassis, France. There, conifer-dominated and angiosperm-dominated vegetation types alternate.However, whether the exceptional environmental conditions had an impact on plant reproduction is unknown to date. Weapplied a new environmental proxy based on spore and pollen teratology on palynological samples from the Cassis succession,to explore if this phenomenon also occurs across the OAE 2. The observed frequencies of <1% malformed spores and pollengrains suggest that plant reproduction was not affected during the Cenomanian/Turonian boundary interval.
... Based on field observations, one sac or three sacs malformation rate < 3% is normal for conifers under low stress; however, the exposure to UV-B radiation induced trees to produce 3-sac pollen. In the paleo-deposit, pollen with 3-sacs instead of 2-sacs was common, but a spike in 3-sacs pollen was interpreted as an indicator of ozone weakening events [47]. As in the case study of Takarkori, this research showed that certain types of malformations may be useful to indicate what kind of stress those plants were experiencing. ...
This paper reports on the most ancient unusual morphological trait of the apertures of Poaceae pollen found in archaeological layers. In Poaceae, high levels of hybridization, polyploidy, apomixis, and multiporate pollen are often related. Multiple genomes in polyploids are critical for the adaptation of plant species to stresses and could be revealed by anomalies in pollen development. Therefore, the paleoenvironmental research can gain great benefits from identifying polyploids in past contexts by observing anomalous pollen morphology during pollen counts. The occurrence of multiporate pollen in Poaceae has also been related to special features of the ecology of the species showing this anomaly, as well as to climatic and environmental stresses experienced by Poaceae living in a given region. Multiporate and bi- or tri-porate instead of monoporate pollen grains have been observed in samples taken from Takarkori rockshelter, an archaeological site in southwestern Libya (central Sahara) that has been occupied between ~10,200 and ~4650 cal BP. Multiporate pollen was found in organic sands and coprolites of ovicaprines. On the basis of archaeobotanical research, this work aims to investigate whether the presence of supernumerary pores in Poaceae pollen may be an effect of both climatic/hydrological changes and continued anthropogenic pressure on the wild grasses living in the region. The presence of multiporate pollen reveals that Poaceae that lived in central Sahara tackled several kinds of stress during the early and middle Holocene. The Takarkori pollen record suggests that climate change could have played a major role in the early Holocene, while human pressure became stronger during the middle Holocene. The change in environmental conditions determined adaptive responses of polyploid grasses even in the form of multiporate pollen.
