Rainforest transformation reallocates energy from green to brown food webs.

Terrestrial animal biodiversity is increasingly being lost because of land-use change1,2. However, functional and energetic consequences aboveground and belowground and across trophic levels in megadiverse tropical ecosystems remain largely unknown. To fill this gap, we assessed changes in energy fluxes across 'green' aboveground (canopy arthropods and birds) and 'brown' belowground (soil arthropods and earthworms) animal food webs in tropical rainforests and plantations in Sumatra, Indonesia. Our results showed that most of the energy in rainforests is channelled to the belowground animal food web. Oil palm and rubber plantations had similar or, in the case of rubber agroforest, higher total animal energy fluxes compared to rainforest but the key energetic nodes were distinctly different: in rainforest more than 90% of the total animal energy flux was channelled by arthropods in soil and canopy, whereas in plantations more than 50% of the energy was allocated to annelids (earthworms). Land-use change led to a consistent decline in multitrophic energy flux aboveground, whereas belowground food webs responded with reduced energy flux to higher trophic levels, down to -90%, and with shifts from slow (fungal) to fast (bacterial) energy channels and from faeces production towards consumption of soil organic matter. This coincides with previously reported soil carbon stock depletion3. Here we show that well-documented animal biodiversity declines with tropical land-use change4-6 are associated with vast energetic and functional restructuring in food webs across aboveground and belowground ecosystem compartments.

Plant roots fuel tropical soil animal communities.

Belowground life relies on plant litter, while its linkage to living roots had long been understudied, and remains unknown in the tropics. Here, we analysed the response of 30 soil animal groups to root trenching and litter removal in rainforest and plantations in Sumatra, and found that roots are similarly important to soil fauna as litter. Trenching effects were stronger in soil than in litter, with an overall decrease in animal abundance in rainforest by 42% and in plantations by 30%. Litter removal little affected animals in soil, but decreased the total abundance by 60% in rainforest and rubber plantations but not in oil palm plantations. Litter and root effects on animal group abundances were explained by body size or vertical distribution. Our study quantifies principle carbon pathways in soil food webs under tropical land use, providing the basis for mechanistic modelling and ecosystem-friendly management of tropical soils.

Linking size spectrum, energy flux and trophic multifunctionality in soil food webs of tropical land-use systems.

Many ecosystem functions depend on the structure of food webs, which heavily relies on the body size spectrum of the community. Despite that, little is known on how the size spectrum of soil animals responds to agricultural practices in tropical land-use systems and how these responses affect ecosystem functioning. We studied land-use-induced changes in below-ground communities in tropical lowland ecosystems in Sumatra (Jambi province, Indonesia), a hot spot of tropical rainforest conversion into rubber and oil palm plantations. The study included ca. 30,000 measured individuals from 33 high-order taxa of meso- and macrofauna spanning eight orders of magnitude in body mass. Using individual body masses, we calculated the metabolism of trophic guilds and used food web models to calculate energy fluxes and infer ecosystem functions, such as decomposition, herbivory, primary and intraguild predation. Land-use change was associated with reduced abundance and taxonomic diversity of soil invertebrates, but strong increase in total biomass and moderate changes in total energy flux. These changes were due to increased biomass of large-sized decomposers in soil, in particular earthworms, with their share in community metabolism increasing from 11% in rainforest to 59%-76% in jungle rubber, and rubber and oil palm plantations. Decomposition, that is the energy flux to decomposers, stayed unchanged, but herbivory, primary and intraguild predation decreased by an order of magnitude in plantation systems. Intraguild predation was very important, being responsible for 38% of the energy flux in rainforest according to our model. Conversion of rainforest into monoculture plantations is associated by an uneven loss of size classes and trophic levels of soil invertebrates resulting in sequestration of energy in large-sized primary consumers and restricted flux of energy to higher trophic levels. Pronounced differences between rainforest and jungle rubber reflect sensitivity of rainforest soil animal communities to moderate land-use changes. Soil communities in plantation systems sustained high total energy flux despite reduced biodiversity. The high energy flux into large decomposers but low energy fluxes into other trophic guilds suggests that trophic multifunctionality of below-ground communities is compromised in plantation systems.

Micro-decomposer communities and decomposition processes in tropical lowlands as affected by land use and litter type.

We investigated how the land-use change from rainforest into jungle rubber, intensive rubber and oil palm plantations affects decomposers and litter decomposition in Sumatra, Indonesia. Litterbags containing three litter types were placed into four land-use systems and harvested after 6 and 12 months. Litter mass loss and litter element concentrations were measured, and different microbial groups including bacteria, fungi and testate amoebae were studied. After 12 months 81, 65, 63 and 53% of litter exposed in rainforest, jungle rubber in oil palm and rubber plantations was decomposed. In addition to land use, litter decomposition varied strongly with litter type and short-term effects differed markedly from long-term effects. After 6 months, oil palm and rubber litter decomposed faster than rainforest litter, but after 12 months, decomposition of rainforest litter exceeded that of oil palm and rubber litter, reflecting adaptation of bacteria and fungi to decompose structural compounds in rainforest litter but not (or less) in rubber and oil palm litter. Bacterial and fungal community composition and testate amoeba species number and density varied strongly with litter type, but little with land use. However, community composition of testate amoebae was mainly affected by land use. Generally, changes in bacteria, fungi and testate amoebae were linked to changes in litter element concentrations, suggesting that element ratios of litter material as basal resource for the decomposer food web shape the structure of decomposer communities and decomposition processes via bottom-up forces. Overall, changing rainforest to monoculture plantations shifts the decomposer community structure and negatively affects litter decomposition.

Seasonal fluctuations of litter and soil Collembola and their drivers in rainforest and plantation systems.

Rainforest conversion and expansion of plantations in tropical regions change local microclimate and are associated with biodiversity decline. Tropical soils are a hotspot of animal biodiversity and may sensitively respond to microclimate changes, but these responses remain unexplored. To address this knowledge gap, here we investigated seasonal fluctuations in density and community composition of Collembola, a dominant group of soil invertebrates, in rainforest, and in rubber and oil palm plantations in Jambi province (Sumatra, Indonesia). Across land-use systems, the density of Collembola in the litter was at a maximum at the beginning of the wet season, whereas in soil it generally varied little. The community composition of Collembola changed with season and the differences between land-use systems were most pronounced at the beginning of the dry season. Water content, pH, fungal and bacterial biomarkers, C/N ratio and root biomass were identified as factors related to seasonal variations in species composition of Collembola across different land-use systems. We conclude that (1) conversion of rainforest into plantation systems aggravates detrimental effects of low moisture during the dry season on soil invertebrate communities; (2) Collembola communities are driven by common environmental factors across land-use systems, with water content, pH and food availability being most important; (3) Collembola in litter are more sensitive to climatic variations than those in soil. Overall, the results document the sensitivity of tropical soil invertebrate communities to seasonal climatic variations, which intensifies the effects of the conversion of rainforest into plantation systems on soil biodiversity.

Tropical land use alters functional diversity of soil food webs and leads to monopolization of the detrital energy channel.

Agricultural expansion is among the main threats to biodiversity and functions of tropical ecosystems. It has been shown that conversion of rainforest into plantations erodes biodiversity, but further consequences for food-web structure and energetics of belowground communities remains little explored. We used a unique combination of stable isotope analysis and food-web energetics to analyze in a comprehensive way consequences of the conversion of rainforest into oil palm and rubber plantations on the structure of and channeling of energy through soil animal food webs in Sumatra, Indonesia. Across the animal groups studied, most of the taxa had lower litter-calibrated Δ13C values in plantations than in rainforests, suggesting that they switched to freshly-fixed plant carbon ('fast' energy channeling) in plantations from the detrital C pathway ('slow' energy channeling) in rainforests. These shifts led to changes in isotopic divergence, dispersion, evenness, and uniqueness. However, earthworms as major detritivores stayed unchanged in their trophic niche and monopolized the detrital pathway in plantations, resulting in similar energetic metrics across land-use systems. Functional diversity metrics of soil food webs were associated with reduced amount of litter, tree density, and species richness in plantations, providing guidelines on how to improve the complexity of the structure of and channeling of energy through soil food webs. Our results highlight the strong restructuring of soil food webs with the conversion of rainforest into plantations threatening soil functioning and ecosystem stability in the long term.

Land-use change shifts and magnifies seasonal variations of the decomposer system in lowland tropical landscapes.

Deforestation and agricultural expansion in the tropics affect local and regional climatic conditions, leading to synergistic negative impacts on land ecosystems. Climatic changes manifest in increased inter- and intraseasonal variations and frequency of extreme climatic events (i.e., droughts and floods), which have evident consequences for aboveground biodiversity. However, until today, there have been no studies on how land use affects seasonal variations below ground in tropical ecosystems, which may be more buffered against climatic variation. Here, we analyzed seasonal variations in soil parameters, basal respiration, microbial communities, and abundances of soil invertebrates along with microclimatic conditions in rainforest and monocultures of oil palm and rubber in Sumatra, Indonesia. About 75% (20 out of 26) of the measured litter and soil, microbial, and animal parameters varied with season, with seasonal changes in 50% of the parameters depending on land use. Land use affected seasonal variations in microbial indicators associated with carbon availability and cycling rate. The magnitude of seasonal variations in microbial parameters in the soil of monocultures was almost 40% higher than in the soil of rainforest. Measured parameters were associated with short-term climatic conditions (3-day period air humidity) in plantations, but not in rainforest, confirming a reduced soil buffering ability in plantations. Overall, our findings suggest that land use temporally shifts and increases the magnitude of seasonal variations of the belowground ecosystem compartment, with microbial communities responding most strongly. The increased seasonal variations in soil biota in plantations likely translate into more pronounced fluctuations in essential ecosystem functions such as nutrient cycling and carbon sequestration, and these ramifications ultimately may compromise the stability of tropical ecosystems in the long term. As the observed seasonal dynamics is likely to increase with both local and global climate change, these shifts need closer attention for the long-term sustainable management of plantation systems in the tropics.

Trophic niche differentiation and utilisation of food resources in Collembola is altered by rainforest conversion to plantation systems.

Intensively managed monoculture plantations are increasingly replacing natural forests across the tropics resulting in changes in ecological niches of species and communities, and in ecosystem functioning. Collembola are among the most abundant arthropods inhabiting the belowground system sensitively responding to changes in vegetation and soil conditions. However, most studies on the response of Collembola to land-use change were conducted in temperate ecosystems and focused on shifts in community composition or morphological traits, while parameters more closely linked to ecosystem functioning, such as trophic niches, received little attention. Here, we used stable isotope analysis (13C and 15N) to investigate changes in the trophic structure and use of food resources by Collembola in Jambi province (Sumatra, Indonesia), a region that experienced strong deforestation in the last decades. Isotopic values of Collembola from 32 sites representing four land-use systems were analyzed (rainforest, rubber agroforest, rubber (Hevea brasiliansis) and oil palm (Elaeis guineensis) monoculture plantations). Across Collembola species Δ13C values were highest in rainforest suggesting more pronounced processing of litter resources by microorganisms and consumption of these microorganisms by Collembola in this system. Lower Δ13C values, but high Δ13C variation in Collembola in oil palm plantations indicated that Collembola shifted towards herbivory and used more variable resources in this system. Small range in Δ15N values in Collembola species in monoculture plantations in comparison to rainforest indicated that conversion of rainforest into plantations is associated with simplification in the trophic structure of Collembola communities. This was further confirmed by generally lower isotopic niche differentiation among species in plantations. Across the studied ecosystems, atmobiotic species (Symphypleona and Paronellidae) occupied the lowest, whereas euedaphic Collembola species occupied the highest trophic position, resembling patterns in temperate forests. Some species of Paronellidae in rainforest and jungle rubber had Δ15N values below those of leaf litter suggesting algivory (Salina sp.1, Callyntrura sp.1 and Lepidonella sp.1), while a dominant species, Pseudosinella sp.1, had the highest Δ15N values in most of the land-use systems suggesting that this species at least in part lives as predator or scavenger. Overall, the results suggest that rainforest conversion into plantation systems is associated with marked shifts in the structure of trophic niches in soil and litter Collembola with potential consequences for ecosystem functioning and food-web stability.

Conversion of rainforest into oil palm and rubber plantations affects the functional composition of litter and soil Collembola.

Rainforest conversion and expansion of plantations in tropical regions are associated with changes in animal communities and biodiversity decline. In soil, Collembola are one of the most numerous invertebrate groups that affect the functioning of microbial communities and support arthropod predators. Despite that, information on the impact of changes in land use in the tropics on species and trait composition of Collembola communities is very limited. We investigated the response of Collembola to the conversion of rainforest into rubber agroforestry ("jungle rubber"), rubber, and oil palm plantations in Jambi Province (Sumatra, Indonesia), a region which experienced one of the strongest recent deforestation globally. Collembola were sampled in 2013 and 2016 from the litter and soil layer using heat extraction, and environmental factors were measured (litter C/N ratio, pH, water content, composition of microbial community and predator abundance). In the litter layer, density and species richness in plantation systems were 25%-38% and 30%-40% lower, respectively, than in rainforest. However, in the soil layer, density, species richness, and trait diversity of Collembola were only slightly affected by land-use change, contrasting the response of many other animal groups. Species and trait composition of Collembola communities in litter and soil differed between each of the land-use systems. Water content and pH were identified as main factors related to the differences in species and trait composition in both litter and soil, followed by the density of micro- and macropredators. Dominant species of Collembola in rainforest and jungle rubber were characterized by small body size, absence of furca, and absence of intense pigmentation, while in plantations, larger species with long furca and diffuse or patterned pigmentation were more abundant. Overall, land-use change negatively affected Collembola communities in the litter layer, but its impact was lower in the soil layer. Several pantropical genera of Collembola (i.e., Isotomiella, Pseudosinella, and Folsomides) dominated across land-use systems, reflecting their high environmental adaptability and/or efficient dispersal, calling for studies on their ecology and genetic diversity. The decline in species richness and density of litter-dwelling Collembola with the conversion of rainforest into plantation systems calls for management practices mitigating negative effects of the deterioration of the litter layer in rubber plantations, but even more in oil palm plantations.

Review of the mite genus Krantzolaspina Datta & Bhattacharjee (Mesostigmata, Parholaspididae) with re-description of K. angustatus comb. nov. (Ishikawa) from Indonesia.

Herein, we update the diagnosis and description of the genus Krantzolaspina Datta & Bhattacharjee and provide a list of the three valid species including new combinations and synonyms, as follows: 1) Krantzolaspina angustatus (Ishikawa, 1987) comb. nov. (= Indutolaelaps jiroftensisHajizadeh et al., 2017syn. nov.), 2) K. rebatii Datta & Bhattacharjee, 1989 and 3) K. solimani (Metwali, 1983) comb. nov. Finally, we re-describe K. angustatus (Ishikawa, 1987) comb. nov. based on the holotype from Japan, voucher specimens from Iran and additional females that we found in soil samples from oil palm plantations in Sumatra, Indonesia.

Functional losses in ground spider communities due to habitat structure degradation under tropical land-use change.

Deforestation and land-use change in tropical regions result in habitat loss and extinction of species that are unable to adapt to the conditions in agricultural landscapes. If the associated loss of functional diversity is not compensated by species colonizing the converted habitats, extinctions might be followed by a reduction or loss of ecosystem functions including biological control. To date, little is known about how land-use change in the tropics alters the functional diversity of invertebrate predators and which key environmental factors may mitigate the decline in functional diversity and predation in litter and soil communities. We applied litter sieving and heat extraction to study ground spider communities and assessed structural characteristics of vegetation and parameters of litter in rainforest and agricultural land-use systems (jungle rubber, rubber, and oil palm monocultures) in a Southeast Asian hotspot of rainforest conversion: Sumatra, Indonesia. We found that (1) spider density, species richness, functional diversity, and community predation (energy flux to spiders) were reduced by 57-98% from rainforest to oil palm monoculture; (2) jungle rubber and rubber monoculture sustained relatively high diversity and predation in ground spiders, but small cryptic spider species strongly declined; (3) high species turnover compensated losses of some functional trait combinations, but did not compensate for the overall loss of functional diversity and predation per unit area; (4) spider diversity was related to habitat structure such as amount of litter, understory density, and understory height, while spider predation was better explained by plant diversity. Management practices that increase habitat-structural complexity and plant diversity such as mulching, reduced weeding, and intercropping monocultures with other plants may contribute to maintaining functional diversity of and predation services provided by ground invertebrate communities in plantations.

Description of four new species of armoured spiders (Araneae, Tetrablemmidae) from Sumatra, Indonesia.

Four new species of armoured spiders from Sumatra, Indonesia are described. Three species are described in the genus Ablemma Roewer, 1963 and one species in the genus Brignoliella Shear, 1978; Ablemmaandriana sp. n. (male), Ablemmacontrita sp. n. (male and female), Ablemmakelinci sp. n. (male) and Brignoliellapatmae sp. n. (male and female). The female of Ablemmasingalang Lehtinen, 1981 is described here for the first time. The first record of Brignoliella for Sumatra is also presented.

Conversion of rainforest to oil palm and rubber plantations alters energy channels in soil food webs.

In the last decades, lowland tropical rainforest has been converted in large into plantation systems. Despite the evident changes above ground, the effect of rainforest conversion on the channeling of energy in soil food webs was not studied. Here, we investigated community-level neutral lipid fatty acid profiles in dominant soil fauna to track energy channels in rainforest, rubber, and oil palm plantations in Sumatra, Indonesia. Abundant macrofauna including Araneae, Chilopoda, and Diplopoda contained high amounts of plant and fungal biomarker fatty acids (FAs). Lumbricina had the lowest amount of plant, but the highest amount of animal-synthesized C20 polyunsaturated FAs as compared to other soil taxa. Mesofauna detritivores (Collembola and Oribatida) contained high amounts of algal biomarker FAs. The differences in FA profiles between taxa were evident if data were analyzed across land-use systems, suggesting that soil fauna of different size (macro- and mesofauna) are associated with different energy channels. Despite that, rainforest conversion changed the biomarker FA composition of soil fauna at the community level. Conversion of rainforest into oil palm plantations enhanced the plant energy channel in soil food webs and reduced the bacterial energy channel; conversion into rubber plantations reduced the AMF-based energy channel. The changes in energy distribution within soil food webs may have significant implications for the functioning of tropical ecosystems and their response to environmental changes. At present, these responses are hard to predict considering the poor knowledge on structure and functioning of tropical soil food webs.

Review of the mite genus Ololaelaps (Acari, Laelapidae) and redescription of O.formidabilis Berlese.

A species of laelapid mite, Ololaelapsformidabilis, is redescribed based on male and female adults from soil in Sumatra, Indonesia. This species is distinguished from other Ololaelaps species by its metapodal platelet narrowly fused with the parapodal plate and by its hologastric shield having two inverted-V-like ridges. The genus is redescribed based on a review of the literature and examination of specimens of some species. Valid species of Ololaelaps are listed and accompanied by notes on morphological characters to assist future revision of the genus.

Shift in trophic niches of soil microarthropods with conversion of tropical rainforest into plantations as indicated by stable isotopes (15N, 13C).

Land-use change is threatening biodiversity worldwide, affecting above and below ground animal communities by altering their trophic niches. However, shifts in trophic niches with changes in land use are little studied and this applies in particular to belowground animals. Oribatid mites are among the most abundant soil animals, involved in decomposition processes and nutrient cycling. We analyzed shifts in trophic niches of six soil-living oribatid mite species with the conversion of lowland secondary rainforest into plantation systems of different land-use intensity (jungle rubber, rubber and oil palm monoculture plantation) in two regions of southwest Sumatra, Indonesia. We measured stable isotope ratios (13C/12C and 15N/14N) of single oribatid mite individuals and calculated shifts in stable isotope niches with changes in land use. Significant changes in stable isotope ratios in three of the six studied oribatid mite species indicated that these species shift their trophic niches with changes in land use. The trophic shift was either due to changes in trophic level (δ15N values), to changes in the use of basal resources (δ13C values) or to changes in both. The trophic shift generally was most pronounced between more natural systems (rainforest and jungle rubber) on one side and monoculture plantations systems (rubber and oil palm plantations) on the other, reflecting that the shifts were related to land-use intensity. Although trophic niches of the other three studied species did not differ significantly between land-use systems they followed a similar trend. Overall, the results suggest that colonization of very different ecosystems such as rainforest and intensively managed monoculture plantations by oribatid mite species likely is related to their ability to shift their trophic niches, i.e. to trophic plasticity.

Description of three new species of Aposphragisma Thoma, 2014 (Araneae: Oonopidae) from Sumatra, Indonesia.

Three species from the family Oonopidae are newly described from leaf litter habitats in Sumatra, Indonesia based on male and female morphology. All three species belong to the genus Aposphragisma Thoma, 2014: Aposphragismaglobosum sp. n., Aposphragismajambi sp. n., and Aposphragismasumatra sp. n.

Trophic niches, diversity and community composition of invertebrate top predators (Chilopoda) as affected by conversion of tropical lowland rainforest in Sumatra (Indonesia).

Conversion of tropical rainforests into plantations fundamentally alters ecological niches of animal species. Generalist predators such as centipedes (Chilopoda) may be able to persist in converted ecosystems due to their ability to adapt and switch to alternative prey populations. We investigated variations in community composition and trophic niches of soil and litter living centipedes in a range of ecosystems including rainforests, jungle rubber agroforests, and rubber and oil palm monocultures in two landscapes in Sumatra, Indonesia. Including information on environmental factors in the soil and litter habitat, we explored drivers shaping ecological niches of soil living invertebrate predators in one of the world's hotspots of rainforest conversion. Conversion of rainforests into agroforests and plantations was associated with a marked change in the composition of centipede communities. However, irrespective of major differences in habitat characteristics, changes in total abundances were small and the overall diversity and biomass of centipedes was similar in each of the systems investigated, suggesting that the number of ecological niches for this group of predators remains unchanged. By using stable isotope analysis (15N and 13C), we investigated trophic niche shifts of the centipede community; lower δ13C values of centipedes in oil palm plantations as compared to other ecosystems suggests that centipedes switch from decomposer prey to other prey, presumably understory associated herbivores, due to reduced availability of litter associated prey species. The results suggest that the ability to utilize alternative prey is a key feature enabling invertebrate predators to persist in ecosystems undergoing major structural changes due to anthropogenic land use change.

The first geophilid centipedes from Malesia: a new genus with two new species from Sumatra (Chilopoda, Geophilidae).

A new genus Sundageophilus is here described for two new species of geophilid centipedes (Chilopoda: Geophilidae) from Sumatra, Indonesia. Both Sundageophilus bidentatus sp. n. and Sundageophilus poriger sp. n. feature a minute body size (less than 1 cm long with 31-35 pairs of legs), a similar structure of the maxillae, elongated forcipules, and few coxal organs. Sundageophilus bidentatus is unique among geophilids because the ultimate article of the forcipule is armed with two conspicuous denticles, one dorsal to the other, instead of a single one or none. The two species of Sundageophilus are the first genuine Geophilidae ever found in Malesia, and among the very few representatives of this family in the entire south-eastern Asia.

Changes in Structure and Functioning of Protist (Testate Amoebae) Communities Due to Conversion of Lowland Rainforest into Rubber and Oil Palm Plantations.

Large areas of tropical rainforest are being converted to agricultural and plantation land uses, but little is known of biodiversity and ecological functioning under these replacement land uses. We investigated the effects of conversion of rainforest into jungle rubber, intensive rubber and oil palm plantations on testate amoebae, diverse and functionally important protists in litter and soil. Living testate amoebae species richness, density and biomass were all lower in replacement land uses than in rainforest, with the impact being more pronounced in litter than in soil. Similar abundances of species of high and low trophic level in rainforest suggest that trophic interactions are more balanced, with a high number of functionally redundant species, than in rubber and oil palm. In contrast, plantations had a low density of high trophic level species indicating losses of functions. This was particularly so in oil palm plantations. In addition, the relative density of species with siliceous shells was >50% lower in the litter layer of oil palm and rubber compared to rainforest and jungle rubber. This difference suggests that rainforest conversion changes biogenic silicon pools and increases silicon losses. Overall, the lower species richness, density and biomass in plantations than in rainforest, and the changes in the functional composition of the testate amoebae community, indicate detrimental effects of rainforest conversion on the structure and functioning of microbial food webs.