Ecology

Inverted paradoxNeutral theory can reproduce properties of terrestrial biodiversity observed at local (e.g., an island) or metacommunity (i.e., a set of interacting communities linked by dispersal of species) scales, particularly ranked species abundance curves (i.e., histograms of species abundance ordered along the x-axis from most to least common) [14]. Central to neutral theory is the interplay between ‘stochastic exclusion’ and either immigration or speciation. Stochastic exclusion is the reduction in biodiversity caused by random deaths and abundance-dependent replacement and, if not countered by other processes, ultimately leads to only a single remaining species [14]. Immigration of species into a local community or speciation within the metacommunity offset stochastic exclusion and maintain biodiversity [14]. This relationship is illustrated in Fig. 1 by simulated time-series of phytoplankton diversity for three populations at steady-state with 10,000, 100,000, and 1,000,000 total individuals and an initial condition of 10,000 species each (Fig. 1) (Methods). Subjection of these populations to 50% random mortality per generation and replacement in proportion to the relative abundance of remaining species results in an eventual rate of decrease in diversity that is equivalent across population sizes (Fig. 1; dashed black lines), eventually yielding the expected final equilibrium of a single species. When a small rate of immigration is added to this simulation (here, 0.03% or 0.3% per generation), complete stochastic exclusion is replaced by steady-state diversities that vary in direct proportion to population size and immigration rate (Fig. 1; colored dashed and dotted lines). Similar considerations led Hubbell [14] to earlier propose in his “Unified Neutral Theory” a fundamental biodiversity number, θ, controlling both species richness and relative abundance:$$theta ,=, 2Jupsilon$$
(1)
where J is the total number of individuals in the community and υ the rate of immigration (local) or speciation (metacommunity).Fig. 1: Phytoplankton biodiversity following purely stochastic processes.Red, blue, and green = phytoplankton populations (J) of 10,000, 100,000, and 1,000,000 individuals, respectively (Methods). Colored solid lines = species richness in the absence of immigration (υ). Colored dashed and dotted lines = species richness for υ values of 0.03% and 0.3% per generation. Black dashed line = mean rate of decline for the primary phase of stochastic exclusion (slope of this line is the same for all three populations). Blue and green downturned triangles = threshold for the two larger populations where diversity begins to decline rapidly because a sufficient number of species have been reduced to an abundance where extinction within a generation becomes likely.Full size imageIn addition to illustrating the balance between stochastic exclusion and immigration into a local phytoplankton community, Fig. 1 shows that significant decreases in species richness only ensue after a subpopulation of species within a community has been sufficiently decimated in number that their remaining individuals might be lost through random mortality within a generation. In our simulations, this threshold is demarked by the downturn in species richness for the populations of 100,000 and 1,000,000 individuals (Fig. 1; blue and green triangles). The significance of stochastic exclusion is thus dependent on the relation between extant species number and size of the physically-homogenized community. With respect to the latter property, typical horizontal eddy diffusion values for the upper ocean are O(103 m2 s−1), implying that the length scale for mixing in 1 day is O(1000 m). Typical number concentrations for phytoplankton of different species in the ocean range from More

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Temporal variation and dynamic analysis of eucalyptus forestsData from the 1st-9th NFIs suggested that the total area of eucalyptus plantations had started to increase since 1973 (Table 1). In 1973–1976, Eucalyptus plantations only existed in Guangxi and Guangdong (including Hainan) in China with a total area of 23.0 × 104 hectares, taking up 0.38% of total forest area in China. The stock volume was 372.0 × 104 m3, about 0.04% of that in China. In 2014–2018, the eucalyptus plantation area increased to 546.74 × 104 hectares, about 24 times of that in 1973–1976. The growing stock has increased to 21,562.90 × 104 m3 in 2014–2018 which increased about 58 times from 1973–1976.Table 1 Eucalyptus plantation area and stand volume in different time periods by province.Full size tableThe stock volume per unit area of eucalyptus plantations did not increase significantly from 1973–2008, ranging from 14–30 m3/hectares, but it increased rapidly from 2009 to 2018, reaching 39.43 m3/hectares. This increase occurred because China started to focus and value the development of eucalyptus plantations. As a. result, plantations expanded rapidly, and the need for eucalyptus with greater trunk radius increased. The extended harvest cycle of eucalyptus plantations, not the rise of eucalyptus productivity, caused the increase in stock volume per unit area29,30,31.Based on CFLDM, the distribution of eucalyptus plantations in 2003 and 2016 are mapped (Fig. 1a,b). It suggests that the distribution of eucalyptus plantations extended from Leizhou Peninsula, Guangdong and Hainan Province to the north (Guangxi, Hunan, and Guizhou provinces), east (Fujian and Jiangxi provinces), and west (Yunan and Sichuan provinces). This is consistent with data from the NFIs. The widespread expansion of eucalyptus also leads to several regions with clustered plantations.Figure 1Distribution of eucalyptus in the south of China [(a) 2003; (b) 2016]. This figure was created by spatially overlaying spatial sample plots data from National Forest Inventory (NFI) and patch vectors data from China Forest-Land Database Map (CFLDM), (a) shows that the point data are from 6th NFIs eucalyptus sample plots and the polygon vector data are from the 2003 CFLDM; (b) shows that the point data are from 9th NFIs eucalyptus sample plots and the polygon vector data are from the 2016 CFLDM. The extents of eucalyptus plantations is mainly concerned with 11 provinces (e.g. Zhejiang, Fujian, Guangdong, Guangxi) in Southern China.Full size imageChanges in spatial distributionBased on the database of sample plots (including climate and elevation data) and sampled eucalyptus, we analyze the distribution of eucalyptus plantations, and how it is affected by elevation and climate conditions. It is found that most eucalyptus plantations are within the region of 110°23′–120°5′E and 18°21′–30°39′N. The annual mean temperature within this region ranges from 11 to 25 °C with an average of 19.5 °C, and the annual precipitation ranges from 600 to 2000 mm with an average of 1455 mm. Elevation in this region is 0–2500 m with an average of 338 m.To find out the most suitable conditions for eucalyptus growth and its plantation management, we classify this region based on their elevation and climate conditions. The classification is done separately and independently for each factor (i.e., elevation, temperature, and precipitation). In terms of elevation, the region is assigned to seven grades from below 300 m to 2100 m with an interval of 300 m in between (i.e., below 300 m, 300–600 m, 600–900 m, 900–1200 m, 1200–1500 m, 1500–1800 m, 1800–2100 m). Land with elevation above 2100 mm has limited eucalyptus plantations, and thus is not taken into consideration. Similar criterion is applied to the classification based on annual mean temperature and annual precipitation. The grades are from 11 to 25 °C within an interval of 2 °C for temperature and 600–2000 mm with an interval of 200 mm for precipitation.We examine how the eucalyptus forest area changes with these factors. This is done by plotting the eucalyptus plantation area within a certain group against the corresponding grade number (Fig. 2). Eucalyptus is mostly distributed below 300 m, reaching an area of 301.1 × 104 hectares and counting for 67.58% of the total eucalyptus plantation area in China. Eucalyptus occurs rarely in areas with elevation above 900 m.Figure 2Area of eucalyptus plantations in China based on grades defined in text.Full size imageEucalyptus is sensitive to temperature, and its distribution is limited within areas with annual mean temperature below 19 °C. Eucalyptus is mostly distributed within areas with annual mean temperature of 19–21 °C. Areas with annual mean temperature within this range have a total of 291.49 × 104 hectares eucalyptus plantations, approximately 65.43% of all eucalyptus plantations in China. This result is slightly different from previous studies3,5, which suggests that eucalyptus prefers areas with mean annual temperature above 20 °C.Eucalyptus has a high tolerance to annual precipitation. Eucalyptus plantations can be found in areas with annual precipitation ranging from 600–2000 mm. It should be noted that this is related to irrigation conditions in production and management. However, in areas with annual precipitation below 600 mm, Eucalyptus plantations are extremely rare. Areas with annual precipitation of 1400–1600 mm (and without considering other factors) have the largest portion of eucalyptus plantations, whose total area reaches 146.49 × 104 hectares. This accounts for about 32.94% of total eucalyptus plantations in China.Productivity analysis of eucalyptusVariability in mean productivityEucalyptus annual productivity for each province based on the 5th to 9th NFIs (no digitized data for the 1th to 4th NFIs) is calculated, which includes 3564 sample plots (Table 2). Among which, 769 sample plots had been harvested at the time of the survey, and to remove the influence of these 769 sample plots, their data were removed during the productivity of the eucalyptus age-productivity relationship graph (see Fig. 3), which shows that the period of maximum productivity for eucalyptus lasts for approximately 2–3 years. Its productivity declines rapidly after 10 years of growth. Therefore, the harvest cycle of eucalyptus is normally 4–5 years. After coppicing and growing for another 4–5 years, Eucalyptus will be harvested again, which will be followed by its replanting.Table 2 Basic sample plot statistics (quantity, mean and maximum annual productivity) of eucalyptus plantations by province from the 5th to 9th NFIs.Full size tableFigure 3Relationship between age and productivity of eucalyptus sample plots.Full size imageVariability in eucalyptus productivityEucalyptus productivity for each province based on the 5th to 9th NFIs is calculated and shown in Table 2. It can be seen that from 1994 to 2018, mean and maximum productivities of eucalyptus plantations have increased. This is especially show for Guangxi and Fujian Provinces during 2009–2018. The averaged productivity of eucalyptus plantations in China increased from 4.14 to 8.57 m3 hm−2 a−1 from 1994–1998 to 2014–2018, which can be explained by the improved management of eucalyptus plantations (e.g., high soil fertility for newly cultivated lands and improved ability for irrigation) and their expansion.Data from the 5th to 9th NFIs suggest that a lot of sampled plots were no longer used for growing eucalyptus before the next inventory (Table 3). There were 226, 273, 687, and 109 eucalyptus plots in the 5th, 6th, 7th, 8th inventories, respectively, and in the corresponding next NFI (6th, 7th, 8th, 9th), only 150, 179, 544, and 848 of these sample plots were left unabandoned. This suggests that 33.63%, 34.43%, 20.82%, and 22.63% of the plots were abandoned before the next inventory. New plots have been included in each inventory, but large portions of these plots were abandoned as well. There are 123, 508, and 552 new eucclyptus plots in the 6th, 7th, 8th inventories, and 76, 413, and 433 of them were left unabandoned in the next inventories. The land abandonment rates for them are 38.21%, 18.70%, 21.56%, respectively.Table 3 Quantity of newly-cultivated, retained, and abandoned sample plots during different NFIs.Full size tableWe examine how the productivity changes with time for eucalyptus plantations that have been operated for more than 20 years. From the 5th to 9th NFIs, we find 55 and 38 such (operating for more than 25 and 20 years, respectively; Table 4). It is found that the productivity of eucalyptus is relatively low in the first 5 years of its growing. The productivity increases in the 5th–10th years, and reaches its peak after 10–15 years of growing eucalyptus. For land that have been continuously growing eucalytptus for 15–25 years or more, the productivity decreases significantly. This is due to the decrease in soil fertility.Table 4 Relationship between Continuous planting time and Mean productivity of reserved and newly-cultivated eucalyptus sample plots during different NFIs (unit: m3 hm−2 a−1).Full size tableMost (~ 90%) of the sample plots have mean annual productivity below 10 m3 hm−2 a−1 (Fig. 4). The productivity reaches its peak after 10–15 years of growing eucalyptus (mean annual average: 7.0175 m3 hm−2 a−1), and starts to decrease afterwards. Statistical model (Table 5) is established between productivity and age of eucalyptus plots. The results suggest that eucalyptus productivity follows a consistent pattern: it increases with time until a peak and then decrease (Fig. 5), and this applies to the old, newly-included plots and their average. The statistical model also agrees to the observed data, suggesting that the productivity peak is reached 10–15 years after the planting of eucalyptus, and the productivity reaches its minimum or even zero after 50 years of growing eucalyptus continuously.Figure 4Distribution of mean annual productivity for sample plot from different NFIs.Full size imageTable 5 Productivity prediction model of multi-stage reserved and increase eucalyptus sample plots.Full size tableFigure 5Statistical model showing how mean annual productivity of eucalyptus sample plots changes with time.Full size imageSoil fertility variation of eucalyptus plantationsHow eucalyptus affects soil fertility is not well-studied. Here, based on 948 sample points from Tang32, which includes monitoring of soil fertility of eucalyptus plantations from 1993 to 2018, we report and study the temporal soil fertility variation for eucalyptus plantations. After 25 years of growing eucalyptus, acidification of the corresponding lands persists. The pH value changed to 4.63 in 2018, a 4.14% decrease compared to that in1993. The organic content within the soil reached its minimum of 17.98 g/kg in 2018, a decrease of 23.19% compared to 1993. Total nitrogen content of the investigated samples changed from 2.11 to 1.98 g/kg, and total phosphorus content decreased from 1.12 to 0.75 g/kg. The temporal variation of potassium does not change in a consistent pattern with time. Alkaline hydrolysis of nitrogen and available potassium content in 2018 are significantly lower than those in 1993. From more to less, the rank of soil fertility indicator affiliation polygon area is 1993  > 1998  > 2003  > 2013  > 2018  > 2008. The rank of soil fertility index is 1993  > 1998  > 2018  > 2003  > 2013  > 2008. It decreased first, and then increased. The minimum soil fertility (0.475) was reached in 2008 (22.51), which is smaller than that in 1993. The soil fertility decreases at the greatest rate after 15 years of growing eucalyptus. This argument from Tang32 is consistent with this work (Table 6). Soil fertility generally decreases with the age of eucalyptus plantations.Table 6 Evolutionary characteristics of soil chemical indicators in eucalyptus plantation forests.Full size tableIn addition, Parfitt et al.33 studied the variation of soil fertility of pine plantations in New Zealand for a period of 20 years, and found that long-term successive rotations lead to an increase of the soil C/N ratio. Carbon is lost at a speed much greater than nitrogen. Successive rotations of eucalyptus lead to environmental issues such as decrease in soil fertility and ecological diversity and soil erosion. These would limit the sustainable management of eucalyptus plantations34,35,36,37,38,39,40.Abandonment of sample plotsWe find that many sample plots were not used for growing eucalyptus anymore after each inventory. The abandonment rate is high, ranging from 18.7 to 38.21%. The 226 eucalyptus sample plots in the 5th inventory decreased to 103 (the others are abandoned) during the 7th inventory, and the land abandonment rate was 31.33%. In the 8th and 9th inventories, the abandonment rates are 30.10% and 23.61%, respectively. The cumulative land abandonment rates are 33.63%, 54.43%, 68.15%, and 75.66% after 5, 10, 15, and 20 years of growing eucalyptus, respectively (Table 7).Table 7 Quantity (rates) of retained and abandoned sample plots after certain periods of plantation management.Full size tableThere are a total of 1843 eucalyptus plots from the 5th to 9th NFIs. In the last NFI, there are 1282 sampled plots still growing eucalyptus, and the rest 561 plots are abandoned. The averaged land abandonment rates of these plots every 5 years are 23.92%, 24.26% (43.52% cumulatively), 32.10% (68.48% cumulatively), and 23.61% (75.66% cumulatively) over 5, 10, 15, and 20 years, respectively.These data suggest that the abandonment rate of eucalyptus plantations reaches its peak (about one third) after 15 years of operation. For other time intervals (i.e., 5, 10, and 20 years), the rate remains at around 25%. This is related to the management of eucalyptus plantations in the south of China: the first eucalyptus harvest cycle is about 6 years. The second generation of eucalyptus reproduces by division propagation (sprout naturally) with 4 years of harvest cycle, and the third generation follows the same pattern. These amount to 15–16 years-long period for plantation management. Eucalyptus requires stubble-cleaning after twice of division propagations (sprout reproduction), and needs to be re-planted. This is consistent with the timing of abandonment rate peak as stated above. It is highly likely that the eucalyptus plantations are abandoned due to the low soil fertility, and plantation managers or land owners decide to stop growing eucalyptus as a result.A simple statistical model (second-order polynomial) is established between eucalyptus plantations abandonment rate and time (Fig. 6), which suggests that all plantations will stop growing eucalyptus after 50 years, and the corresponding lands will be used for other purposes. The expansion of eucalyptus plantations relies on sustained cultivation of new lands (land reclamation). The total area of eucalyptus plantations reached 5,647,400 hectares in the 9th NFI, but only 4.29% of them (that) have been continuously growing eucalyptus since the 5th NFL (i.e., 24.34% of the plots from the 5th NFI are kept).Figure 6Statistical model showing how abandonment and replanting rates of eucalyptus plantations change with time.Full size imageThere are two main reasons to explain the loss of eucalyptus plantations. The land might be taken over for non-agricultural use (e.g., infrastructure and building construction), or they could be used for growing other crops. The latter is help for soil fertility restoration and soil microorganism readjustment. As most eucalyptus plantations in China are cultivated on lands with poor growing conditions, most of them were abandoned voluntarily by the land owner or plantation manager as stated earlier.After harvest, eucalyptus plantations could be reused for the continuation of eucalyptus growing or used for other purposes (e.g., growing other crops). The plots that were temporarily not used for growing eucalyptus could be used for re-growing it under certain conditions after a certain time period. We investigate the replanting rate of the 561 abandoned eucalyptus plantations, and study whether the abandoned plantations are used for growing other outcrops, and, if so, the corresponding tree species (Tables 8, 9, 10, 11). The 6th NFI data suggests that there are 76 plots abandoned after the 5th NFI. Their replanting rates are 2.63%, 7.89% (10.53% cumulatively), 0.00% (10.53% cumulatively), and 5.26% (15.79% cumulatively) within every 5 years, and after 5, 10, and 15 years of abandonment. For all the 561 abandoned plots, replanting rates are 9.09%, 5.53% (cumulatively 14.62% within 10 years), 0.53% (cumulatively 15.15% within 15 years), 5.26% (cumulatively 15.86% within 20 years) within every 5 years, and after 5, 10, and 15 years of abandonment. These suggest that about five sixth of the abandoned plots had not replanted eucalyptus for at least 20 years since abandonment.Table 8 Land use of eucalyptus plantation sample plots during different NFIs.Full size tableTable 9 Temporal change of tree species planted in sample plots.Full size tableTable 10 Replanting rate of eucalyptus plantations.Full size tableTable 11 Productivity of plantations that have replanted eucalyptus.Full size tableA simple statistical model is established between replanting rate and time (second-order polynomial) based on the current data (Fig. 5). It suggests that the replanting rates after 30 and 50 years are around 20% and 30%, respectively. These suggest that if the plantation management does not improve significantly, it would be difficult to maintain the current supply of eucalyptus and areal distribution of its plantations in the long term. It is necessary to rely on both land rotation and cultivation of new lands to maintain the current supply of eucalyptus.The NFI data suggests that very few eucalyputs plots are turned to non-plantation purposes. The exception is from the 6th NFI in which 34.21% of plots have been used for other purposes after harvest. This rate is below 20% for all other inventory data. A lot of abandoned eucalyptus plantations are still used as plantations, and they are for growing eucalyptus, and the rate of regrowing eucalyptus tends to remain low for a long period of time (below one sixth after 20 years based on current data). This is because eucalyptus grows fast with high productivity, and it has high demand for soil fertility and water. Land rotation is necessary after a few harvest cycles to restore the soil fertility, which would take relatively long period of time before the land becomes suitable to regrow euccalyptus. Among the 561 abandoned eucalyptus plots, broad-leaf and economic tree species are the most commonly planted species after stop growing eucalyptus (e.g., rubber tree and Lychee; 18.54% and 18.36%; Table 9). The greater variability of land use for the abandoned plots suggests greater management intensity. Afforestation with eucalyptus is dominated by short rotation period (harvest cycle). Frequently modifying tree species planted within plantations helps maintain a high productivity of the land.
Carbon storage and fixation of eucalyptus plantationsVariability in carbon storageBased on the 9th NFI data and Eqs. (2–8), we calculate the BEF of eucalyptus in each province (Table 12). The results suggest that the BEF ranges from 0.982–1.652 with a weighted average of 1.236 (weight determined by stock volume).Table 12 BEF of eucalyptus by province.Full size tableCalculation from Eqs. (9) and (10) suggests that the total carbon storage (excluding harvest volume) of eucalyptus in China is 2.40 TgC (1973–1976, 1Tg = 1012 g), 4.14 TgC (1977–1981), 2.73 TgC (1984–1988), 5.42 TgC (1989–1993), 9.73 TgC (1994–1998), 12.58 TgC (1999–2003), 28.90 TgC (2004–2008), 98.61 TgC (2009–2013), and 133.00 TgC (2014–2018) in different time periods in the past 45 years (Table 13).Table 13 Eucalyptus carbon density and storage by province.Full size tableThe carbon storage of eucalyptus increased rapidly in the past 45 years especially since the end of last century. This is due to the rapid expansion of eucalyptus plantations in China, and its carbon storage in 2014–2018 is 55.42 times of that in 1973–1976. The carbon density per square hectometer also increases from 5.22 MgC (1 Mg = 106 g) in 1973–1976 to 12.16 MgC in 2014–2018, about 2.33 times of the former.Carbon fixationThe mean annual productivity of eucalyptus is 8.57 m3 hm−2 a−1 in 2014–2018 based on the 9th NFI. This is a lot greater compared to other species widely planted in the same areas (Pinus massoniana Lamb.: 2.91 m3 hm−2 a−1; Cunninghamia lanceolata Lamb.: 3.93 m3 hm−2 a−1). Using the stock volume biomass method with BEF being 1.2336 (from previous calculation) and carbon storage coefficient of 0.5, the mean annual carbon fixed by eucalyptus is 5.29 t hm−2 a−1, which are about 2.95 and 2.18 times that of Pinus massoniana Lamb. (1.79 t hm−2 a−1) and Cunninghamia lanceolata Lamb. (2.42 t hm−2 a−1), respectively. This shows that eucalyptus is characterized by high biomass productivity and high carbon fixation capability. It thus plays an important role in maintaining the carbon balance in China. More

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05 October 2021

Fund natural-history museums, not de-extinction

Corrie S. Moreau

 ORCID: http://orcid.org/0000-0003-1139-5792

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Jessica L. Ware

 ORCID: http://orcid.org/0000-0002-4066-7681

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Corrie S. Moreau

Cornell University, Ithaca, New York, USA.

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Jessica L. Ware

American Museum of Natural History, New York City, New York, USA.

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The only way to study extinct species is by leveraging the irreplaceable collections of natural-history museums. It is unfortunate, then, that instead of supporting these often imperilled institutions, private investors are spending millions on attempts to resurrect species. For example, the US start-up firm Colossal Laboratories and Biosciences, co-founded by synthetic biologist George Church, is exploring such feats.

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Nature 598, 32 (2021)
doi: https://doi.org/10.1038/d41586-021-02710-4

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Botanical content of the Libri Picturati Brazilian collectionOur identifications of all plant illustrations are listed with their vernacular names, page numbers, and associated information on growth form, geographical origin, conservation and domestication status in Supplementary Dataset S1. From the entire collection of Brazilian plant illustrations in the Libri Picturati, we identified 198 taxa that are organized in the Theatrum, LP and MC as indicated in Supplementary Table S1. Between folios 729 and 731 of the Theatrum, an illustration of a tea plant (Camellia sinensis (L.) Kuntze) is glued, which was sent by Cleyer from Batavia (currently Jakarta, Indonesia), the headquarters of the Dutch East Indian Company. As it was inserted later in the Theatrum and not depicted in Brazil, we did not include it in our analysis. A few plants remained unidentified due to a lack of morphological characters, the limited quality of the drawing and/or the lack of references to written sources by Marcgrave or Piso7,8.Among the LP botanical watercolors, we identified 34 vascular plant species (38 images) with the Passifloraceae as the most represented family (five species, six images), followed by the Fabaceae (five species, five images). Among the MC plant drawings, we identified 26 vascular plant species (34 images) and the most represented families were the Cucurbitaceae (three species, seven images) and the Myrtaceae (three species, three images). Among the illustrated content of the Theatrum, we identified 162 vascular plant species (175 images) and one basidiomycete fungus (Copelandia cyanescens (Sacc.) Singer, Bolbitiaceae). Fungi were commonly placed within the plant kingdom until the mid-twentieth century. The most represented families among the illustrated content are the Fabaceae (22 species, 22 images), followed by the Solanaceae (10 species, 11 images), Lamiaceae (six species, six images) and Myrtaceae (six species, eight images). The Fabaceae is the most diverse plant family in the world41, while the Myrtaceae is one of the most rich-species woody plant family in the Atlantic Forest in Brazil42.Mentzel’s unfinished task: the intended botanical content of the Theatrum
The Theatrum also includes 206 empty folios, interleaved between 160 folios with plant illustrations (see example in Fig. 1). On most folios, vernacular names and references to the pages of the HNB and IURNM are written on the top center, often relating to one taxon, but sometimes referring to two taxa (Fig. 1). This occurs specially at the end of the collection, as if the maker had ended up with little space and somehow had to squeeze them in. Among these unillustrated folios, the vernacular plant names and references to Marcgrave and Piso’s sources allowed us to identify 196 vascular plant species (218 records) including five ferns from the families Drypteriaceae (one species), Polypodiaceae (one species) and Pteridaceae (three species); one alga (Sargassum tenuissimum (Endlicher & Diesling) Grunow, Phaeophyceae) and a marine sponge (Clathria cf. nicoleae Vieira de Barros, Santos & Pinheiro, Microcioniadae) (Supplementary Dataset S1). Considering that the study of spongiology (Porifera) did not develop until the mid-nineteenth century, these animal colonies must have been considered an aquatic plant because of the tree-like shape and the fact of living attached to the seabed. The most represented family that would correspond to the empty folios was the Fabaceae (29 unillustrated species, 33 records), followed by the Arecaceae (nine species, ten records), Solanaceae (nine species, nine records), and Asteraceae (seven species, seven records). Estimates of the intended botanical content (i.e., empty folios with references together with the illustrated folios) are shown in Table 1.Figure 1Similar vernacular names for related taxa and distinct taxa associated to the same vernacular name in the Theatrum Rerum Naturalium.Full size imageTable 1 Estimations of the botanical content of the Theatrum Rerum Naturalium, including empty and illustrated folios.Full size tableOn p. 139 of the Theatrum, the vernacular name Ambaibuna is written on an empty page without reference to Marcgrave’s or Piso’s books. The page with Ambaibuna is located between Ambaiba (p. 137), which corresponds to the illustration of Cecropia pachystachya Trécul, and a blank page with only the vernacular name Ambaitinga (p. 141), which corresponds to C. hololeuca Miq.7: 92,24 (Fig. 1). The Brazilian Cecropia species are known in Tupi-related languages as Ambauba, Ambauva or Umbaúba (https://dataplamt.org.br/), which are phonetically and morphologically similar to Ambaibuna. For those reasons, we initially assumed that Ambaibuna referred to a Cecropia species, but the same name Ambaibuna is later repeated together with the name Iito (p. 227) next to an illustration that represents a completely different tree species: Guarea guidonia (L.) Sleumer (Fig. 1). Furthermore, the name Ambaibuna is also written above the illustration of a grapevine, Vitis vinifera L. (p. 257), also unrelated to Cecropia (Fig. 1).Whether Ambaibuna was a generic name to designate several non-related species or represents a mistake by the author who wrote the names on the illustrations remains unknown. On the other hand, neither Marcgrave nor Piso mentioned Ambaibuna in their descriptions of the Brazilian flora. Aside from Marcgrave and Piso’s books7,8, it is yet to be determined which source(s) Mentzel relied on when arranging the botanical content of the Theatrum. It is nonetheless clear that he must have been confused by the similarity of some of the Tupi-related plant names. Unfortunately, Marcgrave was no longer present to help him match the illustrations, names and descriptions, because he died about 16 years before Mentzel started organizing the Brazilian plant illustrations.Origin of the exotic species in the Libri Picturati
The Libri Picturati collection depicts in its majority native Brazilian plants. Most of the species represented in the Theatrum are native from Brazil, but the proportion of native species is much lower in the MC and lowest in the LP, in which almost half of the illustrations represent introduced species (Fig. 2).Figure 2Proportion of native and introduced species in the Brazilian collection of the Libri Picturati: Theatrum Rerum Naturalium (Theatrum), Libri Principis (LP) and Miscellanea Cleyeri (MC).Full size imageThere are 35 species of exotic origin in the complete Brazilian collection of the Libri Picturati (Supplementary Table S2). These introduced species now occur in (sub-) tropical areas around the world. Most of the exotic plants originally came from other parts of the Americas, especially Mexico, the Caribbean and the Andes region (14 species); followed by those that originated in the African continent (10 species) and tropical Asia (nine species) (Supplementary Table S2). Most of the exotic American plants that were introduced to Brazil were domesticated and traded by indigenous groups long before the European colonization, such as papaya (Carica papaya L.), cotton (Gossypium barbadense L.), sweet potato (Ipomoea batatas (L.) Lam.), beans (Phaseolus vulgaris L.), guava (Psidium guajava L.) and maize (Zea mays L.)37. Most of the species of Asiatic origin were already naturalized or cultivated in Africa and introduced to Brazil by means of the Trans-Atlantic slave trade before the Dutch arrived, such as yams (Dioscorea alata L.), plantains (Musa × paradisiaca L.) and weeds like Abrus precatorius L. and Plumbago zeylanica L.43,44. Others were introduced from Europe by merchants and settlers, such as the Portuguese Jesuits, who incorporated them as remedies into their boticas (Jesuit pharmacies in the colonies). For example, the various Citrus and pomegranate fruits were not only planted as fruits but also used to expel roundworms and to combat cold fevers, respectively45: 88. Before their arrival to Brazil, the Portuguese and Dutch must have been familiar with some African plants, such as Aloe vera (L.) Burm.f., Ricinus communis L. and Tamarindus indica L. These useful plants were already known in Europe through Arabic and Greek medical texts, which knowledge was boosted by their translations into Latin during the High Renaissance45,46. Punica granatum L. was introduced into the Iberian Peninsula via ancient merchant routes in the Mediterranean47 and brough to Brazil by the Portuguese45. Grapes (Vitis vinifera L.) were already cultivated by the Portuguese in Pernambuco around 154248. Along the Atlantic coast, lemons, pomegranates and grape vines adapted to the new environmental conditions and thrived in the vicinities of Johan Maurits’ residence, as evidenced by the illustrations in the Theatrum and textual accounts6,7,40.The presence of these globally commodified plants is common today in Brazil as in many regions worldwide. Other species seem to have lost their popularity over time. The so-called Ethiopian, Guinean or Negro pepper, Xylopia aethiopica (Dunal) A.Rich., was present around the 1640s in northeast Brazil, as evidenced in the Libri Picturati by a painting with a fruiting branch with leaves named Piperis aethiopici spés (Fig. 3a). The first iconography of this aromatic tree in Europe is found in Matthioli’s commentaries on Dioscorides under the name of Piper aethiopicum49: 575 and its fruits were previously cited by the Persian polymath Avicenna (980–1037)30. In Europe, this African pepper was commonly used until southeast Asian spices gained popularity in the sixteenth century50. In the plantation societies of tropical America, X. aethiopica constituted a food crop for enslaved Africans in the early colonial period43: 135. Today, its fruits are used in aphrodisiac tonics51 and special dishes prepared for African deities (Orishas) in Cuba43: 90, but it is unclear whether the species grows in Brazil. Its current distribution range encompasses West, Central and Southern Africa (https://gbif.org/occurrence/map?taxon_key=3157151). The dry fruits are used in tropical Africa as a condiment, in rituals and as medicine to treat cough, bronchitis, rheumatism, malaria, amenorrhea and uterine fibroids52,53,54. There is an herbarium record in Brazil made by photographer and anthropologist Pierre Verger. The label on the specimen mentions ‘Brazil’ and ‘Plantas de Candomblé’ and it indicates that the voucher was deposited at the Herbarium Alexandre Real Costa (ALCB, according to Index Herbariorum: http://sweetgum.nybg.org/science/ih/, accessed 23 August 2021) in Bahia (Verger s/n, ALCB012478, available at ALCB, via Species Link: https://specieslink.net/search/, accessed 23 August 2021) Verger presumably collected this specimen in Bahia in 1967 while he was researching on ritual and medicinal plants used in Candomblé (http://inct.florabrasil.net/alcb-resgate/, accessed 2 June 2021)55. However, it seems to be a mixed collection, as the leaves are oppositely arranged and with long petioles, which is uncommon to Annonaceae30. In Brazil, the fruits of the Brazilian relative Xylopia aromatica (Lam.) Mart. have probably served as a good substitute for X. aethiopica, as they have a similar peppery taste and stomachic properties56: 3, and are more easily gathered from the cerrado savannahs or the Amazon rainforest. Voeks57 documented X. aethiopica seed powder as used in Candomblé rituals by Yoruba practitioners in Bahia. Nevertheless, there is no clear information whether X. aethiopica is cultivated in the Neotropics or imported; thus, the origin of the fruits, seeds or its powder in Brazil remains uncertain.Figure 3 (a) The African spice-producing tree Xylopia aethiopica depicted in the Theatrum Rerum Naturalium (p. 321); (b) The first record of the sunflower (Helianthus annuus) in Brazil (Theatrum: 555).Full size imageThe first reference to the sunflower (Helianthus annuus L.) in Brazil dates to the twentieth century, when it was introduced by European immigrants due to its economic value as an oil-producing crop58. Sunflowers are of North American and/or Mexican origin 59,60, and were introduced to Europe in the sixteenth century by the Spanish, as part of the Columbian exchange61. Merchants observed how native Americans benefited from this plant and exported the sunflower to Europe, where it was primarily valued as ornamental and later as a food crop, propelled by genetic improvement by the Russians in the 1800s59. Before the sunflower became a popular and well-stablished crop in the twentieth century, this plant was already encountered in northeast Brazil, as evidenced by the illustration in the Theatrum (Fig. 3b). Portuguese sailors may have played a role in its introduction to Brazilian territories or it could have been intentionally brought by merchants or Jesuits, although the latter paid more attention to medicinal plants45,62. We may also consider the Dutch as active agents in its introduction to their colonies in the northeast. A relevant female agent in the dissemination of the sunflower in the Netherlands was Christine Bertolf (1525–1590), who was acquainted with the Spanish court and keen of the rare plants that thrived in the Royal Botanical Garden in Madrid63. She spread textual and visual information about the sunflower, and possibly also its seeds, among her network of naturalists and collectors, including the Flemish botanists Dodoens and Clusius63. After Dodoens64: 295 depicted the first European sunflower in his herbal in 1568, images and descriptions of this species began to circulate in manuscripts of other naturalists and physicians in Europe (e.g., Matthioli65: preface, Fragoso66: title page, Monardes67: 109 and Clusius68: 14–15). Thus, by the seventeenth century, Dutch scholars and collectors of exotic naturalia were familiar with sunflowers, which possibly promoted its cultivation at Johan Maurits’ gardens with ornamental purposes.Interestingly, the sunflower is referenced as Camará-guaçú, an indigenous term from the macrolinguistic Tupi family. Camará, Kamará or Cambará is a generic name given to several unrelated species, such as Lantana camara L. (Verbenaceae) and Ageratum conyzoides L. (Asteraceae) (http://www.dataplamt.org.br/, accessed 2 June 2021), both found in the Theatrum (p. 341 and 343 respectively). According to Tibiriçá69, in Tupi caa means plant and mbaraá means illness, and according to Cherini70 Cambará means “leaf of rough bark”. Hence, Camara also refers to medicinal plants with rough leaves in general. Guaçú means big and miri small71, which matches with the larger inflorescence of H. annuus in contrast to the African weed Sida rhombifolia L. (Malvaceae), documented as Camara-miri in the HNB and “used by black people as a broom to sweep the houses of their masters”7: 110. According to the Tupi-based nomenclature associated to H. annuus in the Theatrum, Tupi indigenous groups were already familiar with the sunflower in Brazil around the 1640 s.Life forms and domestication status of the Libri Picturati plantsMost of the species in the Theatrum are tropical trees, followed by shrubs, herbs, and lianas (Fig. 4). Several are rainforest trees, such as Andira fraxinifolia Benth., Garcinia brasiliensis Mart. and Syagrus coronata (Mart.) Becc. The same trend was observed for the illustrations in the MC, with trees as the most often represented life forms, followed by shrubs, lianas and herbs. Typically, the LP contains much less trees, but more small herbs, shrubs and vines that were probably found in and around Mauritsstad (i.e., the former capital of Dutch Brazil, currently a part of the Brazilian city of Recife), such as Commelina erecta L. and Turnera subulata Sm., which commonly grow in disturbed landscapes.Figure 4Proportion of life forms of the species depicted in the Brazilian collection of the Libri Picturati: Theatrum Rerum Naturalium (Theatrum), Libri Principis (LP) and Miscellanea Cleyeri (MC).Full size imageAlthough the majority of the species depicted in the Theatrum and the MC are wild forest trees, some species are found both in the wild and cultivated, such as Psidium guineense Sw., which was part of the pre-Columbian anthropogenic forests or ‘indigenous landscape’ in Brazil37,38,72. Some trees were planted in or around Recife. Hancornia speciosa Gomes, known by its Tupi-based name Mangabiba or Mangaiba [Mangabeira]7: 121, was cultivated in Mauritsstad6: 242,40. The fruit of H. speciosa (Mangaba) was harvested in great amounts as it was a highly appreciated food7: 122. Seeds were collected to plant the tree, and Marcgrave gave details about the specific locations of varieties in different northeastern locations (Salvador, Sergipe and Olinda). H. speciosa was already selected and managed by indigenous groups before colonization37, yet wild populations of this tree are still found in the Brazilian rainforest and savannah (http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB15558, accessed 4 June 2021).Domesticated plants are represented in higher proportions within the LP and the MC (Fig. 5), accounting mostly for introduced fruit species (Supplementary Dataset S1), such as Citrus spp., Musa x paradisiaca and Cocos nucifera L., which were cultivated in Maurits’ gardens in Recife40. The influence of the European colonization of Brazil is also visible by the presence of weeds from Asia and Africa among the illustrations in the Theatrum and the LP, such as Abrus precatorius L., Argemone mexicana L., Boerhavia coccinea Mill. and Plumbago zeylanica L. Some of these plants were introduced from Africa via the slave ships, while others may have dispersed naturally44. Guilandina bonduc L., an African scrambling shrub depicted as Inimboi in the Theatrum, was described by Piso7: 95 as “growing in abundance in sandy and dry forests of the coasts”. We categorized G. bonduc as a wild plant: its round seeds could have been brought by oceanic currents from West African shores and germinated in the coastal vegetation of Pernambuco and other South American areas73. However, G. bonduc may also have reached Brazil during the Trans-Atlantic slave trade, as the hard, grey seeds are used in the African game Oware and also used in bead ornaments74.Figure 5Domestication status of the species in the Brazilian collection of the Libri Picturati: Theatrum Rerum Naturalium (Theatrum), Libri Principis (LP) and Miscellanea Cleyeri (MC).Full size imagePlant parts represented in the Libri Picturati
The way plants are depicted in the Libri Picturati provides us with information about the level of botanical skills of the artists, and how closely they worked together with the naturalists in the Dutch colony. Some plants are represented by only loose parts or depicted sterile, while others show us different organs and reproductive stages, which greatly facilitated their taxonomic identification (Table 2).Table 2 Plant parts represented in the botanical illustrations of the Libri Picturati: Theatrum Rerum Naturalium (Theatrum), Libri Principis (LP) and Miscellanea Cleyeri (MC).Full size tableMost illustrations depict fertile plant species with flowers and fruits, often cut in half to show the seeds, which reveals a high level of botanical knowledge. Fertile plants are more common in the Theatrum, in a few occasions also showing their tubers, such as Spondias tuberosa Arruda, known as Umbi [Iva Umbu], of which the prominent tuber in the bottom front captures the attention of the observer (Fig. 6a). Likely associated to a scientific purpose, drawing some plant parts out of proportion corresponds to a pictorial style also observed in other iconographies. This is also the case in the Icones Plantarum Malabaricarum, which depicts plants from Ceylon (modern Sri Lanka) in the eighteenth century and often accentuates useful fruits, flowers or roots75.Figure 6 (a) Spondias tuberosa with the tuber painted in front of the branch with leaves, tiny white flowers and a detail of the immature (green) and mature (yellow) fruit in the back (Theatrum Rerum Naturalium: 261); (b) Infertile individual of Hippeastrum psittacinum (Theatrum: 389); c Ficus gomelleira leaf, probably picked from the ground (Theatrum: 157); (d) Flowering vine of Centrosema brasilianum (Libri Principis: 1); (e) Amphilophium crucigerum dry open fruit without seeds (Theatrum: 387).Full size imagePiso7: 78 indicated that roots [tubers] of S. tuberosa deserved special attention, because of the way they developed underground and their use as a refreshment [water reservoir] for feverish patients and exhausted travelers, as he experimented himself. He and Marcgrave7: 108 also described how its fruits were valued as food. This example not only provides textual and visual evidence of the field trips to the interior by these naturalists and their first-hand experiments, but also adds insights into the connectedness between artistic and scientific practices in seventeenth century Dutch Brazil. Currently S. tuberosa, known as Umbu or Umbuzeiro (https://dataplamt.org.br/), is an important economic and subsistence food resource for rural communities in semiarid regions of northeast Brazil76,77. Its specialized root system (xylopodia) bears tubers that store liquids, sugars and other nutrients and allow the survival of the tree during the dry seasons of the caatinga and central Brazilian savanna, where this species is endemic78. The water or sweet juice of these xylopodia is still used as an emergency thirst quencher in extreme arid areas of the Brazilian sertão79; also see https://www.youtube.com/watch?v=NyGNlrljAww, accessed 25 August 2012].In the Theatrum, a small proportion of plants are illustrated in their sterile stage, such as Hippeastrum psittacinum (Ker Gawl.) Herb. (Fig. 6b) or Ficus gomelleira Kunth & C.D.Bouché (Fig. 6c). Marcgrave7: 32 did not see the impressive flower of H. psittacinum as it is lacking in his observations25: 59. The Theatrum painting must have been made in the wet season in the interior of Pernambuco, when Marcgrave and the painter(s) encountered the lily with only leaves, before these fall off and make place for the mesmerizing flower25. Ficus gomelleira, depicted by a single oblong leaf with its characteristic pinnate venation (p. 157), is a large tree, up to 40 m tall (https://portal.cybertaxonomy.org/flora-guianas/node/3041, accessed 4 June 2021). It can be challenging to collect a branch, so the painter(s) or local assistants possibly picked a leaf from the ground (Fig. 6c).The LP contains mainly flowering plants (e.g., Ruellia cf. elegans Poir.), tendrillate vines (e.g., Centrosema brasilianum (L.) Benth. (Fig. 6d)) and cultivated crops, such as peanuts (Arachis hypogaea L.), pumpkins (Cucurbita pepo L.) or guava (Psidium guajava L.) (Supplementary Dataset S1). Compared to the MC and the LP, a smaller proportion of the illustrations display only flowers or fruits in the Theatrum. Yet, these deserve special attention as the reasons for only painting the reproductive organs in the three collections may differ. While in the MC and LP flowers or fruits represent species that are domesticated or more likely to be found in urban areas, such as Capsicum baccatum L. or Hancornia speciosa, the Theatrum contains more loose parts of native plants found in the rainforest. Amphilophium crucigerum (L.) L.G.Lohmann is a liana referenced by the Tupi-related name Iaruparicuraba (Theatrum: 387) and today known in Brazil as pente-de-macaco (https://dataplamt.org.br/) due to its large dehiscent fruit (c.17 cm long) that opens in two valves covered with soft spines, hence its name “monkey’s comb” (Fig. 6e). Its winged seeds are not present in the drawing, possibly one empty valve was gathered from the ground, and the seeds were already dispersed by the wind.In the MC, we also find some drawings of infertile structures, but these mostly belonged to species that were depicted on several folios. When assembling those folios, we observed the whole plant represented in its fertile stage: the watermelon (Citrullus lanatus (Thunb.) Matsum. & Nakai) is depicted with its leaves and fruit on folio 63 (verso) and its leaves on folio 64 (recto). In the case of Furcraea foetida (L.) Haw., whoever bounded the drawings in the MC collection did not realize that folios 63 (recto), 64 (verso) and double folio 68 formed together one entire plant (See Supplementary Fig. S1).On other occasions, the painters focused on painting the plant parts that were valuable to humans. Several rainforest trees were highly valued for its edible fruits or seeds, such as Hymenaea courbaril L.7: 101 or Lecythis pisonis L., of which the “seeds (also called chestnuts) were eaten raw or roasted”7: 128 and “were considered aphrodisiacs”7: 65. The fruit of Macoubea guianensis Aubl. was “appreciated for its sweetness by the indigenous peoples to eat during their travels, while Europeans used it to treat chest affections”8: 242. The fruit of Swartzia pickelii Killip ex Ducke was “not eaten unless it was cooked, from which the inhabitants made a wholesome delicacy for the stomach called Manipoy”8: 165. The same applies to the tomato-like fruits of the African eggplant Solanum aethiopicum L., which were “eaten cooked, after seasoning with oil and pepper; it has lemon taste”7: 24. While these plants are represented in the Theatrum only by their fruits (Supplementary Dataset S1), the tree branches or the whole plant are depicted in the written sources. The illustrations in the books were most likely made by Marcgrave, who aimed to describe and depict as many plant parts as possible, although compromising in aesthetic aspect. The painters, on the other hand, focused on the edible parts without sacrificing their aesthetics. In any case, the illustrations from the Theatrum and the woodcuts and descriptions in the HNB and IURNM often complemented each other and thus facilitated our identifications.Current conservation status of the Brazilian species in the Libri Picturati
In the past centuries, the Atlantic Forest and savannah regions of northeast Brazil have been severely affected by habitat loss and degradation due to the expansion of urbanization, intensive agriculture, farming and logging80,81. Several plant species that were abundant enough to be noted by European artists around 1640 are not common anymore today. According to the IUCN Red List, eight species in the Libri Picturati, seven in the Theatrum and one in the LP are currently experiencing population decline or are at risk of facing extinction (Supplementary Table S3). Several endemic plants from the northeast Atlantic rainforest and caatinga biomes appear in the illustrations. Four species in the Libri Picturati are currently CITES-listed and restricted to trade: the cacti Brasiliopuntia brasiliensis (Willd.) A.Berger, Cereus fernambucensis Lem., Epiphyllum phyllanthus (L.) Haw. and Melocactus violaceus subsp. margaritaceus N.P.Taylor The latter is an endemic cactus of the coastal sand dunes’ ecoregion in the Atlantic rainforest known as restinga, which is severely threatened by agricultural expansion and urbanization82.Some endemic species are classified as Least Concern by the IUCN or the CNC Flora (12 species), while others (13 species) have not been evaluated yet (Supplementary Dataset S1). The MC does not contain threatened species, but includes two endemic trees: Attalea compta Mart. and Eugenia cf. brasiliensis Lam., which are only found in the biodiversity hotspots of the Atlantic rainforest and the cerrado, both greatly affected by habitat loss23. The mangrove vegetation along the Brazilian coast has been severely affected by urbanization, pollution by industrial and domestic waste and climate change83,84, threatening the populations of the mangrove trees Avicennia schaueriana Stapf & Leechm. ex Moldenke and Laguncularia racemosa (L.) C.F.Gaertn. The occurrence of anthropogenic impacts and the lack of available data call for the implementation of more in-depth and continuous studies on the conservation status of these vulnerable populations.Linking the plant illustrations to the published works and Marcgrave’s herbariumA total of 357 different plant species is described in the HNB and IURNM (Supplementary Dataset S2). Because the Theatrum constitutes a larger number of illustrations, we found more taxa from the books and the herbarium represented in this source (102 out of 163, 63%). However, the largest overlap was found between the MC and the HNB / IURNM: 21 out of 26 taxa (81%) were also described in the books. A smaller overlap exists between the LP and the HNB / IURNM (18 out of 34, 53%). We counted 143 taxa at species level in Marcgrave’s herbarium (Supplementary Dataset S3) and we observed some of these preserved species in all three pictorial works, with the largest percentage of taxa in common with the MC (seven out of 26, 27%), probably because of its smaller number of images. Strikingly, a third of the species illustrated in the whole Brazilian collection of the Libri Picturati could not be ascribed to the species described by Marcgrave or Piso (61 out of 180, 34%). More