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.