5.

Pesticide Toxicity to Earthworms: Exposure, Toxicity and Risk Assessment Meth

odologies
Johnson Stanley1 and Gnanadhas Preetha2
(1)
Indian Council of Agricultural Research, Vivekananda Institute of Hill Agricultu
re, Almora, Uttarakhand, India
(2)
Tamil Nadu Agricultural University, Floriculture Research Station, Kanyakumari,
Tamil Nadu, India
Abstract
Earthworms are exposed to pesticides through contact and ingestion of the contam
inated matter. Pesticides enter into the soil usually as spray drifts or residue
s from plants and from soil applications. Pesticides affect earthworms by killin
g them or my causing temporary or permanent impairments and or by altering their
behaviour and activities. Acute toxicity studies are carried out both by contac
t (topical, vial coating, filter paper, immersion etc.) and by ingestion exposur
es. The most widely conducted, soil contamination bioassay estimates both contac
t and ingestion toxicities of pesticides and thus more realistic to field condit
ions. Sublethal toxicity assays are performed for life history traits along with
reproductive indices. The two important activities of burrowing and litter buri
al of earthworms are analyzed through 2D terraria or 3D soil core x-ray tomograp
hy and by using Daniel s funnel test. Avoidance behaviour, perhaps the most studie
d sublethal parameter is reported to have no relation with soil function of eart
hworms; contrarily the cast production is rarely studied or reported. Semifield
experiments using mesh bags, worm socks, terrestrial model ecosystem etc. along
with some field studies are reported. Ecological risk assessments of pesticide c
ontaminated soils are mostly done using earthworms. Risk assessment based on med
ian lethal doses, ratio of predicted environmental concentration and no effect l
evels, risk estimates like toxicity exposure ratio and hazard quotient, risk ass
essment based on laboratory analyzed acute, chronic and behaviour end points, ex
trapolation and comparison of laboratory and field risks, field tests especially
using a tierd approach and risk assessment for secondary poisoning to predators
are given in detail.
1 Importance of Earthworms in Agriculture
There are about 800 genera and 8000 species of earthworms recorded which belongs
to the order Oligochaeta (Edwards 2004). Most of these species of the so-called
earthworms inhabit soils, submerged muds in freshwater bodies and marine bottom
s (Paoletti 1999). Earthworms are popularly called as ecosystem engineers due to t
heir role in soil structure formation and maintenance especially by creating con
tinuous macropores (Blanchart et al. 2004; Edwards and Shipitalo 1998), stable m
acroaggregates (Six et al. 2004; Blanchart et al. 2004) and organo-mineral compl
exes (Marinissen and Dexter 1990; Six et al. 2004).
If earthworms are not available in the soils, much of the fertility is locked up
in the peaty layer or in the dung and dead plant materials that get accumulated
on the soil surface. In the absence of earthworms, decomposition will be very s
low, soil structure will be poor and compact, there will not be any mixing of so
il and have a significant restriction in moisture penetration and plant root dev
elopment (Stockdill and Cossens 1966). But when earthworms are available, they t
ake bits of fallen leaves and twigs into their burrows where they eventually get
decomposed. About 90?% of normal leaf-fall was found to get buried during winte
r by earthworms in orchards having about 0.75 1 ton of earthworms per acre (Raw 19
62). Darwin (1881), the naturalist famous for his ideas on evolution, estimated
that 10.6 tons of materials per acre are brought to the soil surface by earthwor
ms (Valenzuela 2010). In soils where earthworms are active, all the dung and dea
d plant residues get incorporated under the soil surface. They decompose more ra
pidly to complete the fertility cycle and thus the nutrients will pass rapidly and
frequently in a cycle from soil to plant to animal to soil and so on (Stockdill
and Cossens 1966).

Types of earthworms
Earthworms are of different types and can be classified mainly into three ecolog
ical groups based on their burrowing and feeding habits as epigeic, endogeic and
anecic. The burrowing activity of epigeic species is normally seen in the upper
few centimeters of the soil. They generally dwell in litter and feed on them in
the soil surface and ingest a little or no soil. Endogeic species make largely
horizontal burrows (Hawkins et al. 2008). They consume mineral soil and prefer s
oils rich in organic matter. They are usually found in the upper 10 15 cm but some
times make deeper burrows around the trenches where soil organic matter is plent
y. Anecic species are larger in size, forms vertical burrows, sometimes branched
, that extends to the soil surface and can be as deep as 240 cm (Edwards and Boh
len 1996). These species often emerge at the surface to feed on the decomposing
litter, usually by taking the material into their burrows. They also ingest some
soil along with organic matter (Hawkins et al. 2008). Others such as coprophagi
c species (Eisenia foetida, Dendrobaena veneta , Metaphire schmardae , etc.) liv
e in manure and arboricolous species live in suspended soils especially found in
humid tropical forests (Paoletti 1999).
Though earthworms are of different ecological types, generally plough the field,
enhance the soil fertility and help to increase the soil microbes which make th
e nutrients easily available to the plant and thus called as farmer s friend. Some
of the important activities of earthworms and its uses to mankind are given und
er:
1.1 Improving Soil Physical Properties Including the Structure
Earthworms are increasingly being recognized as ecological engineers and they have
a significant influence on soil physical, chemical and biological properties (V
alenzuela 2010). Earthworms directly improve the structure of the soil and hence
its stability. The soil physical properties such as bulk density, infiltrabilit
y, hydraulic conductivity, porosity, aggregate stability, etc. are proved to be
improved by earthrowms (Ojha and Devkota 2014). With their burrowing, earthworms
help to improve soil aeration and water infiltration apart from improving the s
oil structure. Earthworms are found to involve in moving soil particles, creatin
g pores, stabilizing smaller aggregates and in the lining of biopores (Oades 199
3). They create stable soil aggregates through cast formation e.g. cast produced
by Lumbricus rubellus. The stability of earthworm casts is attributed to the hi
gh organic matter incorporation (Shipitalo and Protz 1989). The plant debris ric
h in carbohydrates are also reportedly responsible for the structural stability
of earthworm casts (Guggenberger et al. 1996). The proper location of the organi
c bonding materials in the soil matrix is more important for stability rather th
an the total amounts (Degens 1997). The natural soil structure is essentially be
en maintained by the diversity of worms, that produce micro and macro aggregates
(Blanchart et al. 1997). The lignin derived phenols were reported to be more in
casts i.e. 31 g/kg of carbon compared to 17 g/kg of carbon in the surrounding t
opsoil (Zhang et al. 2003), which contributes for its stability. Some species of
earthworms such as Pontoscolex corethrurus make the soil more compact and imper
meable to water. The compactness caused by these worms appeared more pronounced
than that of a bulldozer (Chauvel et al. 1999). On the other hand, freshly forme
d casts are more vulnerable for dissolution. Some earthworms are also used in am
eliorating the soil compaction by decreasing the bulk density (Zund et al. 1997;
Langmaack et al. 1999; Jongmans et al. 2003). Thus the compacting and decompact
ing of soil by these worms improves the overall soil structure.
Earthworms till the soil and increase aeration and porosity and thus called as n
atural tillers (Knight et al. 1992), infiltration capacity (Stockdill 1966) and
hydraulic conductivity (Ehlers 1975; Johnson-Maynard et al. 2002). The physical
property of soil such as bulk density (g/cc) was found to be 1.37 in soil with e
arthworm compared to 1.41 in which there were no worms. The field capacity (% mo
isture in 0 4 in. depth) was 39.8 with worms and 34.9 without them; the available
moisture was 1.13 and 1.05, with and without worms, respectively. The porosity (
% in 8 12 in. depth) was 49.0 with worms and 47.4 in soils without them. The basic
infiltration rate per hour was found to get increased by 41.26?% by the introdu
ction of worms (Stockdill and Cossens 1966). Further, water absorption or infilt

ration in fields rich is earthworm can be four to ten times greater as compared
to fields with no earthworms because of their burrowing nature (Edwards and Bohl
en 1996). This may help to reduce water runoff and thus soil erosion (Chan 2004)
. They aerate the soil, make aggregates, incorporate and convert the plant mater
ial into the soil organic matter and thus help to maintain or improve soil struc
ture.