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1
Impact of Human Activity
on Soil ArthropodsAlana Frampton
40100918
Environmental Biology
Dr Tancredi Caruso
Word Count: 3, 728
2
1. Abstract
Soil arthropods carry out a wide range of functions including respiration and decomposition.
Anthropogenic disturbances alter soil biota communities, which results in the community
function changing. There are many factors that affect soil communities which can be
categorised into three main areas; agriculture, pollution and urbanisation. These categories will
be discussed in this review. Through agriculture, lower plant diversity can cause lower microbial
diversity, which lowers the diversity of the whole food web. High input management systems
can cause waterlogging and increased salinity, which reduces diversity. Invasive species can
lower abundance of soil arthropods. Moderate grazing and maintenance can increase
abundance and diversity through creating many microhabitats. Pollution in the form of
pesticides, herbicides, heavy metals and other sources causes a reduction in abundance and can
take many years to recover. However, it is suggested that toxic chemicals naturally become
unavailable to be absorbed by organisms over time, so the effects of these compounds could be
exaggerated. CO2 levels are continually increasing which is having a detrimental effect on soil
communities. During urbanisation many communities have changed due to loss of habitat and
invasive species. Green roofs and open gardens provide new habitats for soil arthropods. Some
urban area communities could benefit from increased temperatures and moderate CO2 levels.
This review clearly demonstrates that soil arthropods respond to all these factors. However,
there is a lack of research to have a mechanistic understanding of these responses. Future
research should focus on soil arthropods to better understand them, so that they could be used
as soil health indicators.
2. Introduction
Nutrient rich and well structured soil leads to the growth of healthy crops (Anwar et al., 2014).
Nitrogen, Phosphorus and Potassium are among those nutrients essential for increased crop yield
(Parmar, 2014). Poor soil fertility and higher numbers of weeds are linked and contributes to
lower production (Birkett et al., 2014). Pea-barley intercrops in Western Europe suppressed the
weeds more effectively when there was higher soil Nitrogen availability: the increased leaf areas
made them more competitive for light than the weeds (Ambus et al., 2011).
3
Soil arthropods assist to form productive nutrient rich soil (Eggleton & Stork, 1992). Bottinelli et
al. (2015) discuss how earthworms, ants and termites are good indicators of soil quality and how
these macro-invertebrates produce and maintain biostructures that contribute to the variety and
health of the soil. Decomposer biota including earthworms are considered to be vital to maintain
the agricultural ecosystems in the tropics through altering the soil (Beare, 1997). These larger soil
fauna stabilize the soil structure, the linings of biopores and smaller aggregates (Oades, 1993).
However, to help to incorporate the nutrients needed into the soil, the smaller soil fauna are also
an essential part of the ecosystem (Caruso, 2015).
These smaller biota break down leaf litter and other debris which transforms the nutrients into a
form that is easily used by plants (Capinera, 2008). The abundance and species richness as part of
a healthy ecosystem can be illustrated in a small way through Oribatid mites. This is explained by
Coleman & Hansen (1998) through an experiment on a forested area in the North Carolina
mountains in the USA. Plots of pure birch, oak and maple litter were named simple litter
treatments. Plots of these three leaf litters and seven other leaf litters mixed were the complex
litter treatments. The complex litter treatments contained significantly more species of Oribatid
mites and a significantly greater variety of microhabitats than the simple litter treatments. This is
shown in Figure 1.
Microhabitat Variety among Litter Treatments at Four Depths along a 5cm Transect
Figure 1 (Coleman & Hansen, 1998)
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The activities of humans are changing the soil ecosystems (Bender et al., 2014). Agriculture,
pollution and urbanisation are three factors that show a clear change in the soil biota
communities. When the soil environment is changed, the soil biota have to adapt to new roles to
survive (Mellino & Ulgiati, 2015) (Coviella et al., 2015). However, for many species the changes
are too rapid to adapt to and the ecosystem is out of balance (Akrami et al., 2015). This review
discusses how these three human activities affect the soil and how this influences the soil
communities.
3. Humans Activities Impacting Soil Arthropods
3.1 Agriculture
Large areas of crops contain lower densities of soil arthropods than in overgrown and natural
areas. Microbial biomass is higher in overgrown areas. Microbes are consumed by nematodes
which are in turn consumed by soil micro-arthropods. Fewer microbes in a food web leads to the
reduction of micro-arthropods and meso-arthropods since they are an essential food source
(Heidemann et al., 2014; Frouz et al., 2015).
To elaborate, microbe biomass can be reduced when agriculture causes lower plant diversity.
Grandy et al. (2014) states that the soil microbe biomass increased significantly when a
monoculture was rotated with another crop or an additional crop was introduced to the
monoculture. This would affect the organisms higher in the food chain such as the Oribatid mites
and Collembola. In addition, the management method can effect soil arthropods as well as the
plant variety.
Low input agriculture management methods conserve soil biodiversity. High input methods (large
amounts of fertilisers and environmental disturbance) reduce diversity. Bardgett & Cook (1998)
observe that high input methods encourage bacterial decomposition. From the previous
discussion it is logical to assume that this would increase the abundance of the nematodes,
therefore, the Oribatid mites and other groups would increase in numbers. However, it was
discovered that is not the case. Increase in bacteria increases the abundance of other
opportunistic bacterial feeding organisms. These compete with other groups and reduce
biodiversity.
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Livestock and defoliation are specific aspects of high input methods that can have a significant
effect on the soil biota. As aerobic organisms, well aerated soil is the most suitable habitat.
Vegetation cover is needed for the food chain to be healthy and productive. When large grazers
trample the ground and reduce vegetation cover, the soil becomes waterlogged. Soil salinity is
increased by defoliation and increased to greater levels by defoliation and compaction. When
waterlogged, micro-arthropods showed a fourfold decrease in abundance and compaction caused
smaller average body size (Bakker et al., 2015). The anaerobic decomposition of large quantities of
fertilisers could reduce the oxygen levels of the soil. This could be another reason why the
Oribatid mites could not compete with the opportunistic fauna discussed previously. Excessive
fertilisation causes waterlogged soil which increases the crop production for the short term but
damages the soil communities and the soil itself. This leads to soil not being able to sustain itself
and continued damage to the soil arthropods (Chen et al., 2009).
However, moderate grazing and trampling by livestock can increase the number of microhabitats
which would increase the abundance and diversity of soil arthropod species. A study by Benoist et
al. (2015) stated that moderate cattle grazing increased the variety of soil and vegetation. The
impact of grazing was sampled at three different levels of cattle pressure; low, medium and high.
Invasive species can be encouraged through agricultural disturbance, this affects the species
richness and abundance of soil arthropods. Forty to fifty percent of available land has been
converted to agricultural and urban areas. This has influenced some species to utilise these
habitats and outcompete other species. The level of vulnerability to invasive species is usually
affected more by the characteristics of the native and invasive species than the species richness
and availability of vacant niches. Disturbance and other factors are affected by humans and
increase the invasion of exotic species. Figure 2 displays how humans interact with the
environment (Chapin FS et al., 2000). When Bromus tectorum was introduced to native perennial
grass (Hilaria jamesii) the abundance of nematodes and microarthropods dropped significantly
(Belnap et al., 2005). Anthropogenic changes through agriculture alter the food chain completely
and invasive species further alter the food chain.
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Humans Interacting with the Ecosystem
Cattle grazing and invasive species can be linked. The disturbance can encourage new species to
invade the habitat and the two factors combined alter the soil community. Borer et al. (2015)
states that the biovolume of arthropods was 79% higher in the grazed plots. However, predatory
arthropods were 13% higher in the ungrazed plots. Where non-native grasses were grazed, the
volume of the arthropods increased as native plants replaced them. This displays how many
factors are linked through agriculture to affect soil arthropods.
Agriculture would benefit from soil arthropods properly carrying out their natural functions.
Neher (1999) states that these organisms are essential in many ecosystem functions such as
decomposition; maintaining stability of soil; increasing plant productivity; enhancing water
relations. If management methods more closely resembled natural ecosystems then the soil
community could become stable and healthier crops would result (Abawi & Widmer, 2000).
Bender & Heijden (2015) studied how soil biota affected nutrient-use efficiency, nutrient leaching
and plant performance. Crop rotation caused a significant increase in the crop yield, Nitrogen and
Phosphorus uptakes and reduced leaching losses of Nitrogen. The crop rotation had increased the
soil life which led to these results.
3.2 Pollution
Figure 2 (Chapin FS et al., 2000)
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Chemicals can influence the species richness and abundance of soil inhabiting mites. An example
is when they are removed by pesticides as non-target organisms (European Commission, 2013;
Bauda et al., 2015). When two biofungicides were applied to plots on fields of cucumber in Egypt,
the community composition of the Oribatid mite community changed. Some species numbers
decreased while another species numbers increased resulting in the same overall total abundance
of mites as before the experiment. Many Oribatid mites are fungal feeders so these species would
decrease as their food source is removed by the biofungicides (Ageba et al., 2014).
In addition, some groups such as the Oribatid mites recover more slowly than Collembola from
pollutants including fertilisers and pesticides. They have lower fecundity rates, slower
development and lower metabolic rates than the Collembola. Due to this life history they cannot
respond rapidly when large numbers are removed from the population. Astigmata have a very
different life history which allows them to respond quickly after exposure to toxic compounds
(Behan-Pelletier, 1999). This demonstrates that the soil community does not return to its original
condition swiftly since some species need more time, therefore, the soil ecosystem needs time to
function properly again. Malkomes & Wohler (1983) explains that inhibitory effects lasted several
months under laboratory conditions.
To add, Stegeman (1964) stated that Collembola took longer than mites to recover from treatment
of the Carbamate Insecticide Cararyl. As in the previously discussed experiment, it took several
months for the soil community to recover based on the Collembola and mite data. Despite a
couple of these experiments being older the biota responds the same way to chemicals now as in
the past.
Pollution can come from unexpected sources, for example, olive mill wastewater. The waste
water is applied to the soil in olive orchards. It was discovered that Oribatida populations were
restricted and this resulted in a community shift. The abundance of Collembola increased (Bruhl
et al., 2015). The diversity of pollutants and species causes each study to produce different
results. However, the overall picture displays that the soil communities are changed.
Other groups are affected by pollution apart from Oribatid mites and Collembola, Enchytraeid
communities were confirmed to be reduced in species richness and abundance through heavy
metal pollution (Zinc and Lead). The data was compared to results from unpolluted areas and the
abundance of Enchyraeid species was generally lower in the polluted areas as shown in Figure 3.
The closer to the smelter, the less healthy the community structure was. Interestingly,
8
Enchytraeids are not affected by the natural soil properties but were affected by soil pH (Kapusta
& Sobczyk, 2015). Other arthropods such as Collembola are more sensitive to pH than the
pollutant. Folsomia candida Collembola were proven to react to the acidity of the soil and not the
Lead. Collembolan mortality, avoidance and lower reproduction were all significantly greater in
acidic soil (Gestel et al., 2014a).
Abundance and Diversity of Enchytraeids Decreases during Heavy Metal Pollution
However, it is suggested that the effect of toxic compounds on soil biota is exaggerated. As
organic compounds age they become less available to be absorbed by organisms. Therefore, their
toxic effects reduce over time (Alexander M, 2000). In previous studies this has not been
discussed. It is possible that the effect of pollution on these organisms is not as severe as at first
appearance.
Other factors combined with pollution can have different effects on soil biota. On a permanent
grassland the effects of fertilizer addition (Nitrogen, phosphorus and Potassium), cutting frequency
and herbicides on soil microorganisms were measured. Microbial biomass decreased when cut
once a year but not three times a year when fertilizer was applied during both experiments. This
suggests that cutting reduces the negative effect of applying fertilisers. Earthworms and beetles
increased in abundance when fertiliser was applied but grass cutting was detrimental. This shows
that polluting substances can be detrimental but the effects are complicated when comparing
short and long term effects and other management processes (Lemanski & Scheu, 2015).
Pollutants can be absorbed from the atmosphere, they are not always toxic chemicals or
fertilisers. CO2 levels will become more available to soil biota over time since CO2 levels are
Figure 3 (Chapin FS et al., 2000)
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continually increasing. In a mesocosm study involving Collembola, Oribatid mites (Acari) and
Enchytraeidae, the organisms were collected after five and eleven weeks as the CO2 levels
increased. The CO2 increase did not affect the plants but the predatory mite and two Collembola
species reduced in abundance (Audisio et al., 2015).
Cold CO2 producing gas vents provide the ideal environment to research how soil biota will
respond to the continuing increase in CO2. The top few centimetres of the soil contained
microhabitats of 100% CO2 and <2% CO2. Collembola and nematodes declined in abundance as
CO2 levels increased. However, nematode densities were not affected until 62% CO2 levels.
Collembola developed viable populations up until 20% CO2. The mofettophilous species had
denser populations in the higher CO2 areas due to either a lack of competition or a more suitable
food supply. This suggests that as atmospheric CO2 levels increase, the soil microarthropod
abundance and species diversity will decrease and be replaced by others (Balkenhol et al., 2015).
3.3 Urbanisation
Urbanisation creates the ideal physical environment to fulfil the needs of humans only. The
species that are able to adapt well to urban environments are multiplying since they are able to
outcompete other species (McKinney, 2006). It was expected that the soil community
composition would change following the same logic as previously discussed. However, a study in
Italy disagrees. Urban and suburban holm oak in a small city and a large city were sampled. There
was no significant difference between anthropogenic factors resulting from urbanisation, and
arthropod density and variety. This data is displayed in Table 1 (Agamennone et al., 2014).
Over time biodiversity could show different results. A study specifically examining Collembola
community composition displayed differences over time. Native species diversity reduced, the lost
species being replaced by more generalised and invasive species. This resulted in a species poor
community. The more resistant Collembola species persist and less stressed urban grass areas
contain more diversity. The changes over time suggest that the response is influenced by multiple
processes. This information is displayed in Figure 4 (Rzeszowski & Sterzyriska, 2015).
Collembola Species Accumulation for Whole Warsaw Area using Old (Longer Time after
Urbanisation) and New (Shorter Time after Urbanisation) Data
10
Interestingly, in urban areas new environments are being created that soil communities are taking
possession of. In Germany green roofs were sampled during 2002, ‘old roofs’ were built between
1990 and 1994, ‘young roofs’ were built between 1998 and 1999. In ‘old roofs’ there was
improved niche specialisation of the collembolan and a more stable community. ‘Young roofs’ had
less advanced soil formation and the soil arthropod community was not as stable (Boning &
Schrader, 2006). This shows that while habitats are being removed by urbanisation, new ones are
being created within urban areas as the environment adapts. However, the number of species
was very similar in the ‘old’ and ‘new roofs which suggests that the communities will not develop
more than they already have. Even if green roofing was extensive it would still not replace the
natural environments.
In Naples, Italy it was discovered that agriculture has more of an effect on soil properties than
urbanisation. It is possible that it is more important to create new habitats in agricultural areas
than urban areas. The agricultural soil was dominated by very few species, mainly Proisotoma
minuta and Entomobrya multifasciata. These two species are adapted to environments of high
disturbance. The urban soil community more closely resembled the forest community (Cortet et
al., 2015). These results could vary from country to country but this evidence suggests that the
level of disturbance in an urbanised area will affect how much the soil community changes. It is
Figure 4 (Rzeszowski & Sterzyriska, 2015)
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possible that the level of pollution in urban areas is what reduces the species diversity and
abundance in urban areas. Another study in Naples, Italy stated that collembolan density
decreased as pollution increased. The higher the organic content of the soil the greater the
species richness and diversity (Arena et al., 2014). This provides more evidence that the
urbanisation itself does not cause changes in soil biota but the human activities in those areas do
change the community.
How human activities within urbanisation change soil communities is emphasised through
different types of soil communities being found in different types of garden. Research was
conducted on lawns, open beds and closed canopy beds in Dunedin, New Zealand. Collembola
were most frequently found in lawns. Detritivores were found in higher numbers in gardens that
had experienced no pesticides (Barratt et al., 2015). Considering studies discussed previously, it
suggests that lawn soils were less disturbed than beds that would be turned over regularly for
maintenance of the plants.
To add, some soil biota could benefit from urbanisation due to plants benefiting. One paper
highlights that within urbanised areas increased temperatures and high CO2 levels increase the
productivity of plants (Vodyanitskii, 2015). It has been previously discussed that increased soil CO2
levels are detrimental to the soil community. However, if the CO2 was not too high and used
primarily by the plants without large amounts being absorbed by the soil, the soil community
could resemble forest arthropod communities.
3.4 Additional Discussion
It is difficult to predict how these organisms respond to human activity. One paper states that due
to Oribatid mites having generalised diets, they are less affected by environmental changes than
other groups. These mites do not suffer from a lack of leaf litter because it only contributes to
22% of their diet (Gan et al., 2014). However, there are many more factors affecting this group
and it does not explore any of the other arthropods.
An example of one of these factors could be the introduction of invasive species. Acacia dealbata
(Australian tree legume) produces allelopathic compounds that reduce microbial biomass and
reduce the diversity of the native plants around it. The arthropods reacted differently depending
on the ecosystem (Lorenzo et al., 2013). This further displays that many factors affect them
12
depending on how anthropogenic activity alters the environment, plant species and other biota
surrounding them.
Gestel et al. (2014b) emphasises the importance of the time of year of sampling. In the autumn
higher temperatures and lower precipitation were recorded than in the spring. In both seasons
the most abundant taxa were Collembola and Acarina but the relative abundances were affected
differently by seasonality and the metal contamination in the area. Therefore, for accurate future
sampling, time needs to be taken into consideration.
Urbanisation and pollution are closely linked while affecting soil arthropods over time. One study
states that there was no significant difference between the toxicity of soil in different forested
areas except in different seasons. Different forested areas were sampled along an urbanisation
gradient and are displayed in Figure 3. Significantly higher levels of pollutants were recorded in
the autumn than in the spring (Baranyai et al., 2016). This provides more evidence suggesting that
sampling over time is a good idea for future studies.
Areas of Forest Sampled Along an Urbanisation Gradient in Debrecen in Hungary
Figure 5 (Baranyai et al., 2016)
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Mechanistic processes could be studied by observing how soil arthropods are affected over time.
Therefore, dynamical studies would give more insight into the processes within soil arthropod
communities. In Egypt two fields were sampled from October to March 2015. The effects of
changing from conventional to organic management were studied. Over time, the organic matter
built up which increased Oribatid mite abundance (Al-Assiuty et al., 2015). If these fields had not
been sampled over a period of time, the relationship between organic matter and mites would not
have been observed.
4. Conclusion
Most studies have been conducted at the community level. Due to all the complexities discussed
above, it is difficult to obtain a mechanistic understanding of processes at that level. Integrating
studies of species, populations and communities would provide useful information on how
different factors affect soil arthropods.
A useful method to distinguish between species, population and community level effects would be
to examine studies on ecotoxicology that focus on soil invertebrate species. Gestel et al. (2012)
examined the quality of urban soil through bioassays with Eisenia Andrei, Folsomia candida and
Enchytraeus crypticus. Metal bioaccumulation was the highest in E. crypticus and was more
sensitive than the other two species. Evidence suggested that the reasons for this species being
more sensitive was related to soil properties and the metal contamination. Therefore, this
information can be used to assess how this species interacts with the ecosystem and provides a
mechanistic understanding.
If the factors affecting soil biota could be more clearly understood then it would be a useful way to
measure the health of soil. In 1998 a conference was held entitled ‘Soil Health: Managing the
Biological Component of Soil Quality’ to emphasise how important soil organisms are as measures
of soil quality and health. This could assist in the understanding of how to manage soil properly so
it can function properly and humans can utilise it in a sustainable way (Doran & Zeiss, 2000).
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