Climate Change Effects On Earthworms - A Review: December 2019
Climate Change Effects On Earthworms - A Review: December 2019
Climate Change Effects On Earthworms - A Review: December 2019
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German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany
Departamento de Solos e Engenharia Agrícola, Universidade Federal do Paraná, Rua dos Funcionários 1540, 80035-050 Curitiba, Brazil
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Brazilian Agricultural Research Corporation (EMBRAPA), Embrapa Forestry, Estrada da Ribeira Km. 111, 83411-000 Colombo, Brazil
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Leipzig University, Institute of Biology, Deutscher Platz 5e, 04103 Leipzig, Germany
E-mail for correspondence: [email protected], [email protected]
Abstract
Climate change can have a plethora of effects on organisms above and below the ground in terrestrial ecosystems. Given the
tremendous biodiversity in the soil and the many ecosystem functions governed by soil organisms, the drivers of soil biodiversity
have received increasing attention. Various climatic factors like temperature, precipitation, soil moisture, as well as extreme climate
events like drought and flood have been shown to alter the composition and functioning of communities in the soil. Earthworms are
important ecosystem engineers in the soils of temperate and tropical climates and play crucial roles for many ecosystem services,
including decomposition, nutrient cycling, and crop yield. Here, we review the published literature on climate change effects on
earthworm communities and activity. In general, we find highly species- and ecological group-specific responses to climate change,
which are likely to result in altered earthworm community composition in future ecosystems. Earthworm activity, abundance, and
biomass tend to increase with increasing temperature at sufficiently high soil water content, while climate extremes like drought
and flooding have deleterious effects. Changing climate conditions may facilitate the invasion of earthworms at higher latitudes and
altitudes, while dryer and warmer conditions may limit earthworm performance in other regions of the world. The present summary
of available information provides a first baseline for predictions of future earthworm distribution. It also reveals the shortage of
studies on interacting effects of multiple global change effects on earthworms, such as potential context-dependent effects of
climate change at different soil pollution levels and across ecosystem types.
Keywords Biodiversity | Climate change | Climate drivers | Cocoons | Earthworm invasions | Soil organisms
amount of rainfall is predicted to remain about the same 2019). Despite many interactions between aboveground
as at present but with increasing variability (Wuebbles and belowground communities (Wardle 2002, Wardle et
& Hayhoe 2004). While changes in precipitation al. 2004), biodiversity patterns in one compartment may
may show substantial small-scale heterogeneity and not necessarily represent those in the other (Cameron et al.
may thus be challenging to predict, there is no doubt 2019), highlighting the need to further explore biodiversity
regarding the expected increase in global mean surface of above- and belowground communities simultaneously
air temperature. Depending on CO2 emission levels, the (Eisenhauer et al. 2019). Many anthropogenic activities
predicted temperature increase ranges between +1.1 and are likely to accelerate the loss of biodiversity and
+6.4°C by the year 2100 (Nakicenovic et al. 2000) or ecosystem services in soil (Veresoglou et al. 2015, Wall
between +1.4°C and +5.8°C over the period 1990 to 2100 et al. 2015), and approximately 60 % of these services
(IPCC 2013). are likely to be degraded, because soil is not used in a
Climate change may affect the functioning of sustainable way (Black et al. 2003, Skubala 2013).
ecosystems by altering the biodiversity and species Earthworms are important soil organisms of
composition of communities (Bates et al. 2008, Bardgett temperate and tropical regions (Lee 1985) and constitute
& van der Putten 2014). The impacts of climate change approximately 40–90 % of soil macro-faunal biomass
on biodiversity are likely to include changes in ecological in many terrestrial ecosystems (Fragoso et al. 1999).
interactions, habitat preference, species abundance and Earthworms are divided into 23 families, and over
distribution, phenology and increases in invasive species 700 genera and > 7,000 species have been described
(Eggleton et al. 2009, Lurgi et al. 2012, Eisenhauer et al. worldwide (Csuzdi 2012, Orgiazzi et al. 2016), but the
2014). Despite some attempts to synthesize information expected number of species is much higher (Orgiazzi
on potential responses of soil organisms to climate et al. 2016, Phillips et al. 2017). They are considered as
change (Blankinship et al. 2011, Coyle et al. 2017), soil keystone species (Power & Mills 1995, Lavelle & Spain
community responses as well as their most important 2001), especially due to their role as ecosystem engineers
drivers are still insufficiently studied, especially for large (Jones et al. 1994). Earthworms have the capacity to
soil invertebrates (Veresoglou et al. 2015, Eisenhauer et create, modify, and maintain habitats for other soil
al. 2017). Climate change effects on soil food webs can organisms as well as plant communities through the
be caused by altering the activity and mortality of soil physical and chemical modification of their environment
organisms. Increasing temperature (enhancing metabolic (Byers et al. 2006, Eisenhauer 2010, Bernard et al. 2012;
demands), frequency of extreme precipitation events and Blouin et al. 2013). Earthworms influence ecosystem
droughts may additionally cause mortality by changing functions through litter fragmentation, burrowing, and
the life cycle and nutrition of soil animals (Bates et al. casting activities, and thereby drive nutrient cycling, soil
2008, Thakur et al. 2018). Increases in the frequency and aggregate stability, water infiltration, plant growth, and
intensity of extreme rainfall together with changes in land soil carbon storage (Coleman et al. 2004). Moreover, they
use make soils more vulnerable to erosion (Nearing et al. are often used as bio-indicators and model organisms
2004) and impair their function as habitat for soil fauna. in eco-toxicological studies due to their role in various
Soil biodiversity is vital to humans as it supports a wide ecosystems and the simple identification in comparison
range of ecosystem processes, functions, and services to other soil taxa (Fründ et al. 2011).
(Blouin et al. 2013, Skubala 2013, Bardgett & van der Earthworm diversity has been studied by many
Putten 2014, Jouquet et al. 2014, Wall et al. 2015) and biologists throughout the world (e.g., Tsai et al. 2000,
includes different types of organisms, ranging from Blakemore 2003, Blakemore 2006, Sautter et al. 2006,
micro-flora and fauna, such as bacteria, algae, fungi, Phillips et al. 2019). A recent global analysis highlights
and protists, to macro- and mega-fauna like earthworms, the importance of climate changes like increasing air
insects, small vertebrates, and plants (Orgiazzi et al. temperature and altered mean annual precipitation on
2016). Biodiversity loss has been reported worldwide earthworm diversity (Phillips et al. 2019). However, these
(IPBES 2018), and this rapid loss has become one of the drivers may not only directly impact earthworms, but
most important global environmental issues (Millenium rather, they frequently alter soil properties like moisture,
Ecosystem Assessment 2005, Maxwell et al. 2016). The temperature, pH, and texture (Burke et al. 1989, Ruiz-
evidence of current extinction caused by climate change Sinoga & Diaz 2010) which then affect earthworm
is very limited, but the rate of species loss is predicted communities (Tiunov et al. 2006, Nieminen et al. 2011).
to increase considerably over the next 50 years (Leadley Moreover, climate-induced changes in vegetation biomass
et al. 2010, Bellard et al. 2012). However, reported and and composition may also affect earthworm populations
predicted biodiversity changes are mostly based on (Eisenhauer et al. 2009). Finally, management at the field
aboveground biodiversity observations (Eisenhauer et al. and landscape scale also influences earthworm diversity
and could alter belowground biological processes (Curry number of studies and high variability in the design, we
& Schmidt 2007, Johnston et al. 2014). For instance, did not perform a meta-analysis but present a review of
reduced earthworm communities in intensively-used the overall trends. Moreover, we provide perspectives for
agricultural fields might be the result of pesticide and future research (Section 3) and conclusions.
fertilizer applications as well as physical disturbances
(Johnston et al. 2014, Pelosi et al. 2014, Singh et al. 2016;
Briones & Schmidt 2017). Such disturbed communities in
degraded soils may be particularly vulnerable to climate 2. Effects of climate change on
change effects (Siebert et al. 2019a). earthworm diversity
Climate change will affect soils and soil processes
mainly through changes of temperature and rainfall 2.1 Temperature
patterns. Increasing temperature, drought, and winter
rainfall will affect soil moisture and temperature regimes, 2.1.1 Effects of increasing temperature and
which have been reported to have variable impacts on context-dependencies
earthworm populations (Carroll et al. 2000, Wever et
al. 2001, Perreault & Whalen 2006, Staley et al. 2008). Temperature is one of the most important climate
However, in order to develop and improve models of the change drivers determining the activity of soil biota
effects of climate change on soil fauna distributions and and decomposition processes. As a consequence,
predict potential impacts on ecosystem processes, more temperature effects have been studied on activities of
ecological research into the climatic tolerances of these soil microorganisms (Insam & Domsch 1988) and soil
important soil invertebrates is required (Sutherland et al. invertebrates (Byzova 2007). Warming has been shown
2006, Moreau-Valancogne et al. 2013, Eisenhauer et al. to cause range shifts in many plant and animal species,
2017). Despite the widely acknowledged important role with range expansion being strongly influenced by biotic
of earthworms for ecosystems and the obvious threats interactions (Chen et al. 2011, Gilman et al. 2010). Several
from climate change phenomena (e.g., Cock et al. 2013, studies have stressed the possibility of warming-induced
Eisenhauer et al. 2014, Hughes et al. 2019, Siebert et al. northward range expansions of some macro-detritivore
2019b), there is still no comprehensive overview of the species, including earthworms (Bohlen et al. 2004, Berg
effects of climate change on earthworm communities. et al. 2010, Eisenhauer et al. 2014).
In this review paper, we present a systematic review Earthworms are poikilothermic, i.e., their body
of the scientific literature and synthesize the potential temperatures are variable and fluctuate with the temperature
climate change effects on earthworm communities of their environment. Hence, the activity, growth, density,
(Section 2), focusing on changes in temperature and metabolism, respiration, and reproduction of earthworms
rainfall, as well as on extreme climate events like are affected by temperature (Edwards & Bohlen 1996).
drought and floods. We focus on responses of earthworm Both high and low temperatures cause a direct response,
communities, abundance, biomass, and activity, while with earthworms tending to congregate in areas where
further physiological responses of earthworms were conditions are optimal for their metabolism. Lower lethal
beyond the scope of this study. We conducted a search temperatures tend to be less known than upper lethal
in Web of Science on July 2, 2019, using published temperatures, which typically range between 25 and 35°C,
literature between 1945 and 2019, applying the following but vary substantially among species, with tropical species
search string: (‘climate change’ OR ‘warming’ OR often being more resistant to higher temperatures than
‘flood’ OR ‘drought’ OR ‘precip*’ OR ‘temperature’) temperate species, and vice-versa for lower temperatures
AND (‘lumbric*’ OR ‘earthworm*’). We restricted the (Lee 1985). Below 10°C, earthworms generally reduce
search to the Web of Science Categories ‘Ecology’ and feeding activities, and above 40°C, cocoon production
‘Articles’, which returned 264 papers. Review, opinion, and development of young earthworms ceases completely
and perspectives papers were excluded from the list, (Edwards & Bohlen 1996, Satchell 1967). The lower
which resulted in 177 papers. As usual, most of the studies temperature limit for earthworm activity may be at
reported were from earthworms living in temperate ~5°C or lower, depending on species and the population/
regions (Cameron et al. 2018, Maestre & Eisenhauer genotype. Many common earthworm species from cooler
2019), with few of them involving species present in the climatic regions are typically active at temperatures above
tropics or other climatic zones (e.g., Mediterranean). 2–4°C (Nordström & Rundgren 1974). Temperature and
We screened for appropriate studies that tested climate moisture interactions are also important: Presley et al.
change effects on earthworm communities and report (1996) observed the maximum growth rate of Eisenia
their findings in Table 1–3. Given the relatively low fetida at high moistures and moderate temperatures, but
after reproductive maturity, the maximal growth and especially if accompanied by changes in rainfall intensity
survivorship occurred in moderate/high moistures and and distribution throughout the year (Hughes et al. 2019).
low temperatures. Eisenhauer et al. (2014) found lower Changing temperature is likely to affect the spatial and
earthworm densities (mainly of Lumbricus rubellus, temporal habitat use by earthworms both at local and
Aporrectodea caliginosa, Dendrodrilus rubidus, and regional scales. At the local scale, temperature changes
Dendrobaena octaedra, with a smaller proportion of may change the vertical and horizontal distribution, while
Aporrectodea rosea, Allolobophora chlorotica, and at the regional scale, it may impact species distribution
Octolasion lacteum) with increasing soil temperature, patterns. If earthworms stay closer to the soil surface
unless rainfall increased as well. Many earthworm species at higher temperature, they may be more susceptible
enter into diapause or become quiescent, frequently to detrimental conditions like heat produced by UV
migrating to deeper soil layers, if higher temperature radiation (Chuang et al. 2006). Moreover, several studies
causes soil water limitation (Jiménez et al. 2000). The reported seasonal variations in the growth and activity of
ability of the anecic or large-bodied species to migrate earthworms with respect to a change in temperature and
vertically in the soil (some to more than 3 m depth; Buck soil moisture (Domínguez & Edwards 1997, Eisenhauer
& Abe 1990) ensures survival during dry and/or warmer et al. 2009).
condition on the soil surface (Gerard 1967, Eisenhauer et As a consequence, climatic conditions are major
al. 2009, Drumond et al. 2013, 2015). determinants of earthworm distribution and diversity
According to the soil moisture-dependent effect of (Fisichelli et al. 2013, Phillips et al. 2019). It is expected
increasing temperature, previous studies on earthworm that future warmer and drier climates will decrease the
performance reported inconsistent and partly contradictory spread of earthworm invasions, because the activity
results (Table 1). It was previously reported that a of earthworm is limited by higher temperatures under
moderate increase in soil temperature could positively drought stress (Curry 2004, Eggleton et al. 2009,
affect earthworm biomass and activity (Boström & Lofs- Zaller et al. 2009), while the opposite might be true if
Holmin 1996). Particularly for Aporrectodea caliginosa, warming coincides with sufficiently high soil moisture
growth rates of juveniles (Eriksen-Hamel and Whalen levels. For instance, the ability of Amynthas species to
2006) and burrowing activity were higher at 20°C than respond quickly to winter warming has been shown to
at 15°C (Perreault & Whalen 2006). The metabolic, have positive consequences for invasiveness and range
burrowing, and casting activity of endogeic earthworms expansion (Görres et al. 2018; Table 1). Eisenhauer et al.
typically increases with increasing soil temperature (2014) also concluded that warming limits the invasion
(Table 1), up to a point, often displaying a slightly bell- of earthworms in northern North America by causing
shaped curve pattern with rapid increases or decreases less favorable soil abiotic conditions, unless warming
at very low and high temperatures, respectively, and is accompanied by increased and temporally even
smaller increases or decreases closer to the metabolic distributions of rainfall sufficient to offset greater water
optima (e.g., Satchell, 1967, Lavelle et al. 1987, Berry losses from higher evapotranspiration.
& Jordan 2001, Wever et al. 2001). Hence, in colder and Earthworms may show very pronounced seasonal
temperate regions, endogeic earthworm activity is likely dynamics in their occurrence and activity patterns,
to increase under elevated soil temperatures in the future, particularly in seasonally dry or cold climates. Earthworm
if soil moisture levels are sufficiently high. A study by abundance tends to decline in the dry or very cold season
Marhan et al. (2015) also indicated a higher loss of N in and reaches highest densities and biomass when climatic
the form of N2O emission from soil with high earthworm and soil conditions are more favorable, e.g., conditions
populations and warmer climate. González-Alcaraz & van typically occurring in spring and autumn in temperate
Gestel (2016) reported higher weight loss of earthworms regions when temperature is modest and soil water
when kept at 25°C than at 20°C, and Lima et al. (2015) content is high (Satchell 1967, Lavelle 1983, Jiménez
also found higher weight loss of Eisenia andrei at 26°C et al. 1998, Walsh & Johnson-Maynard 2016). Notably,
compared to 20°C, stressing the context-dependency the interaction effects of temperature and soil moisture
of temperature effects (with both studies evaluating on earthworms were shown to differ from species to
earthworm behavior in polluted environments). Effects species. Allolobophora chlorotica and Dendrobaena
of increasing temperature can therefore be expected to be octaedra were reported to respond more positively to
positive mostly in colder and moist environments (Berman an increase of temperature at lower soil moisture levels,
& Meshcheryakova 2013; Table 1). On the other hand, while Aporrectodea caliginosa and Lumbricus rubellus
temperature increases in warmer tropical and particularly showed negligible responses (Eggleton et al. 2009).
seasonally dry regions may cause additional water and Zaller et al. (2009) found that moderate experimental
metabolic stresses to earthworms inhabiting these soils, warming significantly reduced the density and biomass
Table 1. Summary table of studies on effects of temperature and/or precipitation/soil moisture as climatic drivers on earthworm species
abundance and biomass, earthworm populations, and earthworm activity. t: effects of temperature; m: effects of moisture; tm: effects of
temperature and moisture.
Earthworm
Climatic drivers Earthworm activity and
Earthworm population
Study Earthworm species* additional comments
Precipitation/ biomass Density/ Cocoons/ and details
Temperature Soil moisture abundance juveniles
Satchell Below 10°C NA Eisenia fetida Reduced feeding activity.
(1967) t t
25-30°C NA Increased feeding
t t activity.
Daugbjerg Below 10°C Wide range of Lumbricus terrestris NA NA Reduced feeding and
(1988) soil moisture
conditions
tm juvenile activity.
Continued table 1.
Earthworm
Climatic drivers Earthworm activity and
Earthworm population
Study Earthworm species *
biomass additional comments
Precipitation/ Density/ Cocoons/ and details
Temperature Soil moisture abundance juveniles
Perreault 5-20°C Soil water Aporrectodea a) Burrow length
& Whalen matric caliginosa, increased with increasing
(2006) potential Lumbricus terrestris temperature and in a
a)-5kPa NA drier soil (-11kPa) than in
(wetter) or
30 %
tm tm wetter soil (-5kPa).
b) Surface casting
b)-11kPa NA
(drier) or 25 % m m activity increased at
higher temperature and
wetter soil.
c) Feeding activity
increased in wetter soil.
d) Activity of juveniles
increased with increasing
temperature and drier to
wetter soil.
Eriksen- 20°C a)-5 kPa Aporrectodea The instantaneous
Hamel &
Whalen
caliginosa tm tm tm growth rate (IGR) was
significantly affected
(2006) by soil moisture,
5-20°C b)-54 kPa temperature, and the
m m m temperature×moisture
interaction.
Optimum growth
conditions for A.
caliginosa were at
20°C and −5 kPa water
potential.
Earthworm
Climatic drivers Earthworm activity and
Earthworm population
Study Earthworm species biomass
*
additional comments
Precipitation/ Density/ Cocoons/ and details
Temperature Soil moisture abundance juveniles
Zaller et al. 5.5°C Reduced Dendrobaena NA Epigeic earthworm
(2009) water
availability
octaedra t t density and biomass was
decreased by 36 % by
warming.
Lima et al. 20°C 40 % WHC Eisenia andrei NA NA Mortality and weight loss
(2011) of soil m in earthworms were not
significantly affected by
moisture.
Uvarov et al. 10-15°C NA Lumbricus rubellus, Smoothed temperature
(2011) Dendrobaena
octaedra
t t t fluctuations than ambient
temperature condition
beneficially affected
earthworm population.
Greiner et al. 18°C NA Dendrobaena veneta, NA NA Adult earthworms
(2011) Eisenia fetida t exhibited near 100 %
survival in the room
1.5°C
t temperature treatment,
but survivorship varied
among species in the low
temperature treatment.
Number of hatchlings
decreased in the low-
temperature treatment
relative to the room-
temperature treatment for
D.veneta and E. fetida
Bessolitsyna Moderate Increased soil Eisenia nordenskioldi NA Over-moistened soils
(2012) temperature moisture nordenskioldi,
Eisenia nordenskioldi
m m were unfavorable for
earthworms.
pallida, Eisenia
atlavinyteae, They could survive long-
Eisenia sibirica, term flooding (provided
Dendrobaena air supply is sufficient)
octaedra but avoided areas with
waterlogged peaty soils.
Berman & -3 to -25°C 50-60 % Eisenia nordenskioldi Water content in tissue
Meshcherya-
kov 2013
moisture nordenskioldi,Eisenia
nordenskioldi pallida
t t t of E. n. nordenskioldi
and cocoons was lower
in winter than in late
summer. Cocoons could
withstand cooling below
–40°С. E.n. pallida was
less cold hardy than E. n.
nordenskioldi
Fisichelli et Moderate Increased Multiple earthworm NA Moderate temperature
al. (2013) temperature precipitation species tm tm and annual precipitation
had a positive impact on
earthworm abundance.
Eisenhauer About 3.57 Decrease soil Lumbricus rubel- NA NA The detrimental warming
et al. (2014) and 4.23°C
increases
moisture less
than 21 %
lus, Aporrectodea
caliginosa,
t effects on earthworm
densities and biomass
Dendrobaena rubi- could be due to warming-
dus, Dendrobaena induced reductions in soil
octaedra, Aporrect water content (SWC);
odea rosea,Allolob warming may limit
ophora chlorotica, earthworm invasion by
Octolasion lacteum decreasing earthworm
performance.
Marhan et al. Increase NA Aporrectodea NA NA Increasing risk for N
(2015) from 15°C to
18.5°C
caliginosa t losses in the form of
nitrate leaching and/
or N2O emissions from
earthworm populated
arable soils with a
warmer climate in the
future.
Continued table 1.
Earthworm
Climatic drivers Earthworm activity and
Earthworm population
Study Earthworm species *
biomass additional comments
Precipitation/ Density/ Cocoons/ and details
Temperature Soil moisture abundance juveniles
Rajkhowa et Varied Soil moisture Drawida nepalensis, NA Density of the
al. (2015) between 17-
26°C
28-39 % Eisenia sp., Amynthas
diffringens, Perionyx
m m earthworm species
varied under different
sp., Lampito mauritii, soil habitat conditions.
Drawida sp.,Perionyx In open grassland, it was
excavatus, Eisenia positively correlated
fetida,Glyphidrilus with soil moisture,
gangeticus, Drawida temperature and
sp, Pontoscolex cor- humidity, while biomass
ethrurus, Eutyphoeus correlated only with
sp.,Gordiodrilus ele- moisture.
gans, Metaphire post-
huma, Dichogaster
saliens,Perionyx an-
nandalei, Amynthas
alexandri
Gonzalez- a) 20°C 50 % and 30 % Eisenia andrei NA NA Earthworms exposed at
Alcaraz &
van Gestel
WHC t 25°C and 30 % WHC
showed significantly
(2016) higher weight loss than
those at 20°C, both at
50 % and 30 % WHC.
Earthworm weight loss
was more pronounced in
b) 25°C 30 % and 50 % the polluted study soils
WHC and greater than 20 %
after 14 days of exposure
of climatic condition.
The threshold of
tolerance of cocoons
was between 27.1°C and
38.1°C for A. tokioensis
b) < 40°C NA NA NA
20-55ºC t and A. agrestis.
*Earthworm species names given are the ones in the publication and do not necessarily reflect current taxonomic opinions as to their
actual species status (particularly problematic for some of the cryptic species).
Climate change factor increases earthworm performance, Non-significant effect of climate change factor on earthworms
Climate change factor decreases earthworm performance
tundra and Taiga and control the northward expansion of Earthworm communities gradually decrease in
Drawida ghilarovi from the south of Khabarovsk Territory abundance as the annual rainfall decreases and the dry
(Berman et al. 2002, 2010). Many of the European season becomes longer, so that in western Africa, for
earthworm species colonizing the Great Lakes region instance, earthworms were observed to disappear when
in the Northern USA (Aporrectodea rosea, Lumbricus the mean annual rainfall was less than 800–1000 mm/
rubellus, Lumbricus terrestris) are not frost-tolerant, year and the dry season exceeded 3–5 months (Lavelle
and hibernate in deeper soil layers (Tiunov et al. 2006). 1983, 1987). Extended dry seasons often lead to a drastic
Moreover, the cold winter climate of the region may decrease in the density of earthworms (Lavelle 1971).
have prevented the expansion of Eisenia fetida and Asian Accordingly, Walsh & Johnson-Maynard (2016) reported
species of the genus Amynthas (Tiunov et al. 2006). Taken that all sampled sites in southeastern Washington (Pacific
together, these findings indicate that a changing climate is Northwest USA) with a mean annual precipitation below
likely to alter the geographic distribution of earthworms 330 mm were free of earthworms. The same trend was
in a species-specific way and may be modulated by local observed in the Iberian Peninsula of Europe, a region
environmental conditions, such as soil type and texture, with dry summers and wet winters that also restricted
pH, vegetation type, and chemical stressors. survival of some earthworm species (Fernandez et al.
2011). Morón-Ríos et al. (2010) conclude that inter-
and intra-annual variability in precipitation is a key
2.2 Precipitation environmental factor for earthworms in Mediterranean
ecosystems, and the capacity to migrate vertically into
According to the Fifth Assessment Report of the the soil may determine the earthworms’ responses to
Intergovernmental Panel on Climate Change (IPCC precipitation.
2013), the chance of heavy rain events and flooding is
increasing globally, as precipitation will be concentrated 2.2.2 Effects of precipitation and soil moisture
into more intense events with longer periods and little
precipitation in between such events. So far, drought has Soil moisture is a key variable controlling the exchange
been given more attention in the ecological literature of water and heat energy between land surface and the
than intense rainfall (Beier et al. 2012), but both can have atmosphere through evaporation and plant transpiration,
major effects on earthworms. and it is thus considered to be critical for the survival,
growth, and reproduction of earthworms (Zorn et
2.2.1 Effects of precipitation and precipitation al. 2008). Accordingly, Diehl & Williams (1992)
seasonality reported that both moisture and food availability had
significant effects on the growth and burrowing rate of
Generally, earthworm communities respond positively earthworms. Low soil moisture caused a reduction in
to precipitation at the local, regional, and global scale aerobic metabolism and growth, and aerobic metabolism
(Table 2; Satchell 1967, Lavelle 1983, Phillips et al. varied in earthworm species exposed to air versus water
2019). Many studies have shown maximum abundance of (Saroja 1964). Bessolitsyna (2012) studied the effect of
earthworms in the rainy/moist season(s) of the year (e.g., soil moisture and different soil types in the landscape of
Bennour & Nair 1997, Jiménez et al. 1998, Eisenhauer et southern middle Siberia and found that the abundance
al. 2009, Rajkhowa et al. 2015). Hence, Tondoh (2006) and distribution of earthworms were mainly affected by
reported that the monthly abundance of earthworms soil moisture. Forest and meadow ecosystems with high
was significantly related to rainfall amount, and Lavelle soil moisture and moderate temperature in the upper soil
(1983) observed a close relationship between rainfall layer and litter were reported to be most favorable for
and earthworm casting (indicating earthworm activity). earthworm communities, but over-moistened soils can
Furthermore, greater accumulation of litter on the soil also be unfavorable for the survival of earthworms, e.g., in
surface of agricultural and mixed forest systems during the case of anaerobic conditions. Although, earthworms
the wet season could provide more space, food, shelter, can live under submerged conditions for a certain period
and protection from predation, and thereby contribute to of time, particularly if the oxygen content of water is high
enhancing earthworm populations and diversity (Ruan enough, most species will die when exposed to excessive
et al. 2005). The increase in earthworm density during water logging conditions.
humid periods follows reproductive peaks, resulting in Similar to the context-dependent effects of temperature,
enhanced growth of individuals. Therefore, in the humid precipitation and soil moisture effects on earthworms are
periods, some earthworm species can accomplish most of variable and depend on temperature (Table 1). Thus, a
their life cycle (Jiménez et al. 1998). significant correlation was observed between earthworm
density and biomass with soil moisture and temperature only when soil moisture becomes adequate for earthworm
(Fournier et al. 2012). Moreover, positive interaction survival (Parmelee & Crossley 1988, Holmstrup 2001),
effects between temperature and soil moisture have been underling the need to explore species- and development
found to result in high earthworm population densities stage-specific responses of earthworms to soil moisture.
at locations with lower precipitation due to higher
reproductive rates (Wever et al. 2001). Soil moisture
content generally decreases with higher temperature due 2.3 Effects of drought
to increased evapo-transpiration, but it was shown to drop
even faster in the presence of earthworms (Lumbricus Drought has both direct and indirect impacts on the
terrestris) after intense rainfall (Ernst et al. 2009, soil environment (Coyle et al. 2017). Water content in
Eisenhauer et al. 2014, Andriuzzi et al. 2015, Gonzalez- upper soil layers is reduced quickly, but deeper soil layers
Alcaraz & van Gestel 2016). This finding indicates that may not be immediately impacted (Nepstad et al. 2002).
the presence of particular earthworm species can also Lower soil water content increases soil hardness (Anh et
modulate the interacting effects of precipitation and al. 2014), and reduces the extent of water films (Coleman
temperature on ecosystem, for instance by changes in et al. 2004), compromising the movements of many soil
soil water content and litter layer (Eisenhauer et al. 2012). fauna. Moreover, drought can result in reduced vegetation
In addition to variations with temperature, the cover (Franklin et al. 2016, Garssen et al. 2014), which
sensitivity and effects of soil moisture depend on other can lead to increased temperatures, altered microclimate
environmental conditions like biogeographical zones and on the soil surface, and reduced resource availability.
the hydrological conditions of the soil (Huhta et al. 1998). Taken together, these direct and indirect drought effects
In arid ecosystems, the survival of earthworms is highly typically reduce the biological activity and earthworm
dependent on soil moisture, while in temperate zones biodiversity in soils.
their survival is unlikely to be at stake, unless the soil Despite the increasing frequency and growing
dries out. Several studies reported seasonal variations importance of droughts in many regions of the world
in the growth and activity of earthworms in response (Dai 2013), only a few studies have explored the effects
to changes in soil moisture (Lavelle 1983, Lavelle et of drought on earthworm communities (Zaller & Arnone
al. 1987, Eriksen-Hamel & Whalen 2006, Perreault & 1999, Holmstrup 2001, Holmstrup & Loeschcke 2003,
Whalen 2006, Eggleton et al. 2009, Fisichelli et al. 2013). Plum & Filser 2005, Petersen et al. 2008, Owojori &
However, earthworm responses vary with life-history Reinecke 2010, Morón-Ríos et al. 2010, Holmstrup et
traits, and some earthworm species (e.g., Pontoscolex al. 2016) (Table 2). Earthworms have only very limited
corethrurus, Amynthas gracilis, Amynthas hupeiensis) morphological or physiological means for reducing water
have a remarkable ability to withstand desiccation transport through the cuticle (Carley 1978), and they are
(Grant 1955, Ayres & Guerra 1981, Caballero 1979). As active only if free water is available in the soil (Lee 1985).
mentioned earlier, many species can also survive under Accordingly, the growth rate of adults and juveniles as
dry soil conditions by entering diapause, para-diapause, well as the production of cocoons were shown to decline
or aestivation (Jiménez et al. 2000). For instance, dramatically in response to drought, and the percentage
Aporrectodea trapezoides is able to survive dry conditions of diapausing in earthworms increased between -20
by aestivating in the soil, and it is able to remain dormant, to 30 kPa of water potential in soil (Holmstrup 2001).
conserving moisture, until soil conditions are favorable Earthworms often lose weight, decrease their burrowing
again (Lee 1985, McDaniel et al. 2013). Baker et al. activity, and may also enter diapause or become quiescent
(1993) reported that lumbricid earthworms in Australia when soils become too dry (Rundgren 1975, Booth et al.
remained active in the top 10 cm of the soils only in the 2000, Owojori & Reinecke 2010).
autumn-spring months when the soil water potential was Moreover, differences in plant community
above 150 kPa. Aporrectodea longa was found to start composition can modulate earthworm community
losing water below a soil water potential of 35.5 kPa and responses to drought (Mariotte et al. 2016). However,
to enter diapause below 20 kPa (Kretzschmar & Bruchou a more nuanced perspective on drought effects on
1991). In a similar study, Holmstrup (2001) also found that earthworm communities may be required, as earthworm
decreasing soil water potentials had a negative effect on species were shown to respond differently to drought
the life cycle of Aporrectodea caliginosa. The change of (Eisenhauer et al. 2014). Epigeic species living at the soil
soil moisture was found to affect earthworm growth and surface are strongly affected by dry and hot conditions
cocoon production, but it did not show any significant during summer, because these species dwell in and
effect on cocoon development (Holmstrup 2001). feed on the litter layer and have limited ability to move
However, other studies have shown that cocoons hatch down into the soil (Eggleton et al. 2009). The drought
Table 2. Summary table of studies on the effects of drought as climatic driver on earthworm species abundance and biomass, earthworm
populations, and earthworm activity. p: effects of precipitation.
Climatic Earthworm
driver Earthworm population Earthworm activity and
Study Earthworm species biomass Density/ Cocoons/ additional comments and details
Drought
abundance juveniles
Lumbricus terrestris,
Allolobophora chlorotica,
Zaller & Nicodrilus longus, Nicodrilus Increased soil moisture, with
Low soil nocturnus, Aporrectodea additional rain, did not affect
Arnone
(1999) moisture rosea, Nicodrilus caligino-
sus, Octolasion cyaneum,
earthworm activity at any earthworm
density level.
Dendrobaena mammalis,
Lumbricus castaneus
Cocoon development was less
sensitive to water potential than
growth and cocoon production
Holmstrup -2 kPa and
(2001) -300 kPa. Aporrectodea caliginosa when drought exposure was for 14
days. Cocoon production decreased
below-10kPa.At -6 kPa, the growth
of juveniles was significantly lower.
Holmstrup 91.6 % Cocoons showed different sensitivity
at different geographic regions.
& Loeschcke relative
(2003) humidity
Dendrobaena octaedra NA NA Epigeic species produced drought-
resistant cocoons.
Drought Drought reduced earthworm
Plum & Marsh soil
Octolasion tyrtaeum,
Octolasion cyaneum, population size.
Filser (2005) Allolobophora chlorotia,
Lumbricus rubellus
Soil-dependent effect in peat soil,
Peat soil highest earthworm density was
found during the drought.
Gradually dehydrated cocoons
Petersen et Gradual showed an increased tolerance
al. (2008) drought Dendrobaena octaedra NA NA to extreme drought compared to
acutely dehydrated cocoons.
Owojori et Toxicity of pollutants was more
al. (2010) Less rain Aporrectodea caliginosa NA NA pronounced in the dry period than
the wet winter period.
Reduction of inter-annual
precipitation variability and
Reduced reduced summer drought in autumn
Morón-Ríos precipitation No species information
et al. (2010) and drought provided
NA NA and spring increased earthworm
abundance. Earthworm density was
higher in irrigated plots, i.e.,the
effects of drought were negative.
Drought
Lima et al. stress Mortality and weight loss in
(2011) 10-40 %
WHC
Eisenia andrei earthworms were not significantly
affected.
Drought in combination with copper
1.5 pF-5 pF caused an increase in mortality. With
Friis et al. increasing drought level, the effect
(2004) (wet tovery
dry)
Aporrectodea caliginosa NA of copper increased from about
40 microg Cu/g dry weight to about
90 microg Cu/g.
Drought significantly increased the
18 % Lumbricus terrestris, biomass of earthworms in plots
Mariotte et reduction Aporrectodea caliginosa
nocturna,Aporrectodea where subordinate plant species
were present. The ratio of the
al. (2016) of mean caliginosa caliginosa, number of juvenile earthworms
summer
precipitation Aporrectodea longa longa,
Aporrectodea rosea
significantly decreased in plots
where subordinate plant species
were removed during drought.
Walsh & No earthworms were detected below
Johnson- Precipitation Aporrectodea trapezoides 330 mm mean annual precipitation.
Maynard
(2016)
increases p p NA Earthworm density showed a
negative correlation with increasing
precipitation.
Climate change factor increases earthworm performance, Non-significant effect of climate change factor on earthworms,
Climate change factor decreases earthworm performance
SOIL ORGANISMS 91 (3) 2019
Climate change effects on earthworms - a review 126
resistant cocoons produced by epigeic species could thus Aporrectodea longa. This increase in the concentration
represent a main strategy (Bouché 1972, Petersen et al. of free amino acids in desiccated earthworm reduced the
2008) of these species to persist during summer drought rate of water loss from the body. Moreover, results of this
perturbations (Holmstrup & Loeschke 2003), and they study suggested that the accumulation of alanine provides
may recover very rapidly in abundance after the end protection against deleterious effects of desiccation in
of drought conditions (Eggleton et al. 2009). Also the earthworms. Taken together, these observations indicate
cocoons of the peregrine species of endogeic category the importance of physiological responses of earthworms
Microscolex dubius were reported to survive hot and to dry conditions, which merits further research and
dry summer periods and hatch when placed in a more synthesis.
favorable environment (Doube & Auhl 1998). In addition to differences in drought effects with
Similar to earthworm abundances, the biomass response respect to earthworm life-history traits, earthworm
of earthworms during and after droughts varies according responses to drought were reported to further depend on
to different ecological strategies. For instance, the other environmental conditions like chemical stressors,
biomass of Lumbricus terrestris, Aporrectodea caliginosa oxygen supply, and food availability in the soil (Diehl
nocturna, and Aporrectodea caliginosa caliginosa & Williams 1992). For instance, Friis et al. (2004)
increased significantly, while that of Aporrectodea observed that drought in combination with heavy metals
rosea was reported to decrease after drought (Mariotte (copper) caused an increase in mortality of Aporrectodea
et al. 2016). Aporrectodea rosea has low assimilation caliginosa. Moreover, Plum & Filser (2005) recorded that
efficiency and forms aestivation chambers close to the soil soil water holding capacity and organic matter content
surface (Edwards & Bohlen 1996, Gerard 1967), while are important factors modulating earthworm responses to
Aporrectodea caliginosa nocturna forms aestivation drought conditions. In fact, high water holding capacity
chambers below 10–20 cm depth (McDaniel et al. 2013), of the soil and artificially raised groundwater table were
which makes them less vulnerable to drought conditions. shown to favor earthworms during drought periods.
Anecic earthworms form permanent vertical burrows These context-dependent effects might explain the high
in the soil, enter into a diapause during dry periods, variability in earthworm responses to drought in previous
and can stay in a dormant stage for several months studies (Table 2), and should be considered in future work
(Jiménez & Decaëns 2004). Endogeic earthworms (such and meta-analyses on this topic.
as Aporrectodea caliginosa), by contrast, form non-
permanent horizontal burrows in the top soil and are
able to survive for short periods of drought by burrowing 2.4 Effects of flooding
to soil depths of 10–20 cm and by forming aestivation
chambers covered with mucus and gut content to protect Floods lead to rapid changes in soil conditions and
themselves against water loss (Bayley et al. 2010). can cause the loss of existing plant biomass (Williamson
These dissimilar ecological strategies are thus likely to & Wardle 2007, Wright et al. 2014, Zhang et al. 2015,
cause changes in earthworm community composition Schomburg et al. 2018), but the deposition of nutrient-rich
in response to pronounced and/or repeated droughts. sediments make floodplains some of the most productive
Moreover, during long-lasing drought, some physiological ecosystems around the globe (Tockner & Stanford
mechanisms were shown to promote dehydration 2002). During the flood, however, mineralization and
tolerance in earthworms. Various earthworm studies decomposition processes of dead organic material
reported that glucose is an important osmolyte governing and ultimately soil nutrient availability are reduced
freeze tolerance (Holmstrup et al. 1999, Holmstrup & due to limited soil gas diffusion and low oxygen
Overgaard 2007), whereas sorbitol is the main osmolyte availability (Schuur & Matson 2001). Consequently,
in dehydrated eggs (Holmstrup 1995, Petersen et al. anaerobic conditions develop fast in flooded soil,
2008). Spectroscopic analysis of compatible osmolytes which have significant effects on the composition of
in gradually dehydrated cocoon/embryos revealed the soil food webs, microbial biomass, and soil microbial
presence of more free amino acids like sorbitol, glucose, community structure (Schuur & Matson 2001, Visser
betaine, alanine, and mannitol than in acute dessicated & Voesenek 2005, Unger et al. 2009, Plum 2005). Once
embryos (Petersen et al. 2008). Bayley et al. (2010) also an environment has been disturbed by a flood, it can
reported an increased concentration of alanine in the take several years for the invertebrate community to
dehydrated adult individuals of Aporrectodea caliginosa. return to its pre-disturbance state (Piearce & Piearce
Recently, Holmstrup et al. (2016) discovered the presence 1979, Gerisch et al. 2012). A meta-analysis of terrestrial
of the free amino acid alanine in three earthworm species invertebrates in flooded grassland concluded that
Aporrectodea tuberculata, Aporrectodea icterica, and flooding reduced the diversity, abundance, and biomass
of all groups of soil macrofauna, including earthworms, earthworms (Bullinger-Weber et al. 2012). Plum &
and the detrimental effects increased with the duration of Filser (2005) also noted that controlled flooding should
flooding and rising temperature (Plum 2005). However, be kept short, especially in winters following natural
the ability of soil invertebrates to survive during flooding summer floods, and a recovery time of about six months
was shown to depend on their behavioral, morphological, was sufficient for the re-establishment of earthworm
and physiological traits (Plum 2005). In the present populations.
review (synthesized in Table 3), several studies showed Various behavioral responses of earthworms can help
that earthworm abundance was reduced in flood plain them to escape from the flooded site, such as horizontal
areas, and periodical flooding also had species-specific migration and climbing onto trees or other vertical
effects on earthworm populations. The reported absence structures like wooden poles of fences (Adis & Righi
of anecic earthworms indicates more erosion and 1989, Pizl 1999, Plum 2005). In a field experiment,
sedimentation processes in flood plains, while the higher the earthworm species Allolobophora chlorotica,
biomass of epigeic earthworm species may be positively Aporrectodea caliginosa, Aporrectodea longa, and
correlated to topsoil texture and organic matter quality Lumbricus castaneus were observed to move upwards in
(Bullinger-Weber et al. 2012). soil samples when the lower parts of the samples were
Many species of earthworms can survive long periods flooded (Ausden et al. 2001, Plum 2005). In addition to
submerged in water (Roots 1956, Edwards & Bohlen behavioral responses, earthworms have developed several
1996), and Zorn et al. (2008) suggested that earthworms physiological adaptations to overcome the lack of oxygen
are able to survive in flooded soil, but there are important during flooding. For example, Eiseniella tetraedra and
differences among species (Ayres & Guerra 1981). Octolasion tyrtaeum retain contact to the aerated zone by
Furthermore, the time period between two flooding events holding the tail vertically upwards and moving it within
determines the earthworm population size and their the water to maintain gas exchange (Pizl 1999, Beylich &
maturity. In fact, it was shown that earthworms mature at Graefe 2002). The prospects of these responses depend
a younger age at sites that are frequently flooded (Klok et on the severity and duration of the flood.
al. 2006a). Earthworm numbers may also be reduced by
floods, because cocoons cannot develop into reproductive
adults and enhanced exposure to soil contaminants after
flooding may further suppress earthworms (Klok et al. 3. Conclusions, implications, and
2006b, Thonon & Klok 2007). outlook
On the other hand, land-use change of floodplains may
also have diverse effects on earthworm communities. The present review highlights the effects of different
For instance, Ausden et al. (2001) found hardly any climatic drivers (temperature, precipitation, drought,
Aporrectodea caliginosa in flooded grassland in Western and flood) on the abundance, survival, and distribution
Europe, while Eiseniella tetraedra (a species adapted to of various earthworm species and ecological groups in
flooded soils) was more abundant in flooded grassland different habitats and land-use types. Overall, we note
in England. However, Ivask et al. (2007) found that that extreme climate events like droughts and floods are
Aporrectodea caliginosa was less abundant in flood plain likely to have the most detrimental effects on earthworm
meadows than in non-flooded meadows, and Keplin & communities. However, most of the results discussed
Broll (2002) found similar results with lower numbers of and synthesized (in Tables 1–3) are based on studies of
this species in flooded grasslands in Germany. In contrast, earthworm communities in temperate climate regions
Pizl (1999) observed an increase in the relative abundance of the world (mainly composed of lumbricid earthworm
of Aporrectodea caliginosa after summer flooding. These species), although we have attempted to incorporate some
inconsistent results suggest that the same species can of the very limited literature from the tropics and other
show dissimilar responses in different environments, and climatic regions (e.g., Mediterranean). Hence, many of
further studies are needed to investigate which conditions the principles presented here, in terms of the potential
may help buffer flooding effects. impacts are in dire need of further verification for these
One important factor that certainly plays a role is the lesser-known earthworm communities. Although we
duration of flooding. Short flooding periods followed suspect many of the climate drivers may have similar
by long recovery periods can benefit certain earthworm impacts in these regions, differences in soil types,
species (Lumbricus rubellus and Allolobophora vegetation, climate, and earthworm communities present
chlorotica), which showed increased abundance and therein (where lumbricids are not the main family) must
biomass in intermittently flooded areas (Schütz et al. be taken into consideration, in order for a more global
2008), and led to compositional shifts favoring epigeic synthesis to be conducted in the future.
Table 3. Summary table of studies on the effects of flooding on earthworm species abundance and biomass, earthworm populations, and
earthworm activity.
Climatic Earthworm
driver Earthworm population Earthworm activity and
Study Earthworm species
biomass Density/ Cocoons/ additional comments and details
Flooding
abundance juveniles
Plum & High flood Octolasion tyrtaeum, Earthworms were less affected
Filser Octolasion cyaneum,
by shorter duration of the flood,
(2005) Allolobophora but prolonged flood reduced
chlorotia, Lumbricus earthworm population size.
rubellus
Klok et al. High flood Lumbricus rubellus At frequent flooding sites,
(2006)
earthworms matured at lower
weight and a younger age.
Ivask et al. High flood Aporrectodea rosea, Cocoons could not hatch, if period
(2007) Lumbricus rubellus,
between two floods was short.
Lumbricus terrestris,
Aporrectodea longa,
Allolobophora
chlorotica,
Lumbricus castaneus
Thonon High flood Lumbricus rubellus Flooding reduced earthworm
& Klok
numbers.
(2007)
Schütz et Short-term Lumbricus rubellus, NA Total earthworm numbers and
al. (2008) flooding Allolobophora biomass in flooded sites exceeded
chlorotica those of non-flooded sites (+51%
and +71%, respectively). Short-
term flooding (max.10days)
interrupted by long recovery
periods favor earthworm
populations.
Zorn et al. Flooding Lumbricus terrestris NA L. terrestris was found more often
(2005) events (3-8 after the flooding period.
weeks) once
per year
Allolobophora A. chlorotica: low populations of
chlorotica juveniles after flooding events, no
effect on biomass or adults.
Lumbricus rubellus L. terrestris was negatively
influenced by flooding.
Continued table 3.
Climatic Earthworm
driver Earthworm population Earthworm activity and
Study Earthworm species
biomass Density/ Cocoons/ additional comments and details
Flooding
abundance juveniles
Lima et al. Flood stress Eisenia anderi Mortality and weight loss of
(2011) 8-120%WHC earthworms were not significantly
affected.
Climate change factor increases earthworm performance, Non-significant effect of climate change factor on earthworms,
Climate change factor decreases earthworm performance
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