Xinwei Wu

Predatory beetles facilitate plant growth by driving earthworms to lower soil layers

Theory suggests that predators of soil-improving, plant-facilitating detritivores (e.g. earthworms) should suppress plant growth via a negative tri-trophic cascade, but the empirical evidence is still largely lacking. We tested this prediction in an alpine meadow on the Tibetan Plateau by manipulating predatory beetles (presence/absence) and quantifying (i) direct effects on the density and behaviour of earthworms; and (ii) indirect effects on soil properties and above-ground plant biomass. In the absence of predators, earthworms improved soil properties, but did not significantly affect plant biomass. Surprisingly, the presence of predators strengthened the positive effect of earthworms on soil properties leading to the emergence of a positive indirect effect of predators on plant biomass. We attribute this counterintuitive result to: (i) the inability of predators to suppress overall earthworm density; and (ii) the predator-induced earthworm habitat shift from the upper to lower soil layer that enhanced their soil-modifying, plant-facilitating, effects. Our results reveal that plant-level consequences of predators as transmitted through detritivores can hinge on behaviour-mediated indirect interactions that have the potential to overturn predictions based solely on trophic interactions. This work calls for a closer examination of the effects of predators in detritus food webs and the development of spatially explicit theory capable of predicting the occurrence and consequences of predator-induced detritivore behavioural shifts.

Domesticated honey bees evolutionarily reduce flower nectar volume in a Tibetan lotus

Plants have evolved costly flowering traits, including the provisioning of rich nectar, to attract and reward their pollinators. Beekeeping (apiculture) locally increases densities of honey bees, which might drive economization of pollinator-attracting traits, but the potential evolutionary consequences of beekeeping on plant–pollinator interactions remain unknown. Here, we present evidence suggesting that intensive apiculture has driven the rapid evolution of plant traits in the alpine lotus (Saussurea nigrescens) on the Tibetan Plateau by allowing reduced nectar volume provisioning without compromising pollination success. This conclusion is supported by measurements of reproductive and vegetative traits, including nectar, at sites of varying distance from apiaries that have housed introduced honey bees (Apis mellifera) since the early 1980s. Nectar volume was more than 60% lower at sites close to apiaries than at more distant sites, while nectar concentration remained consistent. When seedlings from field sites were grown under common garden conditions, trends in nectar volume identical to those in the field were observed, indicating that recently evolved genetic differences likely underlie patterns observed in the field. The adaptive advantage of reduced nectar volume under high pollinator density was clear in both the field and in the common garden. Specifically, plants from sites close to apiaries were taller, had more aboveground biomass, and produced more flowers and seeds compared to those at distant sites, which is consistent with the tradeoffs between nectar volume per flower and flower number per inflorescence within sites. The evolution of reduced nectar volume suggested by our results shows that the widespread practice of beekeeping might be a strong selective agent acting on wild plant populations and illustrates that human activities may indirectly affect evolution by changing critical species interactions.

Cascading effects of predator–detritivore interactions depend on environmental context in a Tibetan alpine meadow

Studies of grazing food webs show that species traits can interact with environmental factors to determine the strength of trophic cascades, but analogous context dependencies in detrital food webs remain poorly understood. In predator-detritivore-plant interaction chains, predators are expected to indirectly suppress plant biomass by reducing the density of plant-facilitating detritivores. However, this outcome can be reversed where above-ground predators drive burrowing detritivores to lower soil levels, strengthening their plant-facilitating effects. Here, we show that these trait-mediated indirect interactions further depend on environmental context in a Tibetan alpine meadow. In our study system, undulating topography generates higher (dry soil) patches interspersed with lower (wet soil) patches. Because the ability of detritivores to form deep burrows is likely to be limited by oxygen availability in low patches (wet soil), we hypothesized that (i) burrowing detritivores would undergo a vertical habitat shift, allowing them to more effectively avoid predation, in high - but not low - patches, and (ii) this shift would transmit positive effects of predators to plants in high patches by improving conditions in the lower soil layer. We tested these hypotheses using complementary field and glasshouse experiments examining whether the cascading effects of above-ground predatory beetles (presence/absence) on the density and behaviour of tunnel-forming detritivorous beetles, soil properties, and plant growth varied with patch type (low/high). Results revealed that predatory beetles did not reduce the density of detritivores in either patch type but had context-dependent trait-mediated effects, increasing the tunnelling depth of detritivores, improving soil conditions and ultimately increasing plant biomass in the high but not low patches. This study adds to an emerging predictive framework linking predators to plants in detritus food webs, demonstrating that these indirect interactions depend not just on the relative habitat domains of predators and prey, but also on environmental conditions that can predictably constrain the behavioural response of detritivores to predation risk.

Soil drainage facilitates earthworm invasion and subsequent carbon loss from peatland soil

1. Human activities have been a significant driver of environmental changes with tremendous consequences for carbon dynamics. Peatlands are critical ecosystems because they store ~30% of the global soil organic carbon pool and are particularly vulnerable to anthropogenic changes. The Zoige peatland on the eastern Tibet Plateau, as the largest alpine peatland in the world, accounts for 1‰ of global peat soil organic carbon storage. However, this peatland has experienced dramatic climate change including increased temperature and reduced precipitation in the past decades, which likely is responsible for a decline of the water table and facilitated earthworm invasion, two major factors reducing soil organic carbon (SOC) storage of peatlands. 2. Because earthworms are often more active in low- than in high- moisture peatlands, we hypothesized that the simultaneous occurrence of water table decline and earthworm invasion would synergistically accelerate the release of SOC from peatland soil. We conducted a field experiment with a paired split-plot design, i.e. presence vs. absence of the invasive earthworms (Pheretima aspergillum) nested in drained vs. undrained plots, respectively, for three years within the homogenous Zoige peatland. 3. Water table decline significantly decreased soil water content and bulk density, resulting in a marked reduction of SOC storage. Moreover, consistent with our hypothesis, earthworm presence dramatically reduced SOC in the drained but not in the undrained peatland through the formation of deep burrows and decreasing bulk density of the lower soil layer over three years. The variation in SOC likely was due to changes in aboveground plant biomass, root growth, and earthworm behavior induced by the experimental treatments. 4. Synthesis and applications. We suggest that incentive measures should be taken to prevent further water table decline and earthworm invasion for maintaining the soil C pool in Zoige peatland. Artificial filling of drainage canals should be implemented to increase the water table level, facilitating the recovery of drained peatlands. Moreover, the dispersal of earthworms and their cocoons attached to the roots of crop plants and tree saplings from low-lying areas to the Zoige region should be controlled and restricted.