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Cyanobacteria and seasonal death: A new taphonomic model for the Eocene Messel lake

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Abstract

Two new observations lead us to reconsider the taphonomy of Messel. First, several horses as well as turtles indicate death at a specific season although they come from different horizons. Second, specific structures in the Sediments are very similar to those found in Neumark-Nord. There they could be related to Cyanobacteria. Blooms of Cyanobacteria may poison die surface water. From actual observations it is known that animals drinking such poison water collapse immediately and die mostly near or within the water soon. This model might explain why birds and bats are so frequent throughout the entire profile of Messel. Both drink from the water surface during flight. In contrast to volcanic exhalations, assumed so far, such algae blooms occur repeatedly and always during early summer and autumn. Zwei neue Beobachtungen verändern das Bild der Taphonomie von Messel: Zum einen gibt es bei den Pferden und Schildkröten eindeutige Hinweise, dass viele dieser Tiere zu einer bestimmten Jahreszeit umgekommen sind, obwohl sie aus ganz unterschiedlichen Horizonten stammen. Zum anderen gleichen spezielle Strukturen im Sediment solchen aus Neumark-Nord in hohem Maße, die dort durch Blüten von Cyanobakterien verursacht wurden. Diese Bakterien können bei hoher Konzentration das Oberflächenwasser zeitweise vergiften. Wie Rezentbeobachtungen zeigen, treten bei Tieren, die dieses Wasser trinken, sehr schnell Lähmungen und Krämpfe auf, und sie sterben meist sehr schnell im Wasser oder in dessen unmittelbarer Nähe. Das würde auch erklären, warum im ganzen Profil von Messel so viele Vögel und Fledermäuse überliefert sind, weil diese Tiere von der Wasseroberfläche trinken. Im Gegensatz zu bislang angenommenen vulkanischen Exhalationen treten derartige Cyanobakterienblüten immer wieder auf, meist im Frühsommer oder Herbst.
... [42]). Second, the density of vertebrate fossils is very low throughout the Messel Formation [43]. Spatially closely associated specimens (i.e. ...
... As in the abovementioned case of the living marine teleost L. griseus, these holostean fishes from the ELM may have locally developed such an opportunistic feeding behaviour because of the relatively large amount of bats available in the lake (i.e. numerous drowning/dying individuals and floating/sinking carcasses; see [43,44]), representing an unusual but significant food source. It is known that modern gars and bowfins are opportunistic feeders, which primarily consume prey items that appear to be most available (e.g. ...
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Direct evidence of trophic interactions between extinct species is rarely available in the fossil record. Here, we describe fish–mammal associations from the middle Eocene of Messel (Germany), consisting of three specimens of holosteans (one Atractosteus messelensis (Lepisosteidae) and two Cyclurus kehreri (Amiidae)) each preserved with a bat specimen (Palaeochiropteryx tupaiodon) lying in close contact with its jaws. This suggests that these fishes probably died after failed swallowing attempts, with the bat wing membrane entangled in their jaws resulting in a fatal handicap. Based on data from modern gars and bowfins, A. messelensis and C. kehreri may have opportunistically attacked drowning and dying individuals or scavenged on floating/sinking carcasses. This hypothesis is also supported by the unusually high number of bat specimens preserved in the deposits of the Eocene Lake Messel, suggesting that this group of small mammals may have represented a substantial food source for generalist feeders. This is the earliest case of chiropterophagy and the first known evidence of bat consumption by lepisosteid and amiid fishes, emphasizing the high trophic variability and adaptability of these groups throughout their evolutionary histories. The newly described associations provide important information for reconstructing the Eocene Lake Messel palaeoecosystem and its trophic web.
... While extensive discussions about the worldwide spread of HABs only began recently, historical records dating back centuries document HAB occurrences and HAB-associated poisoning [18][19][20]. Through the years, some factions in the scientific community have been skeptical about the persistence of HABs as a global phenomenon as supported by the argument that the increase in reported incidence is due to heightened awareness and monitoring efforts (see Figure 1) [1,3,4,21,22]. ...
... While extensive discussions about the worldwide spread of HABs only began recently, historical records dating back centuries document HAB occurrences and HABassociated poisoning [18][19][20]. Through the years, some factions in the scientific community have been skeptical about the persistence of HABs as a global phenomenon as supported by the argument that the increase in reported incidence is due to heightened awareness and monitoring efforts (see Figure 1) [1,3,4,21,22]. ...
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In a constantly changing environment brought about by the climate crisis and escalated anthropogenic perturbations driven by the growing population, harmful algal bloom dynamics and their impacts are expected to shift, necessitating adaptive management strategies and comprehensive research efforts. Similar to primary productivity, HABs have been thought to be driven primarily by major nutrients such as N, P, and Si. However, recent investigations on the role and importance of micronutrients as limiting factors in aquatic environments have been highlighted. This paper provides a review of metal and phytoplankton interactions, with a specific emphasis on pertinent information on the influence of trace nutrients on growth, toxin production, and other underlying mechanisms related to the dynamics of HABs. Low to near-depleted levels of essential nutrients, including Fe, Cu, Zn, Se, Mn, Co, and Mo, negatively impact cell growth and proliferation of various marine and freshwater HAB species. However, evidence shows that at elevated levels, these trace elements, along with other non-essential ones, could still cause toxic effects to certain HAB species manifested by decreased photosynthetic activities, oxidative stress, ultrastructure damage, and cyst formation. Interestingly, while elevated levels of these metals mostly result in increased toxin production, Co (i.e., yessotoxins, gymnodimine, and palytoxins) and Mn (i.e., isodomoic acid, okadaic and diol esters) enrichments revealed otherwise. In addition to toxin production, releasing dissolved organic matter (DOM), including dissolved organic carbon (DOC) and humic substances, was observed as an adaptation strategy, since these organic compounds have been proven to chelate metals in the water column, thereby reducing metal-induced toxicity. Whilst current research centers on free metal toxicity of specific essential elements such as Cu and Zn, a comprehensive account of how trace metals contribute to the growth, toxin production, and other metabolic processes under conditions reflective of in situ scenarios of HAB-prone areas would yield new perspectives on the roles of trace metals in HABs. With the growing demands of the global population for food security and sustainability, substantial pressure is exerted on the agriculture and aquaculture sector, highlighting the need for effective communication of information regarding the interactions of macro- and micronutrients with HABs to improve existing policies and practices.
... They also cited numerous other examples, less dramatic than at Lake Nyos, of animal and human death by asphyxiation in the vicinity of volcanic lakes. Braun and Pfeiffer (2002) and Koenigswald et al. (2004) presented a different hypothesis. They postulated that the occurrence of mating pairs of the turtle Allaeochelys crassesculptata (see Joyce et al. 2012) and of gravid females of the perissodactyl that is now called Eurohippus messelensis (Franzen 2007) indicate seasonal death. ...
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The Messel Pit is an ancient maar lake that preserves an ecosystem from the last greenhouse phase of Earth’s climate with exceptional fidelity. There are two main competing hypotheses to explain the occurrence of animal fossils at Messel: asphyxiation in layers of heavy, toxic gases like carbon dioxide, and death following ingestion of surface water contaminated by cyanobacterial toxins. Both hypotheses imply mortality much higher than the null hypothesis of accidental death, for instance by drowning. We tested these hypotheses amongst bats by recourse to a unique survey on bats that drowned in modern swimming pools. We further conducted experiments on the fate of fresh bat carcasses that simulate drowning. Finally, we estimated the annual rate of bat fossil production at Messel. Overall, there are few good surveyed predictors of whether bats drown in swimming pools: most physical parameters like pool size or the height and distance of obstructions were not associated with mortality, although pool liner type would be a good candidate parameter for future study. In our experiments, carcasses with water-filled lungs tend to sink more quickly than those with air-filled lungs; all carcasses that initially sink “bloat and float” at shallow depths, but all floaters eventually disarticulate and sink within days to weeks. Our estimates of annual bat mortality at Palaeolake Messel are of the same order of magnitude as mortality in swimming pools. Mass mortality horizons for vertebrates are very rare at Messel. In sum, our quantitative analyses provide no evidence that bat mortality at Messel rises above background levels.
... Researchers suspect that freshwater CyanoHABs have occurred since prehistorical times (Braun and Pfeiffer, 2002;Koenigswald et al., 2004). The first toxicologic report on eutrophicated poisonous water bodies was made by George Francis in 1878, suspecting that Nodularia spumigena, overgrowing an Australian lake, contained a toxin that led to the death of livestock (Francis, 1878). ...
... Researchers suspect that freshwater CyanoHABs have occurred since prehistorical times (Braun and Pfeiffer, 2002;Koenigswald et al., 2004). The first toxicologic report on eutrophicated poisonous water bodies was made by George Francis in 1878, suspecting that Nodularia spumigena, overgrowing an Australian lake, contained a toxin that led to the death of livestock (Francis, 1878). ...
... In contrast, an alternative hypothesis proposes water poisoning (microcystins) after episodic Cyanobacteria blooms as the main cause of mass terrestrial animal casualties (Koenigswald et al. 2004). This hypothesis remains yet to be proven since neither gases nor bacterial toxins left traces in the form of the posture of the skeletal elements (Wuttke et al. 2018). ...
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The Jarrow assemblage is a Lagerstätte of Pennsylvanian tetrapods and fish preserved in the Leinster Coalfield, Ireland. Fossils from this site have an interesting taphonomy that is not observed in other Pennsylvanian coal swamp assemblages. Jarrow tetrapod bone material has undergone alteration and eventual coalification, causing specimens to become poorly defined from the surrounding coal matrix. Bone alteration at Jarrow has traditionally been linked to early diagenesis. A multi‐analytical approach, combining x‐ray scanning electron microscopy, cathodoluminescence, micro computed tomography and laser ablation quadrupole inductively coupled plasma mass spectrometry, was used to investigate the origin of alteration within the Jarrow fossil specimens. Original bone morphology is no longer present, being replaced by bituminous material and sphalerite surrounded by tabular apatite (a morphology atypical of bone apatite). Direct U–Pb dating of this recrystallized apatite provides an age of 302.03 ± 11.38 Ma. In this recrystallized apatite, core‐to‐rim variation in halogen elements, variably positive and negative Eu‐anomalies and depletion in light rare earth elements (REEs) suggest an influence of hydrothermal fluids sourced during the maturation of the Leinster Coalfield. A new taphonomic model for the Jarrow assemblage is proposed: alteration of primary fossil bone occurred primarily due to burial heating of the Leinster Coalfield caused by Variscan deformation. Bone apatite was dissolved and subsequently recrystalized as tabular crystals, probably concurrent with mineralization of sphalerite and during coalification, giving the Jarrow assemblage fossils their unique appearance.
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The Messel Pit, located near Frankfurt am Main, Germany, is inscribed on the list of UNESCO World Heritage sites due to the breathtaking quality of its fossils and the wealth of detail they reveal about life in an ancient ecosystem. Its age, about 48 million years old, places it in the last sustained greenhouse phase of Earth's climate, the Eocene. Fossils of most major terrestrial groups of organisms are preserved together, from freshwater algae to fungi, plants and animals. Species diversity in many groups is higher than in the same area today. Extraordinary details of organismic anatomy are preserved, from iridescent insect colouration to bird plumage and reptile scales. Furthermore, stunning specimens record organismic interactions, from predator–prey relations to reproductive behaviour. Messel arguably holds the greatest promise to elucidate a terrestrial ecosystem in a greenhouse climate. Key Concepts • Messel is an ancient maar lake that resulted from volcanic eruptions 48 Ma. • Climate at the time was warm and equable, a so-called ‘greenhouse climate’. • The sediment in which the fossils are preserved is an ‘oil shale’ with a high water and organic content. • A special transfer method developed in the mid-twentieth century made possible the long-term conservation of vertebrate fossils from Messel. • Messel preserves an exceptional taxonomic range of fossils, from algae to plants and animals. • Soft-tissue preservation at Messel gives unparalleled insight into the anatomy of ancient organisms. • Extraordinary specimens from Messel document organismic interactions, from trophic relations to reproductive behaviour.