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The phototrophic species Rhodovastum atsumiense G2-11 acquired MGCs from an unknown alphaproteobacterial MTB by recent HGTIn a systematic database search for novel MGCs, we identified several orthologs of known magnetosome genes in the recently released draft genome sequence of the culturable anoxygenic phototroph Rhodovastum atsumiense G2-11 [25]. This finding was unexpected as, after isolation of G2-11 from a paddy field more than 20 years ago, no magnetosome formation has been reported [26]. Furthermore, no MTB has been identified so far among phototrophs or within the Acetobacteraceae family to which G2-11 belongs [26] (Fig. 1a).Fig. 1: Phylogeny, chromosome, and MGCs organization of G2-11.a The maximum likelihood phylogenetic tree based on ribosomal proteins demonstrates the position of G2-11 (highlighted in red) within family Acetobacteraceae (highlighted in the yellow box). The Azospirillaceae family was used as an outgroup based on the latest Alphaproteobacteria phylogeny. Branch length represents the number of base substitutions per site. Values at nodes indicate branch support calculated from 500 replicates using non-parametric bootstrap analysis. Bootstrap values 20 genes with no homology to known magnetosome genes (Fig. 1c). In contrast, the compact MGCs in G2-11 include only a few genes that could not be associated with magnetosome biosynthesis.Tetranucleotide usage patterns are frequently employed as a complementary tool to group organisms since they bear a reliable phylogenetic signal [32]. Likewise, deviations of tetranucleotide usage in a certain fragment from the flanking genome regions can indicate HGT [21]. Comparison of the z-normalized tetranucleotide frequencies of the MGCs (27.5 kb) with the flanking upstream (117.7 kb) and downstream (79.5 kb) fragments showed a considerably lower correlation between them (Pearson’s r = 0.88 with both flanking fragments) than between the flanking fragments themselves (Pearson’s r = 0.97, Fig. 1e). This indicates a significant difference in the tetranucleotide composition of the MGCs compared to the flanking genomic regions and supports a foreign origin of the magnetosome genes in G2-11 suggested by the phylogenetic analysis. Besides, the presence of a mobile element (transposase) and position of the MGCs directly downstream of a tRNA gene, a common hotspot for integration of genomic islands [33,34,35], suggests that the MGCs of G2-11 are indeed located on a genomic island, i.e., represent MAI, like in many other MTB [20, 21]. Unfortunately, the lack of other representatives of the genus Rhodovastum makes it impossible to infer whether the MAI was transferred directly to G2-11 or the last common ancestor of the genus. Nonetheless, its compact organization and conspicuous tetranucleotide usage suggest a relatively recent HGT event.G2-11 does not form magnetosomes under laboratory conditionsAlthough magnetosome genes discovered in G2-11 comply with the minimal set required for magnetosome biomineralization in MSR-1 [36], no magnetosomes have been detected in this organism. It might have several explanations: (i) the strain might switch to the magnetotactic lifestyle only under very specific, yet not tested, conditions; (ii) it once was able to synthesize magnetosomes in its natural environment but lost this ability upon subcultivation due to mutations before its characterization; (iii) the strain might naturally not exploit magnetotaxis as its genes might be non-functional or not actively expressed. To clarify which of these explanations is most likely, we first tested whether G2-11 can form magnetosomes under different laboratory conditions. To this end, the strain was cultivated photoheterotrophically, anoxic or microoxic, in a complex medium with potassium lactate and soybean peptone, as commonly used for MSR-1 (FSM) [37], as well as in minimal media with different C-sources previously shown to support growth in G2-11 (glucose, pyruvate, L-glutamine, and ethanol) [26]. All media were supplied with 50 μM ferric citrate to provide sufficient iron for magnetite biomineralization. Since magnetosome biosynthesis is possible only under low oxygen tension, aerobic chemoheterotrophic growth of G2-11 was not tested. The best growth was observed in the complex FSM medium and a minimal medium with glucose or pyruvate, whereas L-glutamine and ethanol supported only weak growth (Supplementary Fig. S3). Irrespective of the growth stage, none of the tested cultures demonstrated magnetic response as measured by a magnetically induced differential light scattering assay (Cmag) [38]. Consistently, micrographs of cells collected from stationary phase cultures did not show any magnetosome-like particles (Supplementary Fig. S3). This confirmed that G2-11 indeed cannot biosynthesize magnetosomes, at least under the conditions available for the laboratory tests. During cultivation, we also noticed that G2-11 cells did not move at any growth stage despite the initial description of this organism as motile using a single polar flagellum [26], and containing several flagellum synthesis operons and other motility-related genes. Moreover, the cells tended to adhere to glass surfaces under all tested conditions and formed a dense clumpy biofilm immersed in a thick extracellular matrix (Supplementary Fig. S3a-ii).Considering that G2-11 generally lacks magnetosomes and appears to have a stationary lifestyle, which is not consistent with magnetotaxis, we assessed whether the maintenance of MGCs comes at fitness costs for the organism. To this end, we deleted the entire region containing the magnetosome genes (in the following, referred to as the MAI region) using the genetic tools we established for G2-11 in this work (Supplementary Fig. S4a, see Materials and Methods for details). After PCR screening, replica plating test, and genome re-sequencing, two of G2-11 ΔMAI mutants were selected for further analysis (Supplementary Fig. S5). These mutants showed no significant differences in the growth behavior compared to the wildtype (WT) when incubated in minimal media supplied with acetate or pyruvate as a sole carbon source (Supplementary Fig. S4b). This finding suggests that the presence of the magnetosome genes neither provides benefits nor poses any substantial metabolic burden for G2-11, at least under the given experimental conditions.RNAseq reveals poor expression levels and antisense transcription in the MGCs of G2-11We set on to determine whether the magnetosome genes are transcribed in G2-11. To this end, we analyzed its whole transcriptome for the photoheterotrophic conditions, under which the best growth was observed, in two biological replicates. The expression levels of all the encoded genes calculated as TPM (transcripts per million) demonstrated a high correlation between the two replicates (Pearson’s r = 0.98). Most genes of the (mms6-like1)(mmsF-like1)mamH1IEKLMOH2 cluster were only poorly or not transcribed at all (Fig. 2a, Supplementary dataset). Transcription of mms6-like1, mamF-like1, mamL, mamH1, mamI, and mamK, for example, did not pass the noise background threshold (TPM ≤ 2) in both replicates and were unlikely to be expressed, whereas mamE, mamM, mamH2, feoAm, and feoBm slightly exceeded the threshold in at least one replicate and might be weakly transcribed (Fig. 2a). Although the TPM of mamO (TPM = 5.67–6.10, Supplementary dataset) exceeded the background threshold, the coverage plot reveals that the number of mapped reads sharply rises at its 3’-end, whereas the 5’-end has low read coverage (Fig. 2b). This indicates the presence of an internal transcription start site (TSS) and its associated promoter within the coding sequence of mamO instead of the full transcription of the gene. Localization of an active promoter within mamO was recently described in MSR-1, suggesting that the transcriptional organization of MGCs may be more broadly conserved across MTB than assumed previously [39].Fig. 2: Transcription of the magnetosome genes in G2-11.a Log10 of the transcript abundances for all genes in the G2-11 genome presented as TPM (transcripts per million). Red dots represent the magnetosome genes. Red rectangle shows genes with TPM below the threshold, and blue rectangle shows genes with expression levels above median. R1 and R2: biological replicates. Pearson’s r and the p value is presented on the graph. b RNAseq coverage of reads mapped on the positive (red) and negative (blue) strands of the genome in the MAI region. The gray balk shows the gene map: genes encoded on the negative strand are colored in black, on the positive – in green. Red arrows indicate the anti-sense transcription in the mamPAQRBST operon. Green arrows indicate the intragenic TSS within mamO. TSS are indicated with dashed lines and black arrowheads that show the direction of transcription.Full size imageTranscription of genes within the mag123, (mms6-like2)(mmsF-like2), and mamAPQRBST clusters significantly exceeded the threshold, with the expression levels of mag1, mamT, and mamS being above the overall median. At the same time, antisense transcription was detected in the mamAPQRBST region, with the coverage considerably exceeding the sense transcription (Fig. 2b). This antisense RNA (asRNA) likely originated from a promoter controlling the tRNA gene positioned on the negative strand downstream of mamT. Such long asRNAs have the potential to interfere with sense transcripts, thereby significantly decreasing the expression of genes encoded on the opposite strand [40].In summary, the RNAseq data revealed extremely low or lack of transcription of several genes that are known to be essential for magnetosome biosynthesis (mamL, mamI, mamM, mamE, and mamO) [27, 41]. Additionally, the detected antisense transcription can potentially attenuate expression of the mamAPQRBST cluster that also comprises essential genes, i.e., mamQ and mamB. Although other factors, like the absence of several accessory genes mentioned above and the potential accumulation of point mutations, might also be involved, the lack or insufficient transcription of the essential magnetosome genes appears to be the primary reason for the absence of magnetosome biosynthesis in G2-11.Magnetosome proteins from G2-11 are functional in a model magnetotactic bacteriumAlthough visual inspection of the G2-11 magnetosome genes did not reveal any frameshifts or other apparent mutations, accumulation of non-obvious functionally deleterious point substitutions in the essential genes could not be excluded. Therefore, we next tested whether at least some of the magnetosome genes from G2-11 still encode functional proteins that can complement isogenic mutants of the model magnetotactic bacterium MSR-1. In addition, we analyzed the intracellular localization of their products in both MSR-1 and G2-11 by fluorescent labeling.One of the key proteins for magnetosome biosynthesis in MSR-1 is MamB, as its deletion mutant is severely impaired in magnetosome vesicle formation and is entirely devoid of magnetite crystals [42, 43]. Here, we observed that expression of MamB[G2-11] partially restored magnetosome chain formation in MSR-1 ΔmamB (Fig. 3a, b-i, b-ii). Consistently, MamB[G2-11] tagged with mNeonGreen (MamB[G2-11]-mNG) was predominantly localized to magnetosome chains in MSR-1, suggesting that the magnetosome vesicle formation was likely restored to the WT levels (Fig. 3b-iii).Fig. 3: Genetic complementation and intracellular localization of magnetosome proteins from G2-11 in MSR-1 isogenic mutants.a TEM micrograph of MSR-1 wildtype (WT). b MSR-1 ΔmamB::mamB[G2-11]. b-i TEM micrograph and b-ii magnetosome chain close-up; b-iii) 3D-SIM Z-stack maximum intensity projection of MSR-1 ΔmamB::mamB[G2-11]-mNG. c MSR-1ΔmamQ::mamQ[G2-11]. c-i TEM micrograph and c-ii close-up of the particles; c-iii 3D-SIM Z-stack maximum intensity projection. d MSR-1 ΔmamK::mamK[G2-11]. d-i TEM micrograph of MSR-1 ΔmamK; d-ii TEM micrograph of MSR-1 ΔmamK::mamK[G2-11]; d-iii 3D-SIM Z-stack maximum intensity projection of MSR-1 ΔmamK::mNG-mamK[G2-11]. e MSR-1 ΔmamKY::mamK[G2-11]. e-i-ii Representative cells of MSR-1 ΔmamKY mutant showing examples of a short chain, cluster (e-i), and ring-shaped chain (e-ii); (e-iii) TEM micrograph of MSR ΔmamKY::mamK[G2-11] mutant showing the complemented phenotype; e-iv distribution of cells with different phenotypes in the populations of MSR-1 ΔmamKY and MSR-1 ΔmamKY::mamK[G2-11] mutants (N  > 50 cells for each strain population); e-v 3D-SIM Z-stack maximum intensity projection of MSR-1 ΔmamKY::mNG-mamK[G2-11]. f MSR-1 ΔmamJ::mamJ-like[G2-11]. f-i TEM micrograph of MSR-1 ΔmamJ; f-ii TEM micrograph of MSR-1 ΔmamJ::mamJ-like[G2-11]; f-iii 3D-SIM Z-stack maximum intensity projection of MSR-1 ΔmamJ::mamJ-like[G2-11]-gfp. g MSR-1 ΔF3::mmsF-like1[G2-11] and ΔF3::mmsF-like2[G2-11]. g-i TEM micrograph of MSR-1 ΔF3; g-ii TEM micrograph of MSR-1 ΔF3::mmsF-like1[G2-11]; g-iii TEM micrograph of MSR-1 ΔF3::mmsF-like2[G2-11]; g-iv magnetosome diameter distribution in MSR-1 ΔF3 and the mutants complemented with mmsF-like1/mmsF-like2. Asterisks indicate points of significance calculated using Kruskal–Wallis test (****p 50 cells for each of two randomly selected insertion mutants MSR-1 ΔmamKY::mamK[G2-11] revealed that the long magnetosome chains were restored in 35-40% of the population (Fig. 3e-iv). Of note, mNG-MamK[G2-11] formed slightly shorter filaments in MSR-1 ΔmamKY than in ΔmamK, which were also characteristically displaced to the outer cell curvature due to the lack of mamY [46] (Fig. 3e-v).MamJ attaches magnetosomes to the MamK filament in MSR-1, mediating their chain-like arrangement. Elimination of mamJ disrupts this linkage, causing magnetosomes to aggregate owing to magnetic interactions [47] (Fig. 3f-i). In MSR-1, MamJ is encoded within the mamAB operon, between mamE and mamK. Within the (mms6-like1)(mmsF-like1)mamH1IEKLMOH2 cluster of G2-11, there is an open reading frame (ORF) encoding a hypothetical protein that is located in a syntenic locus (Fig. 1c). Although the hypothetical protein from G2-11 and MamJ from MSR-1 differ considerably in length (563 vs. 426 aa), share only a low overall sequence similarity (31%), and are not identified as orthologues by reciprocal blast analyses, multiple sequence alignments revealed a few conserved amino acids at their N- and C-termini (Supplementary Fig. S6). Moreover, in both proteins, these conserved residues are separated by a large region rich in acidic residues (pI 3.3 and 3.2) suggesting that the G2-11 protein might be a distant MamJ homolog. To test if it implements the same function as MamJ, we transferred this gene to MSR-1 ΔmamJ. Interestingly, it indeed restored chain-like magnetosome arrangement, which, however, often appeared as closed rings rather than linear chains (Fig. 3f-ii). Despite this difference, it indicated the ability of the hypothetical protein (hereafter referred to as MamJ-like[G2-11]) to attach magnetosomes to MamK, suggesting that in the native context, it can have a function identical to MamJ. Consistently, its fluorescently labeled version was often observed in ring-like structures within the cytoplasm of MSR-1 ΔmamJ, suggesting that it is indeed localized to magnetosomes (Fig. 3f-iii).In magnetospirilla, magnetosome proteins MmsF, MamF, and MmxF share an extensive similarity. Their individual and collective elimination gradually reduces the magnetite crystal size and disrupts the chain formation in MSR-1 (Fig. 3g-i; Paulus, manuscript in preparation). The MAI of G2-11 includes two genes, whose products have high similarity to these proteins, designated here as MmsF-like1[G2-11] and MmsF-like2[G2-11]. Expression of each of them in the MSR-1 ΔmmsFΔmamFΔmmxF triple mutant (ΔF3) partially restored the magnetosome size and led to the formation of short magnetosome chains in MSR ΔF3::mmsF-like1[G2-11] (Fig. 3g-ii) or clusters in MSR-1 ΔF3::mmsF-like2[G2-11] (Fig. 3g-iii, iv). Consistently, fluorescently tagged mNG-MmsF-like1[G2-11] and mNG-MmsF-like2[G2-11] localized to magnetosomes in the pattern resembling that in the TEM micrographs of the complemented corresponding mutants (Fig. 3g-v, vii), or were perfectly targeted to the magnetosome chains in MSR-1 WT (Fig. 3g-vi, viii).In G2-11, MamB[G2-11]-mNG, mNG-MamQ[G2-11], MamJ-like[G2-11]-GFP, mNG-MmsF-like1[G2-11], and mNG-MmsF-like2[G2-11] were patchy-like or evenly distributed in the inner and intracellular membranes (Supplementary Fig. S7). No linear structures that would indicate the formation of aligned magnetosome vesicles were observed in these mutants. As expected, mNG-MamK[G2-11] formed filaments in G2-11 (Supplementary Fig. S7c).Expression of MamM, MamO, MamE, and MamL failed to complement the corresponding deletion mutants of MSR-1 (not shown). Although detrimental mutations in the genes cannot be excluded, this result can be attributed to the lack of their native, cognate interaction partners, likely due to the large phylogenetic distances between the respective orthologues.Transfer of MGCs from MSR-1 endows G2-11 with magnetosome biosynthesis that is rapidly lost upon subcultivationHaving demonstrated the functionality of several G2-11 magnetosome genes in the MSR-1 background, we wondered whether, conversely, the G2-11 background is permissive for magnetosome biosynthesis. To this end, we transferred the well-studied MGCs from MSR-1 into G2-11, thereby mimicking an HGT event under laboratory conditions. The magnetosome genes from MSR-1 were previously cloned on a single vector pTpsMAG1 to enable the one-step transfer and random insertion into the genomes of foreign organisms [23]. Three G2-11 mutants with different positions of the integrated magnetosome cassette were incubated under anoxic phototrophic conditions with iron concentrations (50 μM) sufficient for biomineralization in the donor organism MSR-1. The obtained transgenic strains indeed demonstrated a detectable magnetic response (Cmag = 0.38 ± 0.11) [38], and TEM confirmed the presence of numerous electron-dense particles within the cells (Fig. 4), which, however, were significantly smaller than magnetosome crystals of MSR-1 (ranging 18.5 ± 4.3 nm to 19.9 ± 5.0 nm in three G2-11 MAG insertion mutants vs 35.4 ± 11.5 nm in MSR-1 WT, Fig. 4b) and formed only short chains or were scattered throughout the cells (Fig. 4a, c-i). Mapping of the particle elemental compositions with energy-dispersive X-ray spectroscopy (EDS) in STEM mode revealed iron- and oxygen-dominated compositions, suggesting they were iron oxides. High-resolution TEM (HRTEM) images and their FFT (Fast Fourier Transform) patterns were consistent with the structure of magnetite (Fig. 4c). Thus, G2-11 was capable of genuine magnetosome formation after acquisition of the MGCs from MSR-1.Fig. 4: Magnetosome biosynthesis by G2-11 upon transfer of the MGCs from MSR-1.a A cell with magnetosomes (i) and a close-up of the area with magnetosome chains (ii). Scale bars: 1 µm. b Violin plots displaying magnetosome diameter in three MAG insertion mutants of G2-11 in comparison to MSR-1. Asterisks indicate points of significance calculated using the Kruskal–Wallis test (**** designates p  More

Human-modified forests, such as selectively logged forests, are often characterized as degraded ecosystems because of their altered structure and low biomass. The concept of ecosystem degradation can be a double-edged sword. It rightly draws attention to the conservation value of old-growth systems and the importance of ecosystem restoration. However, it can also suggest that human-modified ecosystems are of low ecological value and therefore, in some cases, suitable for conversion to agriculture (such as oil palm plantations) and other land uses3,4,5.Selectively logged and other forms of structurally altered forests are becoming the prevailing vegetation cover in much of the tropical forest biome2. Such disturbance frequently leads to a decline in old-growth specialist species1, and also in non-specialist species in some contexts6,7,8. However, species-focused biodiversity metrics are only one measure of ecosystem vitality and functionality, and rarely consider the collective role that suites of species play in maintaining ecological functions9.An alternative approach is to focus on the energetics of key taxonomic groups, and the number and relative dominance of species contributing to each energetic pathway. Energetic approaches to examining ecosystem structure and function have a long history in ecosystem ecology10. Virtually all ecosystems are powered by a cascade of captured sunlight through an array of autotroph tissues and into hierarchical assemblages of herbivores, carnivores and detritivores. Energetic approaches shine light on the relative significance of energy flows among key taxa and provide insight into the processes that shape biodiversity and ecosystem function. The common currency of energy enables diverse guilds and taxa to be compared in a unified and physically meaningful manner: dominant energetic pathways can be identified, and the resilience of each pathway to the loss of individual species can be assessed. Quantitative links can then be made between animal communities and the plant-based ecosystem productivity on which they depend. The magnitude of energetic pathways in particular animal groups can often be indicators of key associated ecosystem processes, such as nutrient cycling, seed dispersal and pollination, or trophic factors such as intensity of predation pressure or availability of resource supply, all unified under the common metric of energy flux11,12.Energetics approaches have rarely been applied in biodiverse tropical ecosystems because of the range of observations they require11,12,13. Such analyses rely on: population density estimates for a very large number of species; understanding of the diet and feeding behaviour of the species; and reliable estimation of net primary productivity (NPP). Here we take advantage of uniquely rich datasets to apply an energetics lens to examine and quantify aspects of the ecological function and vitality of habitats in Sabah, Malaysia, that comprise old-growth forests, logged forest and oil palm plantation (Fig. 1 and Extended Data Fig. 1). Our approach is to calculate the short-term equilibrium production or consumption rates of food energy by specific species, guilds or taxonomic groups. We focus on three taxonomic groups (plants, birds and mammals) that are frequently used indicators of biodiversity and are relatively well understood ecologically.Fig. 1: Maps of the study sites in Sabah, Borneo.a–d, Maps showing locations of NPP plots and biodiversity surveys in old-growth forest, logged forest and oil palm plantations in the Stability of Altered Forest Ecosystems Project landscape (a), Maliau Basin (b), Danum Valley (c) and Sepilok (d). The inset in a shows the location of the four sites in Sabah. The shade of green indicates old-growth (dark green), twice-logged (intermediate green) or heavily logged (light green) forests. The camera and trap grid includes cameras and small mammal traps. White areas indicate oil palm plantations.Full size imageWe are interested in the fraction of primary productivity consumed by birds and mammals, and how it varies along the disturbance gradient, and how and why various food energetic pathways in mammals and birds, and the diversity of species contributing to those pathways, vary along the disturbance gradient. To estimate the density of 104 mammal and 144 bird species in each of the three habitat types, we aggregated data from 882 camera sampling locations (a total of 42,877 camera trap nights), 508 bird point count locations, 1,488 small terrestrial mammal trap locations (34,058 live-trap nights) and 336 bat trap locations (Fig. 1 and Extended Data Fig. 1). We then calculated daily energetic expenditure for each species based on their body mass, assigned each species to a dietary group and calculated total food consumption in energy units. For primary productivity, we relied on 34 plot-years (summation of plots multiplied by the number of years each plot is monitored) of measurements of the key components of NPP (canopy litterfall, woody growth, fine root production) using the protocols of the Global Ecosystem Monitoring Network14,15,16 across old-growth (n = 4), logged (n = 5) and oil palm (n = 1) plots. This dataset encompasses more than 14,000 measurements of litterfall, 20,000 tree diameter measurements and 2,700 fine root samples.Overall bird species diversity is maintained across the disturbance gradient and peaks in the logged forest; for mammals, there is also a slight increase in the logged forest, followed by rapid decline in the oil palm (Fig. 2b,c). Strikingly, both bird and mammal biomass increases substantially (144% and 231%, respectively) in the logged forest compared to the old-growth forest, with mammals contributing about 75% of total (bird plus mammal) biomass in both habitat types (Fig. 2b,c).Fig. 2: Variation of ecosystem energetics along the disturbance gradient from old-growth forest through logged forest to oil palm.a, Total NPP along the gradient (mean of intensive 1-ha plots; n = 4 for old growth (OG), n = 5 for logged and n = 1 for oil palm (OP); error bars are 95% confidence intervals derived from propagated uncertainty in the individually measured NPP components), with individual plot data points overlaid. b,c, Total body mass (bars, left axis) and number of species counted (blue dots and line, right axis) of birds (b) and mammals (c). d,e, Total direct energetic food intake by birds (d) and mammals (e). f,g, Percentage of NPP directly consumed by birds (f) and mammals (g). In b–e, body mass and energetics were estimated for individual bird and mammal species, with the bars showing the sum. Error bars denote 95% confidence intervals derived from 10,000 Monte Carlo simulation estimates incorporating uncertainty in body mass, population density, the daily energy expenditure equation, assimilation efficiency of the different food types, composition of the diet of each species and NPP. In f,g, the grey bars indicate direct consumption of NPP, white bars denote the percentage of NPP indirectly supporting bird and mammal food intake when the mean trophic level of consumed invertebrates is assumed to be 2.5, with the error bars denoting assumed mean trophic levels of 2.4 and 2.6. Note the log scale of the y axis in f,g. Numbers for d,e provided in Supplementary Data Tables 1, 2.Full size imageThe total flow of energy through consumption is amplified across all energetic pathways by a factor of 2.5 (2.2–3.0; all ranges reported are 95% confidence intervals) in logged forest relative to old-growth forest. In all three habitat types, total energy intake by birds is much greater than by mammals (Fig. 2d,e and Extended Data Table 1). Birds account for 67%, 68% and 90% of the total direct consumption by birds and mammals combined in old-growth forests, logged forests and oil palm, respectively. Although mammal biomass is higher than bird biomass in the old-growth and logged forests, the metabolism per unit mass is much higher in birds because of their small body size; hence, in terms of the energetics and consumption rates, the bird community dominates. The total energy intake by birds alone increases by a factor of 2.6 (2.1–3.2) in the logged forest relative to old-growth forest. This is mainly driven by a 2.5-fold (1.7–2.8) increase in foliage-gleaning insectivory (the dominant energetic pathway), and most other feeding guilds also show an even larger increase (Figs. 2d and 3). However, total bird energy intake in the oil palm drops back to levels similar to those in the old-growth forest, with a collapse in multiple guilds. For mammals, there is a similar 2.4-fold (1.9–3.2) increase in total consumption when going from old-growth to logged forest, but this declines sharply in oil palm plantation. Most notable is the 5.7-fold (3.2–10.2) increase in the importance of terrestrial mammal herbivores in the logged relative to old-growth forests. All four individual old-growth forest sites show consistently lower bird and mammal energetics than the logged forests (Extended Data Fig. 5).Fig. 3: Magnitude and species diversity of energetic pathways in old-growth forest, logged forest and oil palm.The size of the circles indicates the magnitude of energy flow, and the colour indicates birds or mammals. S, number of species; E, ESWI, an index of species redundancy and, therefore, resilience (high values indicate high redundancy; see main text). For clarity, guilds with small energetic flows are not shown, but are listed in Supplementary Data 4. Images created by J. Bentley.Full size imageThe fraction of NPP flowing through the bird and mammal communities increases by a factor of 2.1 (1.5–3.0) in logged forest relative to old-growth forest. There is very little increase in NPP in logged relative to old-growth forests (Fig. 2a) because increased NPP in patches of relatively intact logged forest is offset by very low productivity in more structurally degraded areas such as former logging platforms14,15. In oil palm plantations, oil palm fruits account for a large proportion of NPP, although a large fraction of these is harvested and removed from the ecosystem17. As a proportion of NPP, 1.62% (1.35–2.13%) is directly consumed by birds and mammals in the old-growth forest; this rises to 3.36% (2.57–5.07%) in the logged forest but drops to 0.89% (0.57–1.44%) in oil palm (Fig. 2f,g and Extended Data Table 2).If all invertebrates consumed are herbivores or detritivores (that is, at a trophic level of 2.0), and trophic efficiency is 10% (ref. 10), the total amount of NPP supporting the combined bird and mammal food intake would be 9%, 16% and 5% for old-growth forest, logged forest and oil palm, respectively. However, if the mean trophic level of consumed invertebrates is 2.5 (that is, a mix of herbivores and predators), the corresponding proportions would be 27%, 51% and 17% (Fig. 2f,g). As insectivory is the dominant feeding mode for the avian community, these numbers are dominated by bird diets. For birds in the old-growth forests, 0.35% of NPP supports direct herbivory and frugivory, but around 22% of NPP (assumed invertebrate trophic level 2.5) is indirectly required to support insectivory. The equivalent numbers for birds in logged forest are 0.83% and 46%. Hence, birds account for a much larger indirect consumption of NPP. Bird diet studies in old-growth and logged forest in the region suggest that consumed invertebrates have a mean trophic level of 2.5 (ref. 18; K. Sam, personal communication), indicating that the higher-end estimates of indirect NPP consumption (that is, around 50% in logged forests) are plausible.It is interesting to compare such high fractions of NPP to direct estimates of invertebrate herbivory. Scans of tree leaf litter from these forests suggest that just 7.0% of tree canopy leaf area (1–3% of total NPP) is removed by tree leaf herbivory14,16, but such estimates do not include other pathways available to invertebrates, including herbivory of the understorey, aboveground and belowground sap-sucking, leaf-mining, fruit- and wood-feeding, and canopy, litter and ground-layer detritivory. An increase in invertebrate biomass and herbivory in logged forest compared to old-growth forest has previously been reported in fogging studies in this landscape19. Such high levels of consumption of NPP by invertebrates could have implications on ecosystem vegetation biomass production, suggesting, first, that invertebrate herbivory has a substantial influence on recovery from logging and, second, that insectivorous bird densities may exert substantial indirect controls on ecosystem recovery.The distributions of energy flows among feeding guilds are remarkably stable among habitat types (Fig. 3), indicating that the amplified energy flows in the logged forests do not distort the overall trophic structure of vertebrate communities. Overall bird diet energetics are dominated by insectivory, which accounts for a strikingly invariant 66%, 63% and 66% of bird energetic consumption in old-growth forest, logged forest and oil palm, respectively. Foliage-gleaning dominates as a mode of invertebrate consumption in all three habitat types, with frugivory being the second most energetically important feeding mode (26%, 27% and 19%, respectively). Mammal diet is more evenly distributed across feeding guilds, but frugivory (31%, 30%, 30%) and folivory (24%, 38%, 26%) dominate. Small mammal insectivores are probably under-sampled (see Methods) so the contribution of mammal insectivory may be slightly greater than that estimated here. The apparent constancy of relative magnitude of feeding pathways across the intact and disturbed ecosystems is noteworthy and not sensitive to plausible shifts in feeding behaviour between habitat types (see Supplementary Discussion). There is no evidence of a substantial shift in dominant feeding guild: the principal feeding pathways present in the old-growth forest are maintained in the logged forest.When examining change at species level in the logged forests, the largest absolute increases in bird food consumption were in arboreal insectivores and omnivores (Fig. 4a and Extended Data Fig. 2a). In particular, this change was characterized by large increases in the abundance of bulbul species (Pycnonotus spp.). No bird species showed a significant or substantial reduction in overall energy consumption. In the oil palm plantation, total food consumption by birds was less than in logged forests, but similar to that in old-growth forests. However, this was driven by very high abundance of a handful of species, notably a single arboreal omnivore (yellow-vented bulbul Pycnonotus goiavier) and three arboreal insectivores (Mixornis bornensis, Rhipidura javanica, Copsychus saularis), whereas energy flows through most other bird species were greatly reduced (Fig. 4b and Extended Data Fig. 2b).Fig. 4: Changes in energy consumption by species in logged forest and oil palm relative to old-growth forest.a,b, Changes in energy consumption by species in logged forest relative to old-growth forest (a) and in oil palm relative to old-growth forest (b). The 20 species experiencing the largest increase (red) and decrease (blue) in both habitat types are shown. Bird species are shown in a lighter tone and mammal species are shown in a darker tone. The error bars denote 95% confidence intervals, derived from 10,000 Monte Carlo simulation estimates incorporating uncertainty in body mass, population density, the daily energy expenditure equation, assimilation efficiency of the different food types and composition of the diet of each species.Full size imageFor mammals, the increase in consumption in logged forests is dominated by consumption by large terrestrial herbivores increasing by a factor of 5.7 (3.2–10.2), particularly sambar deer (Rusa unicolor) and Asian elephant (Elephas maximus; Fig. 4a and Extended Data Figs. 2b and 3), along with that by small omnivores, predominantly rodents (native spiny rats, non-native black rat; Fig. 4). A few rainforest species show a strong decline (for example, greater mouse-deer Tragulus napu and brown spiny rat Maxomys rajah). In the oil palm, most mammal species collapse (Fig. 4b) and the limited consumption is dominated by a few disturbance-tolerant habitat generalists (for example, red muntjac Muntiacus muntjak, black rat Rattus rattus, civets), albeit these species are at lower densities than observed in old-growth forest (Extended Data Fig. 2).With very few exceptions, the amplified energy flows in logged forest seem to retain the same level of resilience as in old-growth forest. The diversity and dominance of species within any pathway can be a measure of the resilience of that pathway to loss of species. We assessed energetic dominance within individual pathways by defining an energetic Shannon–Wiener index (ESWI) to examine distribution of energy flow across species; low ESWI indicates a pathway with high dependence on a few species and hence potential vulnerability (Fig. 3). The overall ESWI across guilds does not differ between the old-growth and logged forest (t2,34 = −0.363, P = 0.930), but does decline substantially from old-growth forest to oil palm (t2,34 = −3.826, P = 0.0015), and from logged forest to oil palm (t2,34 = −3.639, P = 0.0025; linear mixed-effects models, with habitat type as fixed effect and guild as random effect; for model coefficients see Supplementary Table 3).Hence, for birds, the diversity of species contributing to dominant energetic pathways is maintained in the transition from old-growth to logged forests but declines substantially in oil palm. Mammals generally show lower diversity and ESWI than birds, but six out of ten feeding guilds maintain or increase ESWI in logged forest relative to the old-growth forests but collapse in oil palm (Fig. 3). Terrestrial herbivory is the largest mammal pathway in the logged forest but is dependent on only four species and is probably the most vulnerable of the larger pathways: a few large mammals (especially sambar deer) play a dominant terrestrial herbivory role in the logged forest. In parallel, bearded pigs (Sus barbatus), the only wild suid in Borneo, form an important and functionally unique component of the terrestrial omnivory pathway. These larger animals are particularly sensitive to anthropogenic pressures such as hunting, or associated pathogenic pressures as evidenced by the recent precipitous decline of the bearded pig in Sabah due to an outbreak of Asian swine fever (after our data were collected)20.Vertebrate populations across the tropics are particularly sensitive to hunting pressure21. Our study site has little hunting, but as a sensitivity analysis we explored the energetic consequences of 50% reduction in population density of those species potentially affected by targeted and/or indiscriminate hunting (Extended Data Fig. 4). Targeted hunted species include commercially valuable birds, and gun-hunted mammals (bearded pig, ungulates, banteng and mammals with medicinal value). Indiscriminately hunted species include birds and mammals likely to be trapped with nets and snares. Hunting in the logged forests lowers both bird and mammal energy flows but still leaves them at levels higher than in faunally intact old-growth forests. Such hunting brings bird energetics levels close to (but still above) those of old-growth forests. For mammals, however, even intensively hunted logged forests seem to maintain higher energetic flows than the old-growth forests. Hence, only very heavy hunting is likely to ‘offset’ the amplified energetics in the logged forest.The amplified energetic pathways in our logged forest probably arise as a result of bottom-up trophic factors including increased resource supply, palatability and accessibility. The more open forest structure in logged forest results in more vegetation being near ground level22,23 and hence more accessible to large generalist mammal herbivores, which show the most striking increase of the mammal guilds. The increased prioritization by plants of competition for light and therefore rapid vegetation growth strategies in logged forests results in higher leaf nutrient content and reduced leaf chemical defences against herbivory24,25, along with higher fruiting and flowering rates19 and greater clumping in resource supply9. This increased resource availability and palatability probably supports high invertebrate and vertebrate herbivore densities25. The act of disturbance displaces the ecosystem from a conservative chemically defended state to a more dynamic state with amplified energy and nutrient flow, but not to an extent that causes heavy disruption in animal community composition. Top-down trophic factors might also play a role in amplifying the energy flows in intermediate trophic levels, through mechanisms such as increased protection of ground-dwelling or nesting mammals and birds from aerial predators in the dense vegetation ground layer. This might partially explain the increased abundance of rodents, but there is little evidence of trophic release at this site because of the persisting high density of mammal carnivores26. Overall, the larger number of bottom-up mechanisms and surge in invertebrate consumption suggest that increased resource supply and palatability largely explains the amplification of consumption pathways in the logged forest. An alternative possibility is that the amplified vertebrate energetics do not indicate amplified overall animal energetics but rather a large diversion of energy from unmeasured invertebrate predation pathways (for example, parasitoids); this seems unlikely but warrants further exploration.Oil palm plantations show a large decline in the proportion of NPP consumed by mammals and birds compared to logged forests12. Mammal populations collapse because they are more vulnerable and avoid humans, and there is no suite of mammal generalists that can step in27,28. Birds show a more modest decline, to levels similar to those observed in old-growth forests, as there is a broad suite of generalist species that are able to adapt to and exploit the habitat types across the disturbance gradient, and because their small size and mobility render them less sensitive to human activity29. There is a consistent decline in the oil palm in ESWI for birds and especially for mammals, indicating a substantial increase in ecosystem vulnerability in many pathways.In conclusion, our analysis demonstrates the tremendously dynamic and ecologically vibrant nature of the studied logged forests, even heavily and repeatedly logged forests such as those found across Borneo. It is likely that the patterns, mechanisms and basic ecological energetics we describe are general to most tropical forests; amplification of multiple ecosystem processes after logging has also been reported for logged forests in Kenya9, but similar detailed analyses are needed for a range of tropical forests to elucidate the importance of biogeographic, climatic or other factors. We stress that our findings do not diminish the importance of protecting structurally intact old-growth forests, but rather question the meaning of degradation by shining a new light on the ecological value of logged and other structurally ‘degraded’ forests, reinforcing their significance to the conservation agenda30. We have shown that a wide diversity of species not only persist but thrive in the logged forest environment. Moreover, such ecological vibrancy probably enhances the prospects for ecosystem structural recovery. In terms of faunal intactness, our study landscape is close to a best-case scenario because hunting pressures were low. If logged forests can be protected from heavy defaunation, our analysis demonstrates that they can be vibrant ecosystems, providing many key ecosystem functions at levels much higher than in old-growth forests. Conservation of logged forest landscapes has an essential role to play in the in the protection of global biodiversity and biosphere function. More

Study area and soil collectionTwenty NRCS map units were selected across Hawaii Commercial & Sugar Company (HC&S) in central Maui that represented seven soil orders, 10 NRCS soil series, and approximately 77% of the total plantation area (Fig. 1). Soil heterogeneity across the landscape allowed for the comparison of a continuum of soil and soil properties that have experienced the same C4 grass inputs and agricultural treatment under sugarcane production for over 100 years. Conventional sugarcane production involved 2-year growth followed by harvest burn, collection of remaining stalks by mechanical ripper, deep tillage to 40 cm, no crop rotations, and little to no residue return. The sampled soils, collected from September-August 2015, thus represent a baseline of SOC after input-intensive tropical agriculture and long-term soil disturbance. Elemental analyses from this work show consistent agricultural disturbances led to degraded SOC content ranging from 0.23 to 2.91% SOC of soil mass with an average of only 1.16% SOC across all locations and depths.Figure 1Hawaiian Commercial and Sugar in central Maui with main Hawaiian Islands inset (left). Soil series identified by NRCS across HC&S fields (right) with black dots indicating 20 locations where soils were sampled to test landscape level differences in topical soil kinetics and associated soil properties under conventional sugarcane. Maps from Ref.19 created using ESRI ArcGIS with soil series data from: Soil Survey Staff, Natural Resources Conservation Service, United States Department of Agriculture, Web Soil Survey, Available online at http://websoilsurvey.nrcs.usda.gov/. Accessed [07/30/2016]19.Full size imageThe homogenized land use history allowed focused investigation of soil property effects on SOC storage across heterogenous soils (Table 1). Though soil inputs (e.g. water, nutrients, root inputs, residue removal) and disturbance regimes (e.g. burn, rip, till, compaction, no crop rotation) were consistent across the 20 field locations, average annual surface temperatures varied from 22.9 to 25.1 °C with a mean of 24.4 °C, average annual relative humidity varied from 70.4 to 79.2% with a mean of 73.4%, and average annual rainfall varied from 306 to 1493 mm with a mean of 575 mm. Gradients of rainfall, relative humidity, and elevation across the site generally increase in an east/north-east direction towards the prevailing winds and up the western slope of Haleakalā. In contrast, surface temperatures increase in the opposite direction towards Kihei and the southern tip of the West Maui Mountains.Table 1 NRCS soil classification and environmental conditions at 20 field sites.Full size tableaSoil descriptions26.bInterpolated estimates from Ref.25.Soil sampling and analysisPit locations were identified with a handheld GPS and were sampled using NRCS Rapid Carbon Assessment methods27. A total of 75 horizons were identified from the 20 selected map units to a depth of 1 m28,29. The central depth of each horizon was sampled using volumetric bulk density cores up to 50 cm. After 50 cm, a hand auger was used to check for any further horizon changes. The bulk density of horizons past 50 cm were estimated using collected soil mass and known auger size. Collected soils were air dried, processed through a 2 mm sieve, and analyzed for total C and nitrogen percent, SOC percent, soil texture, iron (Fe) and aluminum (Al) minerals, pH, cation and anion exchange capacity, extractable cations, wet and dry size classes, aggregate stability, and soil water potential at -15 kPa. Total C and nitrogen were measured by elemental analysis (Costech, ECS 4010, Valencia, CA), with SOC content determined by elemental analysis after hydrochloric acid digestion to remove carbonates. Soil texture was measured using sedimentary separation, while a 10:1 soil slurry in water was used to test soil pH. Soil pressure plates were used to measure soil water potential at -15 kPa.Fe and Al oxides were quantified in mineral phases using selective dissolutions of collected soils, including: (1) a 20:1 sodium citrate to sodium dithionite extraction, shaken 16 h, to quantify total free minerals30, (2) 0.25 M hydroxylamine hydrochloride and hydrochloric acid extraction, shaken 16 h, to quantify amorphous minerals31, and (3) 0.1 M sodium pyrophosphate (pH 10), shaken 16 h and centrifuged at 20,000g, to quantify organo-bound metals30. Extracted Fe, Al, and Si from al extractions were measured by inductively coupled plasma analysis (PerkinElmer, Optima ICP-OES, Norwalk, CT). Exploratory ratios of Fe/Al, Fe/Si, and Al/Si for the citrate/dithionite (c), hydroxylamine (h), and pyrophosphate (p) extractions were calculated. Crystalline Fe, operationally-defined as the difference between the citrate dithionite and hydroxylamine extraction, and Al + ½ Fe32 were calculated for each extraction.Plant-available phosphorus was extracted by the Olsen method using 0.5 M sodium bicarbonate adjusted to pH 8.5 and measured by continuous flow colorimetry (Hach, Lachat Quickchem 8500, Loveland, CO). Exchangeable cations (i.e. calcium, magnesium, potassium, and sodium), effective cation exchange capacity, and anion exchange capacity were measured by compulsive exchange using barium chloride and magnesium sulfate33. Cations were quantified by continuous flow colorimetry and flame-spectroscopy (Hach, Lachat Quickchem 8500, Loveland, CO). Field soils were air dried and initially passed through a 2 mm sieve before size classes of macroaggregate (2 mm – 250 µm) and microaggregate ( More

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