Plant Hormones and Worm casts or vermicomposts

Summary from Blakemore (2002) COSMOPOLITAN EARTHWORMS CD (Ref.)

Plant growth promoting substances (e.g. vitamins, plant hormones, enzymes and amino
acids) have been detected in earthworm extracts (e.g. Gavrilov, 1962; Nielson, 1965;
Graff & Makeschin, 1980; Dell'Agnola & Nardi, 1987 as summarized in Blakemore,
1994). Earthworms have been found to stimulate soil enzymes, such as glucosidase and
phosphatase (possibly of microbial origin) which influence availability of plant nutrients
(e.g. Ross & Cairns, 1982; Tiwari et al., 1989). Nielson (1965) identified indole
compounds in extracts of several lumbricids while Springett & Syers (1979) suggested
that auxin-like substances are present in casts. Microbially derived plant hormones have
also been isolated from earthworm casts (Tomati et al., 1988). Production of specific
plant hormones by earthworms adds weight to the arguments for their co-evolution.
Plant growth is regulated by hormones which act at low concentrations to modify
the metabolic or developmental processes of the plant.
There are five main classes of plant hormone:
Auxins - there is only one naturally occurring auxin: indole-3-acetic acid (IAA) which is
chemically related to the amino acid tryptophan. Auxin alone promotes cell enlargement.
Synthetic auxins are aromatic compounds that affect plant growth in the same way as
auxin. The biggest use of these auxin-like compounds is as herbicides, eg. 2,4-D and
MCPA. Other examples of synthetic auxins are naphthalene acetic acid (used to control
fruit set and sucker growth on trees after pruning); and Indole butyric acid (used as
rooting compound).
Cytokinins several naturally occurring forms, all related to the nucleotide adenine.
Only in combination with auxins do cytokinins promote cell division, growth and tissue
differentiation. Synthetic cytokinins include benzyladenine and kinetin which are used in
tissue culture media and for growth control in fruit.
Ethylene is a hydrocarbon gas derived from the amino acid methionine. This gas is
used commercially for ripening fruit, especially bananas. Synthetics include ethephon
that can be applied as a spray for various applications. Ethylene is known to control
differentiation of root hair cells, and is also implicated in plant defense mechanisms,
possibly acting as a trigger that leads to disease suppressive soils (Penmetsa and Cook,
1997).
Abscisic acid ABA is one of two compounds (the other is xanthoxin) related to
carotenoids. Canot be synthesized.
Gibberellins GAs are the largest group with over 70 compounds, an example is
Gibberellic acid (GA3). They are used commercially to break dormancy and to promote
set of grapes. Gibberellins promote growth, so anti-gibberellins are used as retardants;
dwarf varieties of plants lack gibberellins.

Krishnamoorthy & Vajranabhaiah (1986, as reported in Ishmail, 1995) found that plant
hormone-like compounds were present in the casts of two earthworm species (Table 1),
and that the concentrations of these diminished as the casts aged (Table 2).
Table 1. Rate of plant growth promoter in casts of two tropical earthworm species
_______________________________________________________________________
_
Species
Rate of production (nanograms day-1 worm-1)
Cytokinins
Auxins
_______________________________________________________________________
_
Wormless control soil
nil
nil
Lampito mauritii
4.3
54
Perionyx excavatus
78.1
316
_______________________________________________________________________
_
Note: number of observations were 5 for L. mauritii and 6 for P. excavatus; cytokinins
were benzyladenine equivalents; auxins were indole acedic acid equivalents.
Table 2. Loss of plant growth promoter activities in paper pulp wormcasts of L.
mauritii on aging under constant moisture & darkness at room temperature (26 C)
_______________________________________________________________________
_
Weeks after casting
Loss of activity compared to original level (%)
Cytokinins
Auxins
_______________________________________________________________________
_
0
0
0
1
2
1.5
2
4
4
3
9
7
4
15
18
5
26
21
6
35
34
7
47
41
10
69
58
_______________________________________________________________________
_
Worm casts.

Considerable rates of deposition have been reported and several workers

have also found casts to be enriched in plant available macronutrients and micronutrients,
proteins and enzymes when compared to the soil matrix. Common estimates of annual
productions of surface casts in temperate regions of 4-250 t ha-1 are lower than some reports

from the tropics, of ranges of about 60-600 t ha-1 (Darwin, 1881; Edwards & Lofty, 1977;
Lavelle, 1978; Lee, 1985; Lal, 1987). Highest estimates in the tropics, by Lavelle (1988)
and Lavelle et al. (1989) are of over 1,000 t ha-1 yr-1. Surface casting varies with species,
season and soil type, but the common ranges above represent deposition of continuous
layers of soil from about 0.2 to 2.0 mm thick annually (Darwin, 1881; Lavelle, 1988).
Barleys (1956c) estimate of 2.5 t ha-1 casting in pastures in South Australia is exceptionally
low and may be seasonal. (Note: higher figures for cast production in the tropics of 2,100
and 2,600 t ha-1 yr-1, reported in Edwards & Lofty (1977: 144), are overcalculations from the
original sources by a factor of ten!). It is pertinent that most earthworms work below
ground where their casting may be many times greater (Lavelle, 1988). For example,
Shipitalo et al. (1988) give maximum sub-surface adjusted casting rates in the order of 280950 t ha-1 yr-1.
Lunt & Jacobson (1944) established that worm casts are enriched in N, P, K, Ca and
Mg. Many subsequent studies have shown that secretion of CaCO3 or NH3 in the gut affects
the pH of casts, which tend to neutrality, and that the amounts of exchangeable cations
released in casts are often more than double the rates in the substrate (Lee, 1985). Most
studies have involved lumbricids, relatively little is known about the cast compositions in
other groups (cf. Barois, 1992).
Despite having higher nutrients, direct contribution of casts to improved plant
growth may be moderate, for example, Mansell et al. (1981) detected only slight increases
in yields with cast material when added at "normal" rates of application (equivalent to
average casting rates from the field). Nevertheless, casts are used in India, the Philippines,
Australia, China, USA, Cuba and Mexico at least (ref1, ref2, ref3). Reddy (1988) tested
the effects of vermicasts or vermicompost (the product, along with worm biomass, of
vermicomposting operations) on growth of rice in pots: Rates were 310 g, 620 g, and 940 g
of casts per 2 kg soil (to give the equivalents to 20, 40 and 60 kg K 2O ha-1 ) compared to soil
only. Significant increases in plant growth were recorded after four months. Reddy
surmised that the effects of the casts on the growth of rice may be due to the presence of
plant growth substances identified by others as indole compounds also yield-influencing
substances which could be secreted into the casts, and, in turn increase the plant growth. In
addition, chemical analysis of casts showed that they were richer in various plant nutrients

compared to the underlying soil. Also in India, Kale et al. (1992), found that when
vermicompost was applied to a rice paddy as an organic fertiliser amendment, there were
significant increases in the colonisation of soil by nitrogen-fixing bacteria and mycorrhizal
fungi. Higher levels of total nitrogen in the plot with added vermicompost was attributed to
higher populations of nitrogen-fixing bacteria. A report by Logsdon (1994) makes passing
reference to a study in Pune, India (by H. Jambhekar from Matarasha Agricultural Bioteka)
that grapes fertilized with 2 tons of vermicompost per acre (ca. 5 t/ha) per year for five years
increased yields to 15 tons per acre, higher than yields under conventional fertilization and
there were additional improvements in soils.
Australian trials, reported by Buckerfield & Webster (1998a, 1999), using mulches
of vermicompost derived from grape marc or pomace led to 300% increase in grape yields
within six months.
Native and exotic species casts were characterized by Blakemore (1994: tab. 4.3.21):
Table 4.3.21. Description of surface casts and soil matrices of dismantled cores.
Spp
Drawida barwelli

Appearance of casts; soils

in the field, matrix ramified with re-filled
burrows suggesting sub-surface casting
Dichogaster affinis
fine granular casts (0.5-1.0 mm); friable
Dichogaster saliens
often inhabiting small chimneys
Spenceriella (= Anisochaeta) minor
casts not obvious
Pontoscolex corethrurus
medium sized globular or ribbon casts
especially when soil wet; soils permeated
with burrows
Polypheretima elongata
large globular (30 mm) and long threads;
surface pitted and many large ramifying
burrows (2-9mm)
Po. taprobanae
occasional surface casts
Eudrilus eugeniae
copious regular pellets 2-3x1 mm
especially around sides; burrows also
along edges; roots grow up into casts
Apporectodea trapezoides
extensive globular surface casts
Metaphire californica
patchy subrounded up-wellings
Fletcherodrilus unicus
distinctive elongate pellets 2-6x2 mm
Eukkeria saltensis
fine granules
Digaster brunneus
none; large diameter burrows
Species casting profusely on the surface were Eu. eugeniae in all three soils, and
Dichogaster spp., Pont. corethrurus, Polypheretima elongata, A. trapezoides and M.
californica in either or both Narayen and Samford soils (Table 4.3.20). Species that
appeared to cast mainly below ground were Polypheretima elongata, S. minor, P.

taprobanae and Dg. brunneus (despite mortality of this latter species, several helical
burrows were found in the cores on dismantling). Additional observations were that casts in
the denser clay soils were more aggregated and water-stable than those in sand. Chemical
analyses of samples of air-dried surface casts and topsoils for the Narayen clay and Samford
sandy soils were presented in Blakemore (1994: tabs. 4.3.22 and 4.3.23).
Burrows and roots.

Earthworm species vary in, and have been ecologically

categorised according to, their burrowing and feeding strategies (Lee, 1959, 1985, 1987).
Burrow diameters may range from less than 1 mm to greater than 10 mm, and extend as
deep as 15 m (Blakemore, 2000e). Therefore, they have profound implications not only for
aeration and water conductivity but also for channelling of plant roots. Earthworms are able
to exert considerable pressure when probing compacted soils (McKenzie & Dexter, 1988a,
1988b). Several researchers have noted root proliferation in burrows which they usually
attribute to the combined effects of following paths of least resistance and of better access to
nutrient and moisture gradients in the drilosphere (e.g. Edwards and Lofty, 1978, 1980; van
Rhee, 1965, 1977; Ehlers et al., 1983; Springett, 1985; Wang et al., 1986; Parker, 1989;
Dexter, 1991). Several aspects and examples of the effects of burrows on root growth are
summarised in Logsdon & Linden (1992) who, nevertheless, argue that improved root
growth does not always translate into increased crop yield.
Although earthworms obtain much of their nutrition via dead root material and root
exudates (Lee & Pankhurst, 1992), rhizophagy is uncommon (Lavelle, 1983, 1988) but is
reported for some species (Baylis et al., 1986; Cortez & Bouch, 1992).
Root mats and organic matter. Through feeding, mixing and stimulation of microflora,
earthworms regulate the rates of mineralisation and immobilisation of soil organic matter
(SOM). This aptitude varies according to climatic conditions and the precise nature of the
organic reserves (Martin et al. 1992). In temperate regions, absence of an earthworm fauna
is often accompanied by undesirable accumulation of surface litter and root mats. Barley &
Kleinig (1964) and later Noble et al. (1970) reported that the successful introduction of
lumbricids to pasture soil in NSW greatly reduced root mats and stimulated cycling of N
locked in this organic layer. From the opposite position, Parmelee et al. (1990) and
Clements et al. (1991) showed that when earthworms were excluded, an obvious build-up of
the organic matter occurred in the litter layer. Conversely, earthworms in the humid tropics

were found to have contrasting effects on SOM dynamics: accelerating mineralisation (of
labile SOM) in the short-term due to digestion, but arresting the decomposition (of
recalcitrant SOM) in the long-term by protecting nutrients within water-stable casts (Lavelle
et al., 1989; Martin, 1991; Martin et al., 1992; Lavelle & Martin, 1992). Thus earthworms
activities, although varying with species and region, regulate the rate of mineralization of
nutrients from SOM reserves in different but balanced ways in both temperate and tropical
environments.
Mesofauna and microorganisms.

The

trophic,

symbiotic,

competitive,

and

synergistic relationships with beneficial or pathogenic nematodes, microarthropods,

microorganisms and fungi are complex (Lee & Ladd, 1984; Lee & Pankhurst, 1992). Both
external and internal relationships exist.

Experimental evidence shows that certain

organisms, particularly microflora, are killed during gut transit, whereas others proliferate.
Microfauna populations are also affected, for example Yeates (1981, quoted in Lee, 1985)
reported nematode populations reduced by 37-66% when earthworms were introduced to
soils. Senapati (1992) found that mainly plant parasitic nematodes were reduced whereas
microbivore nematodes increased.

As for Collembola, Marinissen & Bok (1988)

ascertained that presence of earthworms favoured survival of both larger species and
individuals.
Possibly the greatest influences are on protists, other microorganisms and
actinomycetes, some of which increase logarithmically after passing through an
earthworm's gut (Lee & Ladd, 1984; Edwards & Fletcher, 1988). Some microorganisms
are reduced, suggesting they are a major part of the earthworm diet, especially
(bacterivorous) protozoa and fungi, algae less so, with bacteria the least important (Lee &
Ladd, 1985; Edwards & Fletcher, 1988).
Miles (1963) found that Eisenia fetida cultured in sterile soil to which soil fungi
and bacteria were added, failed to grow, but when soil protozoa were added, the worms
grew to maturity, suggesting that at least in this species protozoa are an important part of
the diet.
Mechanisms of mutualistic digestion in earthworms, involving gut symbioses,
have been proposed for several members of tropical and temperate species (e.g. Barois &

Lavelle, 1986; Martin et al., 1987; Martin, 1988; Lavelle, 1988; Barois et al., 1987;
Barois, 1992; Trigo & Lavelle, 1993; Mendez et al., 2004). Moreover, the potential for
free N-fixing in the gut has been demonstrated in some earthworms (Barois et al., 1987,
reported in Lavelle et al., 1987). Barois (1992) discusses the mutualistic microbiology of
Amynthas corticis and A. gracilis. The intestinal caeca of such pheretimoid species
probably serve to culture symbiotic gut flora and microbes (perhaps analogous to
complex typhlosoles in other groups), and although I can find few references to the
specific microbes involved, there are papers of culturing diazotrophic bacteria from the
intestines of pheretimoids (e.g. Risal & Ozawa, 2002; Ozawa & Risal, 2003). Recently
Hyun-Jung Kim et al. (2004) and Kwang-Hee Shin et al. (2004) isolated nearly 200
colonies of aerobic and anaerobic bacteria from the gut of E. fetida (Agric. Chem.
Biotechnol. 47: 137-142; 147-152 http://env1.gist.ac.kr/~aeml/research_3_2004.htm);
and Horn et al. (2005) described new N2O-producing bacteria from A. caliginosa gut.
Enhanced dispersal and viability of spores and propagules of fungi and
microorganisms in the presence of earthworms have been reported for both pathogenic
(Edwards & Fletcher, 1988) and beneficial organisms (Buckalew et al., 1982).
Beneficial, vesicular-arbuscular mycorrhizas (VAM) were transmitted in casts of 13
species of earthworms, as was Frankia (a nodulating, symbiotic N-fixing actinomycete)
in one species (Reddell & Spain, 1991a, 1991b). Kale et al. (1992) reported increased
colonization of plants by mycorrhizae, and higher soil counts of total microbes, especially
N-fixers and spore formers, following application of vermicompost.

Recently, the

potential dual benefit of reduced severity of Rhizoctonia and "take-all" pathology in

wheat combined with increased root colonization with symbiotic Rhizobium and
Pseudomonas through earthworm activities were found (Dr P.M Stephens pers. comm.).
Experimental effects of vermicompost on some plant pathogens by Szczech et al. (1993)
found that Phytophthora and Fusarium fungi were suppressed by vermicompost, but that
parasitic nematodes were not affected. Inoculation of sorghum seeds with Azospirillum
brasiliense and earthworm casts increased growth of sorghum (Savalgi & Savalgi, 1991).
Fungal pathogens Rosellinia necatrix, white root rot of apples, and Plasmodiophora
brassicae, clubroot of brassicas, have both been reduced by vermicompost (Stephens et
al., 1999). It is further reported that soil borne diseases are less prevalent on organic

farms that rely on the kinds of natural microbial activities invoked above (Workneh et al.,
1993 referred to in Hoitink & Grebus, 1994). A two-year project in Florida has further
found that vermicomposting using earthworms to process sewage sludge (biosolids) was
effective in reducing pathogen levels (viz. fecal coliform, Salmonella sp., enteric virus,
and helminth ova) to meet EPA Class A requirements (Eastman, 1999).
Plant growth factors. Release of metabolites that stimulate plant growth has been proposed
by several authors to explain some of the effects of earthworms on plant growth. Plant
growth promoting substances (e.g. vitamins, plant hormones, enzymes and amino acids)
have been detected in earthworm extracts (e.g. Gavrilov, 1962; Nielson, 1965; Graff &
Makeschin, 1980; Dell'Agnola & Nardi, 1987). A report of an Indian study in Ishmail
(1995) was of plant hormone-like compounds (Cytokinins were benzyladenine equivalents;
Auxins were indole acedic acid equivalents) in casts of L. maruitii and P. excavatus that
diminished in concentration as casts aged over 10 weeks.
Earthworms have been found to stimulate soil enzymes, such as glucosidase and
phosphatase (possibly of microbial origin) which influence availability of plant nutrients
(e.g. Ross & Cairns, 1982; Tiwari et al., 1989).

Nielson (1965) identified indole

compounds in extracts of several lumbricids, while Springett & Syers (1979) suggested that
auxin-like substances are present in casts. Microbially derived plant hormones have also
been isolated from earthworm casts (Tomati et al., 1988). Production of specific plant
hormones by earthworms gives credance to arguments for plant/worm co-evolution.
References other references may be sourced from these citations.
Blakemore (1994). PhD thesis Online.
Blakemore (2008). Cosmpolitan Earthworms CD. (Ref.).
Ismail, Sultan, A. (1995) Earthworms in soil fertility management. In Thampan, P.K. (ed). Organic
Agriculture. Peekay Tree Crops Development Foundation, Chochin. Pp 77-100.
Krishnamoorthy, R.V., and Vajranabhaiah, S.N. (1986). Biological activity of earthworm casts. An
assessment of plant growth promoter levels in the casts. Proc. Indian Acad. Sci. (Anim. Sci.). 95:
341-351.
Penmetsa, R.V., and Cook, D.R. (1997). A legume ethylene-insensitive mutant hyperinfected by its
rhizobial symbionts. Science, Jan 24, 1997.

Tomati, U., Grappelli, A. & Galli, E. (1988). The hormone-like effect of earthworm casts on plant growth.
Biology and Fertility of Soils. 5: 288-294.
Springett, J.A. & Seyers, J.K. (1979). The effect of earthworm casts on ryegrass seedlings. In: T.K.
Crosby & R.P. Pottinger (eds.). "Proceedings of the 2nd Australasian Conference on Grassland
Invertebrate Ecology." Government Printer, Wellington, N.Z. Pp. 44-47.