Abstract
Anthropogenic global changes are impacting biodiversity, however, many previous meta-analyses investigating the impact of different global changes on biodiversity have omitted soil fauna, or are limited in the scope of the global changes studied. Threats to soil biodiversity by global changes need to be understood to mitigate effects on ecosystem services provided by soils. We conducted a meta-analysis using 3,173 effect sizes from 627 publications focused on six global changes (climate change, land-use intensification, pollution, nutrient enrichment, invasive species, and habitat fragmentation) and their associated environmental stressors on soil fauna. We classified stressors as either pulse (short-term, acute) or press (long-term, chronic) stressors, and expected pulse stressors to have less impact on soil biodiversity due to buffering effects of the soil. Unexpectedly, pollution caused the largest loss in soil fauna communities, which is worrying due to continually increasing levels of pollution, as well as the poor mechanistic understanding of pollution impacts. There was no clear pattern of pulse stressors having a smaller impact on soil biodiversity than press stressors. Overall, this work shows the importance of including soil biodiversity in large-scale global change analyses, as soil organisms often do not show the same responses as organisms above-ground.
Introduction :
Human impacts are causing unprecedented changes in biodiversity, at local scales and global scales . Climate change, land use intensification, invasive species, and nutrient enrichment are among the human impacts that are often studied, hereafter referred to as Global Changes (GCs) . Understanding the impact of such GCs on biodiversity in a generalisable way is important to be able to predict potential biodiversity changes . Thus, meta-analyses and synthesis studies have become a popular way to investigate GC effects .
Meta-analyses and synthesis studies often find that land-use change and climate change are the biggest threats to biodiversity , and invasive species also are significantly reducing biodiversity . However, other global changes, such as pollution, are often understudied in aboveground terrestrial biomes , despite their potential damaging effects , and their ever-growing rates of use . Moreover, we still lack a general understanding of how the variety of GCs are impacting soil biodiversity. Meta-analyses and synthesis studies have generally overlooked soil organisms, and those focused solely on soil biodiversity tend to address only specific GCs. This could be due to lack a of harmonised terminology resulting in inappropriate search terms , or selection criteria of the analysis (e.g., the focus on species richness; ) that can preclude soil biodiversity studies.
Soil can be regarded as the most biologically diverse habitat providing a variety of ecosystem functions and services . This high diversity is mostly due to the highly complex habitat that spans multiple scales, from between soil pores to across landscapes . Thus, there is a disparity between the scale of GCs and soil biodiversity. Some GCs, such as climate change, are global (although not uniform across the entire world), whereas others act at more regional scales, such as land-use intensification or pollution, although are often widespread .
GCs can impact local biodiversity through a range of different environmental stressors, for example, climate change resulting in decreased precipitation or increased temperature . Despite the term ‘stressor’ implying a negative effect, global change can result in both decreases and increases in biodiversity ). As a result, here, we follow definition, where stressors are causing any detectable biological change, no matter the direction. Although the environmental stressors are a result of a wide variety of different GCs, they may result in similar impacts on biodiversity due to similar mechanisms . Thus, classifying global changes based on the similarities of the characteristics and traits of the environmental stressors may allow better predictions across a wider range of global changes . Moreover, this approach may also provide a framework for exploring potential mechanisms that explain biodiversity responses to certain stressors .
In particular, we consider whether the stress has a ‘pulse’ or a ‘press’ trait . ‘Pulse’ stressors are discrete disturbances that may be extreme in nature and occur less often, such as droughts. Alternatively, pulse stressors may be less severe but occur more regularly; for example, tillage, which can have negative effects on soil fauna . There is some expectation that soil fauna would be less negatively impacted by pulse stressors given that soil can provide a buffer to protect against fluctuations in climate or adverse conditions , as well as a physical buffer for organisms not directly dwelling at the surface . A buffering effect of soil against the pulse stress is especially likely if the stressor does not directly impact the soil environment (e.g., harvesting of aboveground biomass; ).
‘Press’ stressors are more continuous in nature than pulse stressors . Therefore, after a certain timeframe, press stressors result in gradual species loss . For example, pollutants can generally be considered as press stressors in soils. Pollutants, such as heavy metals resulting from industrial or urban activities or persistent pesticides can remain in the soil for centuries because they are not degraded . And although several pesticides are degraded in shorter time-frames, their regular applications over the crop season may represent a press stressor for soil communities. Over longer time frames, it is likely that press stressors would change soil physico-chemical properties, resource availability and habitat structure , as is seen with invasions of new species that directly affect the soil environment or with additions of organic amendments (such as manure, compost and sludge). This eventually can change the soil environment strongly enough to cause compositional changes in soil fauna communities.
This expectation of stress effects on soil biodiversity is not necessarily in line with effects seen in aboveground communities, where organisms may be more directly impacted by pulse stressors due to having a limited number of habitats that can provide a buffer . For example, droughts can have immediate consequences for the physiology of an aboveground organism, resulting in mortality . Alternatively, harvesting aboveground biomass removes or degrades either a part or all the habitats required for aboveground organisms, thereby also reducing populations . Therefore, using the framework of pulse versuspress events, and determining the differences in impact mechanisms in the GCs and environmental stressors, we can start to see the importance of ensuring the explicit inclusion of soil biodiversity into global change research.
The impacts of the environmental stressors are likely to be context dependent , for example, depending on the habitat type . Impacts may also depend on the soil taxa being studied . Due to the huge diversity within the soil, soil organisms are often classified into three body size categories from micro-fauna (< 100μm), to meso-fauna (>100μm to 2mm) up to macro-fauna (> 2mm) . Within these groups, it has been assumed that traits, such as microhabitat requirements, dispersal capabilities, and reproductive rates, are sufficiently similar to influence invertebrates’ responses to external pressures . Larger organisms may be more sensitive to the impacts of stressors than micro- and meso-fauna , because they have longer generation times and require larger microhabitats . As most soil micro-fauna is considered aquatic, their responses may also differ from those seen in meso- and macro-fauna .
We conducted a meta-analysis to compare the effects of six GCs (climate change, land-use intensification, pollution, nutrient enrichment, invasive species and habitat fragmentation) and their associated environmental stressors on micro, meso, and macro soil-fauna. We hypothesize that pulse stressors will have less impact on soil biodiversity than press GCs and stressors. Given that different contexts are likely to affect the impact of GCs and their environmental stressors, we hypothesize that impact of GCs and stressors will vary across the different body size categories, with macro-fauna showing the largest responses.
Methods :
Six global changes (GCs) were considered for the meta-analysis: climate change, land-use intensification, pollution, nutrient enrichment, invasive species, and habitat fragmentation. These were chosen based on the main drivers of biodiversity loss presented in other large-scale works .