Ecology

Elderflora: A Modern History of Ancient Trees Jared Farmer Basic (2022)About 45 million years ago, when the Arctic was ice-free, the world’s earliest known mummified trees flourished on what is now Axel Heiberg Island in Canada’s Qikiqtaaluk Region. In 1986, palaeobotanists identified the megaflora as members of Metasequoia occidentalis, an extinct redwood species. They had been buried in silt, then frozen, their wood preserved.The lead palaeontologist “celebrated his eureka by kindling a fire with 45-million-year-old twigs and boiling water for tea time,” writes historian Jared Farmer in Elderflora, his expansive global history of grand and venerable trees. Granted, these plants had been dead since the Eocene epoch. Nevertheless, as the author describes, the incident is part of a troubling pattern in which scientists rejoice at their discovery of the ‘oldest’ tree of their time — and then destroy it.In 1957, for example, Edmund Schulman at the University of Arizona in Tucson spent the summer seeking ancient bristlecone pines in California’s White Mountains. He found three more than 4,000 years old, and named them Alpha, Beta and Gamma. Then, in the interests of tree-ring science, he chose to “sacrifice” Alpha, taking snapshots as his nephew and a colleague sawed it down. When the University of Arizona issued a press release titled ‘UA Finds Oldest Living Thing’, Farmer writes, “they say nothing about the thing being dead”.Schulman’s aim was dendroclimatology — the reconstruction of climates using tree-ring data. That lofty motive cannot be ascribed to those who, in 1881, bored a tunnel into the 2,000-year-old Wawona tree in Yosemite National Park, allowing tourists to drive their cars through the 71.3-metre-high giant sequoia (Sequoiadendron giganteum), since toppled.Arboreal legendsAs Elderflora shows, big, old trees are objects of veneration and vandalism, appearing “in the oldest surviving mythologies and the earliest extant texts”. They were associated with gods and heroes, prophets and gurus: they had pivotal roles in the Mesopotamian Epic of Gilgamesh and in the Polynesian legend of Rātā, who fells a noble tree to carve a canoe. In more recent times, European settlers “dispossessed Indigenous peoples and cleared forests with abandon”. Research shows that, for 8,000 years after the glaciers of the last ice age retreated, forests in the Midwestern United States doubled in biomass (A. M. Raiho et al. Science 376, 1491–1495; 2022). Just 150 years of industrial logging and agriculture erased this carbon accumulation.
It takes a wood to raise a tree: a memoir
“Imperial conquests and industrial revolutions relied on timber,” Farmer writes. “Wood-stock long guns for capturing lands and peoples; naval vessels with mighty masts for transporting the enslaved and the harvests of their labor.” In New Zealand, European settlers decimated the majestic kauri trees, which can live for up to 2,000 years and that once covered 1.2 million hectares of land. The trees’ 50-metre-trunks became ships’ masts; their resin was made into varnish and linoleum.Like pines, firs, spruces, cedars, cypresses and redwoods, kauri (Agathis australis) is a gymnosperm. These flowerless plants with naked seeds tend to grow slower and live longer than angiosperms, flowering plants that bear fruit. About 25 plant species — most of them conifers — can live for more than a millennium without human assistance, surviving in restricted, vulnerable habitats.Farmer also offers a global survey of ancient trees that have been protected and exalted. They include olive trees of the Levant (Olea europaea); research published this year shows that these were domesticated about 7,000 years ago for their fruit and oil (D. Langgut and Y. Garfinkel Sci. Rep. 12, 7463; 2022). In Africa, the baobab (Adansonia sp.) is both the longest-lived tree and the largest, offering shade and shelter, foods, medicines and textiles. Enslaved Africans planted baobabs in the Caribbean; some survive still. Ginkgo biloba, a species that dates back 390,000 years, survived only in China, whence it was spread around the world in the past millennium. A grove of ginkgo trees survived the atomic bombing of Hiroshima in Japan in August 1945, pushing out new buds the following spring.The planet’s current tree cover, Farmer writes, includes 3 trillion large plants covering about 30% of all land. It is, in fact, expanding. But the new cover consists mostly of shelter belts (trees planted to protect crops or animals), temperate-zone timber crops and tropical plantations of eucalyptus and palm oil. A shrinking proportion of tree cover is made up of species-rich old-growth communities.Epic loss“What would humans and nonhumans stand to lose if these survivors all died prematurely? A world of things,” Farmer writes. “Old trees sustain forest communities” with their seeds and litter. Other plants grow on them, and animals live in them. Their roots share nutrients with other organisms via underground fungi. Groups of “Old Ones” are carbon sinks. Large-scale monocultures are shorter-lived and take less greenhouse gas out of circulation.But even bygone trees of the once-tropical Arctic might offer lessons for a warming world. Palaeobotanist Hope Jahren, in her 2016 memoir Lab Girl, describes how she spent three summers on Axel Heiberg Island, digging “through a hundred vertical feet of time”. Fir, cypress, larch, redwood, spruce, pine and hemlock trees populated this lush conifer forest, with an understory of angiosperms: maple, alder, birch, hickory, chestnut, beech, ash, holly, walnut, sweetgum, sycamore, oak, willow and elm. These plants thrived even through three months of winter darkness and three of constant summer light.“Here stood one of the great forests of all time,” Farmer writes. Today, as the Arctic warms nearly four times as fast as any other place on Earth, the genomes of species related to the trees of this mummified forest might be adaptable enough for the trees to flourish in a rewarmed planet, he says. Old trees have much to teach us: we would be wise to listen. More

replying to Y. Cheng et al. Nature Communications https://doi.org/10.1038/s41467-022-33958-7 (2022)We welcome the comment from Matters arising from Cheng Y et al.1, which provides us an opportunity for further clarification of some of our points2. The Comment raised interesting and important issues about our paper, that undoubtably could enhance our understanding for the Holocene vegetation evolution in the northern China and its relationship with East Asian Summer Monsoon (EASM). In particular, the results from Dali lake pose the questions on the timing of the peak of tree cover, that invokes the further investigation to understand this complex tree changes over Holocene period. However, these comments do not impact the key result in our original study2, that is the periodical asynchronous evolutions between EASM and northern China ecosystem under specific conditions.Main points of our paper are: First, we propose that the EASM and its rainfall over northern China mainly followed the variation of the summer insolation and peaked in the early Holocene, while the relative tree cover of temperate deciduous broadleaf tree peaked in the mid-Holocene; the delayed tree cover peak is caused by the winter warming, and peak soil moisture also in the mid-Holocene, which could be related to a hydrological impact from vegetation shift from grass to tree and the positive feedback between this vegetation shift and soil wetting.Second, this asynchronous evolution between the EASM rainfall, which peaks in the early Holocene, and the northern China ecosystem, which peaks in the mid-Holocene, is caused mainly by the opposing effect of residual ice sheet retreat on the decreasing summer insolation. The declining summer insolation does cause a substantial decrease of EASM rainfall from the early to mid-Holocene. However, 2/3 of this rainfall decrease is canceled by the rainfall increase forced by the retreat of residual Laurentide ice sheet, resulting in a weak decreasing trend of rainfall over this period.Third, under this background of weak rainfall changes, winter warming, induced by increased winter insolation and ice sheet retreat, raised the coldest temperature to above −17 °C, the threshold for the survival of temperate deciduous broadleaf tree3, and then favored an increase in tree, meanwhile induced a decrease in grass for reasons of its lower competitiveness than that of tree. This vegetation shift then supported the wetting of northern China through its hydrological effect2. The vegetation shift and soil wetting could reinforce each other. Furthermore, the dominant effect of winter warming on vegetation from the early to mid-Holocene is supported by our sensitive experiments with an off-line land-vegetation model.As stated in Cheng Y’s Comment1, the land cover in northern China includes forests, grass and bare land. In our interpretation, the process of “the vegetation feedback to climate” is mentioned as a possible feedback that enhances this asynchronous response, but is not critically involved in the mechanism. As such, whether the absolute or relative vegetation cover is not a major issue in our discussion. It’s sure that the reconstructed absolute tree cover, which based on pollen concentration, could enrich our understanding of the vegetation changes over the Holocene period in northern China. Indeed, the hydrological impact of bare land (evaporation) had been considered in our hydrological analysis of northern China soil moisture, and the results indicated its impact is important but not critical to the Holocene long-term changes of soil moisture over this region. The relative tree cover, the percentage of cool mixed tree (COMX4) in fossil pollen which is consistent with that of temperate deciduous broadleaf tree in simulation2, that we cited4 is a synthesis of 31 records, which represented the general evolution of vegetation over a large part of northern China, and its main result is consistent with records from other part of northern China such as the 6 ka peak in Gonghai Lake5. In spite of its low time resolution, the general trend over the millennium scale seems to us clear.It’s true that the −17 °C of the coldest month temperature is the survival threshold for the temperate deciduous broadleaved tree. While, the temperature threshold for C3 grass and C3 arctic grass are complex, its direct impact on the changes of grass proposed in our paper is somewhat not strict. However, considering the different competitiveness between tree and grass, increased temperate deciduous broadleaved tree, which derived by the winter warming, could induce a decrease in the grass from the early to mid-Holocene. Indeed, summer temperature, annual rainfall and fire incidents are all the important factors determining the Holocene changes of vegetation over northern China, but series of sensitivity experiment proposed the key impact of winter temperature on the vegetation shift and soil moisture evolution, which is consistent with the results of transient coupled climate simulation and geological records. This grass-to-tree shift for this period is evidenced in the pollen percentages and well simulated by the climate model shown in our paper2.Fire is an important factor for the long-term changes of vegetation cover over semi-arid regions, and its emergence and impact on vegetation are already incorporated into our model6, then, in turn, the simulation. Future works could assess the impact of fire on the long-term changes of semi-arid vegetation through the combination of reconstruction and process-based simulation of fire7.Focusing on the contrary views of Holocene EASM within proxy records, we proposed an asynchronous evolution of EASM rainfall and northern China ecosystem for the period of early to mid-Holocene. Our proposal is based on a state-of-the-art transient climate simulation, which reproduced the diverse evolution of EASM proxies reasonably well. The mechanisms proposed for this asynchronous evolution appear to us consistent with the current evidences available. There are, however, uncertainties in models and proxies. Meanwhile, the northern China is a broad region with large gradient in rainfall and ecosystem, that could induce the possible diverse evolutions in climate and ecosystem under Holocene climate change. Therefore, we believe further studies using other models and new proxies are important to further improve our understanding of this issue. More

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Electrohydrogenesis effluent as a potential biofertilizerTo characterize the electrohydrogenesis left-over residues as potential biofertilizers, the sample from the operating reactors was performed a 16S rRNA sequencing test, and interestingly, the results revealed that the bio-electrohydrogenesis effluent was enriched with various microorganisms including plant growth-promoting microbes that display biofertilizer-like features. Among the well-known plant-promoting bacterial genera observed in DF-MEC residues included Azospirillum, Mycobacterium, Chryseobacterium, Paenibacillus, Rhizobacter, Pseudomonas, Achromobacter, Bradyrhizobium, Actinomyces, Sphingomonas, Allorhizobium-Neorhizobium-Pararhizobium-Rhizobium, Gordonia, Rhodococcus, Bacillus, Methylobacterium-Methylorubrum, Microbacterium, Flavobacterium, Devosia, Acinetobacter, Mesorhizobium, Enterobacter, Aeromonas, Beijerinckia, etc.24,25,26 (Fig. 2). Lots of investigations working on the feasibility of using biofertilizers other than chemical fertilizers have revealed that those aforementioned microbes play a major role in providing the required nutrients for enhanced crop yield.Figure 2The abundance of the Plant growth-promoting bacteria (genus level) detected from the DF-MEC digestate (%).Full size imageNitrogen-fixing microorganismsThe detected nitrogen-fixing microorganisms from the electrohydrogenesis effluent include Azospirillum sp. (0.11 ± 0.02%), rhizobia (Rhizobium (0.058 ± 0.02%), Bradyrhizobium (0.11 ± 0.04%), and Mesorhizobium (0.1 ± 0.03%)), and Beijerinckia (0.08 ± 0.03%) (Fig. 2) and were repeatedly reported for their superior contribution to the plants’ nitrogen requirements through biological nitrogen fixation, which is an important component of sustainable agriculture25. Although the atmosphere counts about 78% N2, it couldn’t be used by plants in its natural state. Prior to getting used by plants, it needs to be converted to ammonia, which is the readily assimilable form of nitrogen by plants/or crops via a biological nitrogen fixation mechanism25. The biological Nitrogen fixation mechanism is summarized in Fig. 3.Figure 3Mechanism of nitrogen fixation bio-catalyzed by nitrogenase enzyme. The plant growth-promoting bacteria produce nitrogenase which is a complex enzyme consisting of dinitrogenase reductase and dinitrogenase. This complex enzyme plays a major role in molecular N2 fixation. Dinitrogenase reductase provides electrons and dinitrogenase uses those electrons to reduce N2 to NH3. However, oxygen is a potential threat to this process since it has the ability to get bound to the enzyme complex and make it inactive and consequently inhibit the process. Interestingly, bacterial leghemoglobin has a strong affinity for O2 and thus gets bound to free oxygen more strongly and effectively to suppress the available oxygen effects on the whole process of nitrogen fixation.Full size imagePhosphate-solubilizing microorganismsFurthermore, various phosphate-solubilizing and mineralizing strains were also found in bioelectrohydrogenesis residues collected from our DF-MEC integrated reactors. Among those microorganisms with the ability to solubilize/metabolize the insoluble inorganic phosphorus, the dominant bacterial genera included Pseudomonas (0.65 ± 0.15%), Bacillus (0.44 ± 0.11%), Rhodococcus (0.04 ± 0.009%), Rhizobium (0.05 ± 0.02%), Microbacterium sp. (0.04 ± 0.01%), Achromobacter (0.16 ± 0.07%), and Flavobacterium (0.058 ± 0.014%) (Fig. 2). Though enormous amounts of phosphorus are available in the soil, its high portion never contributes to plant growth in its primitive state, unless it is bio-transformed into absorbable forms including monobasic and dibasic. Microbial phosphate solubilizing mechanisms are well described in Fig. 4.Figure 4Inorganic phosphorus solubilization by phosphate-solubilizing rhizobacteria. A bacterium solubilizes inorganic phosphorus through the action of low molecular weight organic acids such as gluconic and citric acids. The hydroxyl (OH) and carboxyl (COOH) groups of these acids chelate the cations bound to phosphate and thus convert insoluble phosphorus into a soluble organic form. The mineralization of soluble phosphorus occurs by synthesizing different phosphatases which catalyze the hydrolysis process. When plants incorporate these solubilized and mineralized phosphorus molecules, eventually, overall plant growth and crop yield significantly increase.Full size imagePhytohormone-producing microorganismsIn this current work, the electrohydrogenesis effluent also contained bacterial genera such as Mycobacterium (0.77 ± 0.18%), Allorhizobium (0.05 ± 0.02%), Pararhizobium (0.05 ± 0.02%), Paenibacillus (1.18 ± 0.24%), Bradyrhizobium (0.11 ± 0.04%), Rhizobium (0.05 ± 0.02%), Acinetobacter (0.14 ± 0.02%), and Azospirillum (0.11 ± 0.025%) (Fig. 2) that have the ability to synthesize indole-3-acetic acid/indole acetic acid (IAA) through indole-3-pyruvic acid and indole-3-acetic aldehyde25. IAA is a well-known type of phytohormone that enhances plant/crop growth. Particularly, Azospirillum sp., also produce various phytohormones namely cytokinins, gibberellins, ethylene, abscisic acid and salicylic acid, auxins, vitamins such as niacin, pantothenic acid, and thiamine. The conceptional model delineating the positive effects of inoculation with Azospirillum sp. a phytohormones-producer plant growth-promoting rhizobacteria and its detailed functions on plant growth are summarized and illustrated in Fig. S1. Therefore, the existence of those rhizobacteria in the bioelectrohydrogenesis residues further implies the suitability of considering the DF-MEC left-over residues as potential biofertilizers.Heavy metals-bioremediating microorganismsSome other bacterial genera with the ability to bioremediate the heavy metal toxicity were also found within the bioelectrohydrogenesis left-over residues as well. Among the detected plant growth-promoting bacterial genera; Rhizobium (0.058 ± 0.023%), Mesorhizobium (0.1 ± 0.026%), Bradyrhizobium (0.11 ± 0.04%), Pseudomonas (0.65 ± 0.15%), and Achromobacter (0.16 ± 0.077%) were reported for their key contribution to alleviate the toxicity of the heavy metals via bioremediation process and improve the soil quality for a relief plant development26 (Fig. 2). Other detected heavy metals-bioremediating microorganisms’ species were Chryseobacterium sp. (0.08 ± 0.007%), Azospirillum (0.11 ± 0.02%), Bacillus (0.44 ± 0.11%), Enterobacter (8.57 ± 0.9%), Gordonia (0.06 ± 0.02%), Paenibacillus (1.18 ± 0.24%), Pseudomonas (0.65 ± 0.15%), and Actinomycetes (0.36 ± 0.05%) that either use microbial siderophores or enzymatic biodegradation process.Electrohydrogenesis left-over residues as a potential source of essential elements for plant growthAs aforementioned in “Materials and methods” section, the electrohydrogenesis left-over residues contained diverse microbial communities that degraded the MEC substrate and generate biogas and inorganic compounds. Moreover, it has been reported that those inorganic nutrients are generally available in fermentation effluent in readily plant-utilizable formats owing to substrate mineralization27. Beside detecting various plant growth-promoting microorganisms in the electrohydrogenesis effluent, a larger number of mineral elements essential for promoted growth and development of crop plants were also investigated and analyzed from the residues. The detected primary and secondary macro-elements’ concentrations in the residues were arranged in decreasing order as follows P  > S  > Na  > K  > N  > Ca  > Mg. Interestingly the findings show that the residues abundantly contained Phosphorus (2.766 × 103 mg/L), Nitrogen (274 mg/L), Potassium (282 mg/L), Calcium (17.66 mg/L), Magnesium (16.3 mg/L), Sulfur (1.225 × 103 mg/L), and Sodium (294.3 mg/L) which are well known as macro-nutrients needed in larger amounts for enhanced plant/ crop growth (Fig. 5).Figure 5Macro-, and micronutrients detected from the bio-electrohydrogenesis left-over residues (mg/L).Full size imageMoreover, small amounts of the microelements including Ni, Pb, Zn, Cu, Cr, Hg, Cd were also found in the electrohydrogenesis residues, and consistently these elements are generally required in small quantities for the development of plants (Fig. 5), otherwise, their high concentrations are toxic for the plant cells thus suppress or inhibit plant growth. The detected concentrations for the main microelements in this current research ranged only from 0.36 to 9.6 × 10–5 mg/L and were all reported to play fundamental roles in plant metabolic reactions.Cultivation of the leguminous crops using electrohydrogenesis left-over residues as fertilizerAfter evaluating the plant-growth promoting bacterial communities and the macro- and micronutrients required for plant/crop growth in the electrohydrogenesis left-over residues, the latter was directly used as fertilizer to grow three different plant species including tomato, chili, and brinjal as afore-described in the “Materials and methods” section. To access the potentials of the electrohydrogenesis effluent as fertilizer, the plants grown in the soil amended with the effluent (Soil + Effluent), were directly compared with their corresponding control plants (Soil + water). The results indicated that at the end of 1st month, the plants with effluent grew faster and generated a good amount of branching than the control plants (see Fig. 6), possibly due to the availability of both microbial species with bio-fertilizing aspects and micro-and macronutrients in the effluent.Figure 6Analysis of the plant growth at the end of the 1st month of cultivation. (a) Tomato in soil with effluent, and its control without effluent (b); (c) Chilli grown in soil with effluent, and its control without effluent (d); and (e) brinjal grown in soil with effluent, and its corresponding control grown without effluent (f) (after 2 months).Full size imageFor instance, tomato (Solanum lycopersicum L.) and chilli (Capsicum annuum L.) height in soil + electrohydrogenesis effluent was ~ 36.9 ± 2.1 cm and ~ 32.6 ± 0.8 cm respectively which was ~ 2.03 and ~ 1.2 times the height of their corresponding plant species in the control protocol, respectively (see Fig. 7). However, the brinjal species (Solanum melongena L.) didn’t show any remarkable height differences in both protocols after a month of cultivation (data not shown), probably due to their low adaptative characteristics to the new environment. However, after the 2nd month, the brinjal height in soil + effluent became 2.7 times that of the brinjal control cultivated without effluent (see Fig. 6e,f). Moreover, both the number of the plants’ leaves and their length in plants cultivated in soil + effluent, were remarkably higher than in plants grown without the supply of the effluent.Figure 7Daily plant growth analysis within one month of cultivation. (a) Tomato growth monitoring, (b) Chili growth analysis.Full size imageAt the end of the 3rd month, the plants in soil + electrohydrogenesis effluent generated more fruit with big size than the control plants (see Fig. 8), but the tomato (Solanum lycopersicum L.) didn’t generate fruits in both protocols at that time probably due to the high weather temperature that inhibitory affected its continuous growth, as previously reported that tomato species are generally so sensitive to temperature change28,29. The final yield was evaluated in terms of the size and number of fruits per cultivated plant. Chili cultivated in soil with MEC effluent generated 3 fruits/plant and its corresponding control without effluent produced only 1 fruit/plant. The chili fruit size in soil + effluent was 16 cm, approximately 18.7% higher than its corresponding control. Moreover, at the time of collecting data, the brinjal plant cultivated in soil with MEC effluent generated brinjal fruits whereas its corresponding cultivated without electrohydrogenesis effluent started flowering (see Fig. 8). These further indicate the significant contribution of the electrohydrogenesis effluent in speeding up the plant growth. Herein, the electrohydrogenesis left-over residues have notably improved the soil quality and significantly promoted the plants’ phenology characterized by plant growth, the generation of new leaves, flowering, and the production of fruits.Figure 8Analysis of plant growth characterized by the flowering and fruiting process at the end of the 3 months. (a) Chili grown in soil with effluent, and its control without effluent (b); (c) brinjal grown in soil with effluent and its corresponding control grown without effluent (d).Full size image More