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 .