Herbicide hormesis – can it be useful in crop production?

DOI: 10.1111/j.1365-3180.2011.00862.x

Herbicide hormesis – can it be useful in cropproduction?

R G BELZ*, N CEDERGREEN� & S O DUKE�*Institute of Plant Production and Agroecology in the Tropics and Subtropics, Department of Agroecology, University of Hohenheim, Stuttgart,

Germany, � Department of Basic Science and Environment, Faculty of Life Science, University of Copenhagen, Frederiksberg C, Denmark, and

�USDA, ARS, Natural Products Utilization Research Unit, University, MS, USA

Received 23 November 2010

Revised version accepted 8 March 2011

Subject Editor: Per Kudsk, Flakkebjerg, Denmark

Summary

The yield-enhancing effects of some pesticides may

change the focus of their use in crop production, from

crop protection to crop enhancement. While such ben-

eficial uses of pesticides are specifically en vogue for

fungicides and seed treatments, the use of herbicides

for crop enhancement has not yet been realised. The

potential for improving crop production by low-dose,

stimulatory effects of herbicides has been proposed, and

reports of 10–25% efficiency of improving certain plant

traits under field conditions seem promising. However,

past attempts to make use of herbicide hormesis, the term

for this effect, have been largely unsuccessful. The

reasons for this may be manifold, but the lack of

understanding of the principles and mechanisms of this

low-dose phenomenon in plants may have contributed

to the often claimed lack of adequate predictability for

commercial use. Thanks to the research progress recently

made in this area, we are now better able to understand

the principles of herbicide hormesis and its potential for

crop enhancement. Therefore, this review highlights the

potential of phytotoxins to induce plant hormesis and the

factors influencing its expression. Based on this, possible

practical constraints and consequences for the portfolio

of uses for herbicides are discussed, along with undesired

but apparent hormetic side effects of herbicides.

Keywords: allelochemical, biphasic, crop enhancement,

dose–response, growth stimulation, phytotoxin.

BELZ RG, CEDERGREEN N & DUKE SO (2011). Herbicide hormesis – can it be useful in crop production? Weed

Research 51, 321–332.

Introduction

Some substances, although toxic at higher doses, can be

stimulatory or even beneficial at low doses. This biphasic

dose–response phenomenon is commonly termed hor-

mesis and it is also characteristic for many herbicides

and other phytotoxins (Duke et al., 2006; Cedergreen,

2008a). Among the herbicides causing hormesis is

glyphosate, the currently most widely used herbicide

(Schabenberger et al., 1999; Cedergreen, 2008a,b; Velini

et al., 2008). Compared with the classical, monotonic

relation between the dose of a toxin and the resulting

response, hormetic or biphasic response patterns are

characterised by an increase in response at low doses

that changes to inhibition at higher doses.

The numerous reports of phytotoxin-induced horme-

sis in plants (e.g. Duke et al., 2006; Cedergreen et al.,

2007; Calabrese & Blain, 2008; Cedergreen, 2008a)

clearly document that hormesis is a reproducible

phenomenon that might be translated into crop

enhancement if causing a desired phenotypic change.

However, hormetic effects are not necessarily beneficial

for an organism, as for example, increased shoot

elongation at the cost of stem robustness may lead to

Correspondence: Regina Belz, Institute of Plant Production and Agroecology in the Tropics and Subtropics, Department of Agroecology 380b,

University of Hohenheim, 70593 Stuttgart, Germany. Tel: (+49) 711 459 23681; Fax: (+49) 711 459 23629; E-mail: [email protected]

� 2011 The Authors

Weed Research � 2011 European Weed Research Society Weed Research 51, 321–332

more fragile plants, or increased biomass growth at the

expense of pathogen defence compounds could make

treated plants more vulnerable to diseases. Nevertheless,

beneficial hormetic effects of herbicides, such as the

increase of sucrose content in sugarcane by low-dose

glyphosate treatments (Mcdonald et al., 2001) or an

increased pathogen defence induced by low-dose proto-

porphyrinogen-inhibiting herbicide treatments (Nelson

et al., 2002), are valuable agronomic effects that could

be commercially exploited. Although hormetic effects of

herbicides on plants were observed by weed scientists

for decades and for several traits (e.g. growth, biomass,

shoot ⁄plant length, protein content, pest resistance), the

resulting potential for enhancement of certain crop traits

has received relatively low attention. The worldwide

use of low-dose glyphosate treatments in sugarcane to

enhance sugar production is the only example of an

efficient commercial use of herbicide hormesis (Duke

et al., 2006; Dalley & Richard, 2010). This is quite

contrary to the long and efficient commercial use of

high doses of numerous herbicides for weed control.

However, challenged by the future gap between food

demand and availability of agricultural land, some are

convinced that the emphasis in crop production is

changing from crop protection to crop enhancement,

facilitated by new technologies such as pesticide-induced

growth stimulation (Rich, 2008; Cedergreen et al.,

2009). While herbicides play a major role in crop

protection, contemporary approaches to exploit pesti-

cide-induced crop enhancement are restricted to fungi-

cides or seed treatments. Most pesticide companies have

such products or are about to commercialise them (e.g.

Invinsa�, Stratego�, Quilt�, Quadris�, Stamina� fun-

gicides) (Rich, 2008). Therefore, the question now is why

not also exploit herbicide hormesis for this portfolio and

so preserve the current importance of herbicides for

future crop production systems?

The idea to commercially exploit beneficial hormetic

effects of herbicides is not new. However, past attempts

to make use of herbicide hormesis have been largely

unsuccessful except for the use of glyphosate in sugar-

cane (Dalley & Richard, 2010). Despite being proposed

in papers and patents, the technology has not been

adopted. For example, Ries et al. (1967) and Pulver and

Ries (1973) developed considerable evidence that low

doses of triazine herbicides improve nitrogen metabo-

lism in some crops, but this information was not

exploited. Thus, it has been known for quite some time

that herbicide-induced hormesis exists and that it can

clearly enhance crop growth. Why it has not been

successfully exploited is worth exploring. The reasons

for not having commercially used such beneficial effects

of low doses of herbicides on crops may be manifold.

Appleby (1998) considered the insufficient predictability

of hormetic effects to be a major reason. The factors

causing this variability were largely unknown at that

time. Thanks to the renewed interest in herbicide

hormesis and the research progress recently made in

this area, we are now better able to understand the

characteristics and principles of this low-dose phenom-

enon in plants. Several factors influencing the expression

of plant hormesis could be identified that may explain

its unpredictability and hamper its practical use to

stimulate crop growth. Therefore, this review highlights

the potential of phytotoxins to induce plant hormesis

and gives an overview of factors influencing the expres-

sion of this potential. Based on this, possible conse-

quences for the portfolio of uses for herbicides are

discussed. Key points covered will thus be the �potentialportfolio� in terms of what herbicide hormesis is able to

provide and �practical constraints� that are by nature

associated with the phenomenon of hormesis in plants.

Furthermore, as plants can be unintentionally exposed

to low doses of herbicides, the last aspect covered is the

�unwanted portfolio� in terms of undesired, but apparent

hormetic side effects of herbicides. The results presented

have been mainly conducted using two different test

systems: (i) a small-scale laboratory test system using a

lettuce (Lactuca sativa L.) bioassay according to Belz

and Cedergreen (2010) as test species and (ii) root

application of phytotoxins and more field-oriented trials

conducted with Sinapis arvensis L. (white mustard),

Hordeum vulgare L. (barley), or Fragaria vesca L.

(strawberry) after spray application and cultivation of

plants under controlled (glasshouse), semi-field (vegeta-

tion hall) or field conditions (for experimental details see

Belz, 2008; Cedergreen, 2008b; Cedergreen et al., 2009;

Andresen & Cedergreen, 2010). Within these test

systems, mainly three phytotoxins have been evaluated,

which are as follows: (1) the anti-auxin PCIB (2-(p-

chlorophenoxy)-2-methylpropionic acid), as auxins are

known to induce hormetic effects (e.g. El-Zeftawi, 1976;

El-Ohtmani et al., 1993; Allender, 1997; Guardiola &

Garcia-Luis, 2000), (2) the sesquiterpene lactone par-

thenin, a natural plant phytotoxin causing growth

stimulatory effects on several plant traits at low doses

(Belz, 2008; Belz & Cedergreen, 2010) and (3) the well-

known herbicide glyphosate inhibiting the shikimate

acid pathway at higher doses and stimulating plant

growth at lower doses (Cedergreen, 2008a,b; Velini

et al., 2008). Besides these pure compounds, a natural

mixture of phytotoxic plant metabolites was included

to illustrate that hormesis of plant extracts can be

pronounced and commercially used. This quite diverse

group of hormetic agents was chosen in order to

highlight the generalisability and the diversity of hor-

metic response patterns. Results will be mostly illus-

trated in the form of dose–response curves that cover

322 R G Belz et al.



both stimulatory and adverse effect concentrations,

an essential prerequisite to prove the existence of a

hormetic effect (Duke et al., 2006). Modelling of dose–

response curves was facilitated by using the biphasic

regression models developed by Brain and Cousens

(1989) or Cedergreen et al. (2005) (for statistical details

see also Cedergreen, 2008a,b; Cedergreen et al., 2009;

Belz & Cedergreen, 2010).

The �potential portfolio� of herbicidehormesis

Developing a herbicide is time and cost intensive and,

thus, attempts to expand the portfolio by hormetic

effects is only reasonable if herbicides do really have

a considerable potential for crop enhancement. The key

questions are whether the maximum stimulation that

can be achieved is large enough to justify exploiting this

phenomenon and whether combining crop protection

with crop enhancement may provide additional pros-

pects for crop production.

Maximum stimulation

The magnitude of stimulatory responses observed in all

fields of sciences, and for different toxicants, organisms

and endpoints, ranges on average between 30% and

60% stimulation above control (Calabrese & Blain,

2005; Calabrese, 2008, 2010). Literature values for

herbicides range on average between 20% and 30%

stimulation above control under more controlled condi-

tions and between 10% and 25% under field conditions,

which is in the low range of the general hormetic

increase reported, but still striking compared with what

can be achieved in plants on a yearly basis by breeding

or molecular biotechnology (Cedergreen et al., 2005,

2007, 2009). Furthermore, this average range can be

considerably exceeded to up to 200% stimulation,

depending on several factors such as compound, trait,

time, or the study design in general (Calabrese, 2008;

Velini et al., 2008).

Compound-specific variations

Comparing the hormetic effect of different phytotoxic

compounds on root elongation of L. sativa under

standard conditions in the lettuce assay shows that not

every herbicidal compound is equally effective in induc-

ing hormesis in a certain trait and some may not even

show the response (Fig. 1). This was also shown in a

database study by Cedergreen et al. (2007) for various

herbicides and a glasshouse study by Cedergreen (2008a)

testing herbicides with eight different modes of action

on H. vulgare. In this study, only glyphosate and the

sulfonylurea metsulfuron-methyl showed consistent

hormesis.

A pronounced hormetic effect is consistently

observed within the lettuce assay for the two sesquiter-

pene lactones parthenin and tetraneurin-A (Fig. 1A)

and the anti-auxin PCIB (Fig. 1B). The magnitude of

hormesis and the hormetic dose range is generally less

pronounced and narrower for the two sesquiterpene

lactones, as compared with the broader range of PCIB

doses stimulating root growth of lettuce. This shows that

the magnitude of hormesis is not the only quantitative

hormetic feature that can vary between phytotoxins.

The two sesquiterpene lactones showed on average 79%

stimulation in root growth, within a hormetic dose range

characterised by a 2.4-fold increase in concentration

between the dose giving maximum stimulation and

the dose where the hormetic effect has disappeared. This

range is rather small compared with the general

hormetic dose range of an average 5-fold dose increase

(Calabrese & Baldwin, 2002a,b), but falls within the

prevalent range of the hormetic dose range observed

in plant biology studies (‡1- to <5-fold) (Calabrese &

Blain, 2008).

A Sesquiterpenlactones B Auxins C Glyphosate

00.25

0.50.75

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22.25

Concentration (μmol mL–1)

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Control0

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0.751

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Concentration (μmol mL–1)

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Control0

0.25

0.5

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1.25

0.1 1 10 0.001 0.01 0.1 1 10 0.001 1 1000

Glyphosate (μmol mL–1)

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Control

Fig. 1 Dose–response relationships of selected phytotoxins achieved under standard conditions in the lettuce assay on root elongation

of Lactuca sativa [5 days after treatment (dat)]. Maximum stimulation of root length above control of 101% for PCIB, 91% for tetraneurin-

A, and 66% for parthenin, while for indole-3-acetic acid (IAA) and glyphosate no significant stimulation was observed (lettuce assay

according to Belz & Cedergreen, 2010) (RG Belz & N Cedergreen, unpubl. obs.).

Hormesis and herbicide use 323



The physiological mechanisms causing individual

biphasic dose responses in plants are still widely

unknown. In mammalian cell cultures, however, mech-

anistically explained examples of biphasic dose–response

curves do exist. Mammalian breast cancer cells will for

example increase their proliferation rates when exposed

to low doses of oestrogenic compounds, until a certain

threshold where the compound starts to be toxic.

Thereafter, cell proliferation decreases (Calabrese,

2001). This is an example of a compound having one

primary mode of action at low concentrations while

another, more lethal mode of action, increases in

importance as concentrations increase. This might very

well be the case for herbicide effects on plants also.

Another example of a mechanistic explanation for

hormetic effects is the growth-enhancing effect of the

strobilurin fungicides. These fungicides have been shown

to be related to a shifted hormone balance favouring

cytokinins, as opposed to ethylene, leading to a so-called

greening effect, which leaves more time for grain filling

under optimal growth conditions (Grossmann et al.,

1999). Other examples have been described from mam-

malian cell cultures where chemicals induce a diversion

of substrate from one branch of a pathway towards

another via inhibition of central enzymes in the pathway

(Ohlsson et al., 2009). If the �benefitting� pathway is

linked to the endpoint of interest, a hormetic response

will be observed. It is very likely that similar mechanisms

are responsible for some of the hormetic effects observed

in plants. However, until more mechanistic studies on

plants have been made, quantitative features are the

only means to measure the compound-specific diversity

in dose–response patterns. Nevertheless, with a higher

maximum stimulation of 101% and a broader 3.2-fold

dose increase in the lettuce assay, compounds like PCIB

may hold a more favourable potential for crop enhance-

ment and may allow using low doses that may under no

circumstances turn inhibitory. In contrast to the sesqui-

terpene lactones and PCIB, glyphosate and the natural

auxin indole-3-acetic acid (IAA) do not stimulate root

elongation under standard conditions in the lettuce

assay, although biomass growth-enhancing effects have

been previously observed in other test systems for both

compounds (Ali et al., 2008a,b; Cedergreen, 2008a,b;

Cedergreen et al., 2009) (Fig. 1C). The reasons for this

differential ability of compounds to induce hormesis

is most likely related to the mechanism with which the

growth stimulations are produced.

Trait-specific variations

A hormetic response can be measured on various

parameters. However, a stimulatory response in one

trait does not necessarily correlate with a stimulatory

response in another trait (Duke et al., 2006). The fact

that not every trait is equally responsive to the induction

of hormesis by a specific compound was demonstrated

for parthenin on S. arvensis after spray application

(Fig. 2A).

At 14 days after treatment, Belz (2008) observed a

slight, non-significant hormetic effect of 13% stimula-

tion on shoot dry weight, a more pronounced stimula-

tion of 21% in shoot length and a maximum stimulation

of 38% in leaf area growth. These magnitudes of

stimulation are considerably lower than the stimulation

usually observed for root elongation of lettuce treated

by parthenin (Figs 1 and 2B). However, compared with

the multiple crop trait stimulation by parthenin ob-

served after spray application, parthenin hormesis

proved to be specifically restricted to root elongation

in the lettuce assay. Here, leaf area growth, shoot dry

weight and leaf chlorophyll content showed monotonic

dose–response relationships, in contrast with the

A Sinapis arvensis B Lactuca sativa C Lactuca sativa

0

0.25

0.5

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Parthenin (kg ha–1)

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Control0

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Parthenin (μmol mL–1)

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Leaf areaShoot dry weightRoot lengthLeaf chlorophyll content

Control0

0.5

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2

2.5

3

0.1 1 10 0.1 1 10 0.01 0.1 1 10PCIB (μmol mL–1)

Rel

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spon

se

Leaf areaShoot dry weightRoot length

Leaf chlorophyll content

Control

Fig. 2 Dose responses measured on different parameters. (A) Effects of parthenin after spray application on Sinapis arvensis [14 days

after treatment (dat)]. Maximum stimulation of 38% in leaf area, 21% in shoot length and 13% in shoot dry weight (adapted from Belz,

2008). (B) Effects of parthenin after root application in the lettuce assay (15 dat). Maximum stimulation of 95% in root length, while

no significant stimulation was observed for shoot dry weight, leaf area and leaf chlorophyll content (adapted from Belz & Cedergreen, 2010).

(C) Effects of PCIB after root application in the lettuce assay (15 dat). Maximum stimulation of 134% in root length and 71% in leaf

chlorophyll content, while no significant stimulation was observed for shoot dry weight and leaf area (RG Belz unpubl. obs.) (lettuce

assay according to Belz & Cedergreen, 2010).

324 R G Belz et al.



biphasicity in root elongation with 95% stimulation

above control (Fig. 2B). Hence, the pattern of traits

stimulated by a specific compound also depends on

the test system studied. Differences in the patterns of

stimulated traits may also be observed depending on test

conditions and ⁄or the compound studied. For example,

leaf chlorophyll content of L. sativa was stimulated

along with root elongation in the lettuce assay in case of

PCIB, but not parthenin (Fig. 2C). The observed

stimulation in leaf chlorophyll content was, however,

1.9-fold lower than the increase in root elongation.

Therefore, achieving a desired stimulation in one or

more traits requires applying the right compound in the

right biological setting.

Time-specific variations

A hormetic growth increase can only be transferred into

a harvestable yield if the induction is applied at the right

time, as the time span for the occurrence of a hormetic

response is limited. For example, studying the time

progression of the hormetic response of parthenin on

leaf area growth of S. arvensis showed that hormesis

needs time to develop (Belz, 2008). No hormetic effect

was detectable between 2 and 6 days after treatment,

while hormesis started from about 8 days after treat-

ment, reaching a maximum after 13 days after treatment

(Fig. 3A).

Comparisons showed that at doses inducing stimula-

tory responses 13 days after spraying, leaf area was

initially inhibited up to 50% (2 days after spraying).

This indicates that parthenin hormesis may represent a

time-consuming, adaptive response to an initial toxic

effect, a feature that would be consistent with the

hypothesis of an overcompensation stimulation process

underlying the hormetic response, rather than a direct

stimulatory mode of action (Calabrese, 2008, 2010). In

addition, studies with glyphosate hormesis onH. vulgare

showed that the hormetic effect is not sustained over

time (Cedergreen, 2008b). Here, the initial 37% increase

in shoot dry weight, obtained 1 week after spraying

7-day-old plants, disappeared starting from about

7 weeks after application (Fig. 3B). Spraying barley

plants closer to grain filling, however, maintained the

stimulatory effect until harvest (Cedergreen et al., 2009).

Thus, the time span between application and harvest

seems of great importance. Another option to transfer

a hormetic effect into a harvestable yield is to try to

prolong the timeframe of hormetic growth stimulation

by repeated applications of the inducing agent. For

example, this was carried out to increase berry yield of

strawberry with water extracts of deoiled tea seeds (Tea

Seed Powder, Co. Nor-Nature), a saponin-rich waste

product from tea seed (Camellia spp.) oil production,

which had induced hormesis in Lemna minor L. and

terrestrial species. Here, a weekly spray application of

1.5 g m)2 during the entire growing season increased the

yield of the berries by 39% without affecting any other

plant trait. The observed beneficial effect on berry yield

was however not carried over to the next growing season

(Fig. 3C and D) (Andresen & Cedergreen, 2010).

Recognising hormesis as a dynamic process has

substantial consequences for studying and exploiting

A Parthenin B Glyphosate

0

6

5

4

3

2

1

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15

10

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00 10 20 30 40 50 380 385 390 400395

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pot

2 Dat8 Dat14 Dat

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ant

7 Dat49 Dat

Control

C Tea seed extract D Tea seed extract

Days after planting

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ries

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nt

2008

Untreated control plantsSprayed plants

Days after planting

Nu

mbe

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ber

ries

per

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Untreated control plantsSprayed plants

Fig. 3 Time expression of the hormetic

effect. (A) Effect of parthenin on leaf area

growth of Sinapis arvensis after spray

application. No significant stimulation at 2,

4 and 6 days after treatment (dat), 15%

stimulation above control at 8 dat, and

38% stimulation at 14 dat (adapted from

Belz, 2008). (B) Effects of glyphosate on

shoot dry weight of Hordeum vulgare after

spray application. The maximum

stimulation of 36% observed at 7 dat

disappeared starting from 49 dat (adapted

from Cedergreen, 2008b). (C) Berry yield

of strawberries in 2008 (C) and 2009 (D)

sprayed with extracts of deoiled tea seeds in

2008. The yield in 2009 was not affected by

the treatment in 2008, as would have been

expected if a trade-off between present

yield and investment in future growth had

taken place; significant differences are

marked with an asterisk (t test, P < 0.05);

error bars indicate standard error (adapted

from Andresen & Cedergreen, 2010).




this phenomenon, as there might be only a certain

timeframe wherein significant levels of stimulation are

present and, hence, hormesis is detectable and func-

tional. Nevertheless, low-dose glyphosate applications

increasing grain yield in H. vulgare or sugar yield in

sugarcane under field conditions show that even such a

temporal phenomenon can be efficiently used (Mcdon-

ald et al., 2001; Cedergreen et al., 2009).

Combining crop protection with crop enhancement

The fact that species differ in their susceptibility to

herbicides provides the basis for dose-selective weed

control. In the low-dose range, this differential suscep-

tibility may be exploited similarly, as it offers the

potential to select a dose where a less sensitive (crop)

plant may be stimulated, while a susceptible (weed)

species may be efficiently controlled. Comparing the

hormetic responses of L. sativa and Ageratum conyzo-

ides L. to parthenin shows that this approach is possible,

as the dose giving maximum stimulation of L. sativa

(31% stimulation) equalled the ED60 (60% inhibition) in

A. conyzoides (Fig. 4A). The same could be observed

comparing the responses of L. sativa and Gypsophila

paniculata L., where the latter was inhibited by 70%

at the dose giving maximum stimulation in L. sativa

(Fig. 4B). However, a significant constraint for the

practical usage of this approach may be that the

optimum time for weed control may not coincide with

the optimum time of inducing a desired phenotypic

change or stimulation in a harvestable trait. Neverthe-

less, if we achieve combining crop protection with crop

enhancement in this manner, herbicide hormesis may

offer enhancement of crop yield at doses that also

provide some measure of weed control.

The examples show that there is considerable

potential for crop enhancement by herbicide hormesis,

at levels similar to or greater than that achieved by

breeding or modern biotechnology. Stimulation of a

certain crop trait, or several crop traits at once, that

leads to desired phenotypic changes can be of economic

significance for a farmer. Furthermore, the prospect of

retaining weed management options if weeds exposed

to a hormetic herbicide dose are controlled provides an

additional advantage for the farmer. However, the given

examples also show that hormesis is not just trivial low-

dose stimulation, but varies between phytotoxins, traits

and species. Therefore, understanding the phenomenon

and the associated practical constraints for specific

crop ⁄weed ⁄herbicide combinations will be essential to

efficiently exploit potential benefits and ensure against

potential risks.

The �practical constraints� of herbicidehormesis

A major problem associated with herbicide hormesis

seems to be the fact that the hormetic effect varies if

plants are exposed to multiple stressors, especially those

encountered under field conditions. This will be dem-

onstrated in the following sections on the basis of the

dose responses of L. sativa if exposed to selected cases

of stress prior to or during the exposure to hormetic

compounds.

Nutrient stress

The standard lettuce assay [according to Belz et al.

(2008) and Belz and Cedergreen (2010)] is conducted

without nutrients, and under these conditions, parthenin

displays a consistent and pronounced hormetic effect on

root elongation of L. sativa. However, conducting the

test with a complete nutrient solution eliminated the

hormetic effect (Belz & Cedergreen, 2010) (Fig. 5A).

With optimal nutrient supply, the growth of control

plants almost equalled the maximum stimulation ob-

served without nutrients. Belz and Cedergreen (2010)

concluded that the addition of nutrients diminished the

A B

00.20.40.60.8

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Parthenin (µmol mL–1)

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Lactuca sativaAgeratum conyzoides

Control0

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Lactuca sativaGypsophila paniculata

Control

Fig. 4 Differential susceptibility of root growth of different species to parthenin under the conditions of the lettuce assay. Maximum

stimulation above control was 37% in Ageratum conyzoides compared with 31% in Lactuca sativa (A) and 38% in Gypsophila paniculata

compared with 33% in L. sativa (B). The dose giving maximum stimulation in L. sativa equalled the ED60 in A. conyzoides and the

ED70 in G. paniculata (from data discussed in Belz et al., 2007; RG Belz, unpubl. obs.).

326 R G Belz et al.



plasticity for hormesis, as a result of increasing growth

of control plants to the maximum response potential of

root elongation achieved under standard conditions in

the lettuce assay. Hence, it appears that the magnitude

of hormesis reflects a response potential that is limited

by the plasticity of the biological system and cannot be

manipulated to achieve multi-fold increases (Calabrese,

2008, 2010). Therefore, hormetic crop enhancement may

only be possible if plants grow under below optimum

conditions because of stress. In other words, hormetic

applications of a phytotoxin may enable the plant to tap

into its genetic potential, but not to bypass it. Another

constraint that becomes evident studying the influence

of nutrient supply on parthenin hormesis is the fact that

low-dose effects are more variable than high-dose

inhibition where the only possible outcome is inhibition.

At low doses, plants may show no significant response,

low-dose toxicity, or hormesis (Fig. 5A). This makes the

use of stimulatory responses more vulnerable to influ-

encing abiotic factors.

Temperature stress

A similar reliance of parthenin hormesis on plant growth

conditions was observed for the influence of temperature

(Belz & Cedergreen, 2010). The standard lettuce assay

is conducted at a day ⁄night cycle of 24 ⁄ 18�C.Under these

standard conditions, parthenin hormesis amounted to

61% stimulation, while at a warmer temperature regime

(30 ⁄ 25�C), the magnitude of hormesis was 1.8-fold lower

and hormesis was even absent at a cooler temperature

regime (15 ⁄ 10�C) (Fig. 5B). Comparing control plant

growth showed that at the warmer temperature regime,

the plasticity for hormesis was lowered because of an

increased control plant growth. At the cool temperature

regime, control plant growth was retarded compared

with standard conditions and obviously the poorly

growing plants did not have the ability for a stimulatory

response within 5 days of exposure. This shows that the

expression of hormesis can be hampered under poor

growth conditions. However, extending the experiment

for another 5 days showed that the hormetic effect of

parthenin was not actually absent under the cool treat-

ment, just the time-expression was delayed as a result of

retarded growth (Fig. 5B).

Now, is this temperature response pattern observed

with parthenin hormesis generally valid? Studying PCIB

hormesis under identical experimental conditions

showed that the reliance on influencing factors is also

compound specific. After 5 days of exposure to PCIB,

A Nutrient supply B Temperature

00.5

11.5

22.5

33.5

4


Roo

t le

ngt

h (

cm)

Full strength nutrient supplyStandard assay (no nutrients)

Control0

0.51

1.52

2.53

3.54

4.55


Roo

t le

ngt

h (

cm)

15/10°C, 10 d15/10°C, 5 dat30/25°C, 5 datStandard assay (24/18°C, 5 dat)

Control

C Temperature D Plant density

00.5

11.5

22.5

33.5

44.5

5

PCIB (μmol mL–1)

Roo

t le

ngt

h (

cm)

15/10°CStandard assay (24/18°C)

Control0

0.5

1

1.5

2

0.1 1 10 0.1 1 10

0.01 0.1 1 10 0.001 0.01 0.1 1 10

PCIB (μmol mL–1)R

oot

len

gth

(cm

)

3 seeds30 seedsStandard assay (10 seeds)

Control

Fig. 5 Influence of experimental conditions on the hormetic effect on root elongation of Lactuca sativa in the lettuce assay. (A) Effect

of parthenin depending on nutrient supply. The maximum stimulation above control of 78% observed under standard conditions

disappeared when adding a full strength nutrient solution (adapted from Belz & Cedergreen, 2010); (B) Effect of parthenin depending

on temperature regime. The maximum stimulation of 61% observed under standard conditions decreased to 34% at the warmer growth

conditions and was delayed under the cooler condition (adapted from Belz & Cedergreen, 2010). (C) Effect of PCIB depending on

temperature regime. Maximum stimulation was 78% under standard conditions and 112% under the cooler condition (RG Belz, unpubl.

obs.). (D) Effect of PCIB depending on plant density. Maximum stimulation was 78% at three seeds per replicate and 46%

at standard conditions, while no significant hormesis was observed at 30 seeds per replicate (RG Belz, unpubl. obs.).




L. sativa showed a pronounced hormetic effect indepen-

dent of cool growth conditions (Fig. 5C). Moreover,

PCIB induced a 1.4-fold more pronounced hormetic

effect under cool conditions, as compared with standard

conditions, with a lower absolute growth level (RG Belz,

unpubl. obs.). Thus, PCIB hormesis seems to be more

reliably expressed under variable growth conditions than

parthenin hormesis. This reflects again the diversity of

hormetic responses and supports the assumption that

the mechanisms behind individual biphasic dose–

response relationships may rarely be the same (Ceder-

green, 2010).

Plant competition

Another stressor that plants are usually exposed to

under field conditions is plant competition. Competition

is well known to affect general plant growth patterns

and, therefore, the question is how plant density may

influence the hormetic outcome in the lettuce assay. The

standard assay is conducted at a density of 10 seeds per

replicate. Under these standard conditions, PCIB hor-

mesis induced 46% stimulation (Fig. 5D). While hor-

mesis was absent at a higher plant density of 30 seeds

per replicate, lowering the density to 3 seeds per

replicate increased the magnitude of hormesis to 77%.

Comparing control plant growth showed that increasing

plant competition increased control plant root growth to

the maximum response potential, leaving no plasticity

for a significant hormetic effect of PCIB. In contrast to

this, alleviating plant competition decreased root elon-

gation of control plants, while promoting PCIB induced

growth stimulation compared with standard conditions

(RG Belz, unpubl. obs.). If this holds true under field

conditions, high crop plant densities or intense weed

infestation may be counterproductive to hormesis. On

the other hand, if producers are economically forced to

reduce planting rates, herbicide hormesis may even be an

option to compensate for resulting yield losses.

Preconditioning

Precondition hormesis or chemical conditioning hor-

mesis are terms describing the situation where an

organism has been exposed to a mild level of stress

prior to the main stressor (Calabrese et al., 2007). Such

a pre-exposure can initiate defence systems or initiate

damage that will affect the response to the exposure of

a second chemical (Kovalchuk et al., 2003). The first

mechanism is for example exploited when using herbi-

cide safeners (Riechers et al., 2010). The mechanism of

damage initiation was exploited to produce a hormetic

effect on growth of Sinapis alba L. by the allelochem-

ical juglone. Here, a hormetic effect only appeared for

methanol pre-treated S. alba seedlings (Chobot &

Hadacek, 2009). As preconditioning with methanol is

proposed to increase the production of reactive oxygen

species (ROS), Chobot and Hadacek (2009) hypothes-

ised that the observed preconditioning hormesis by

juglone may rely on its ROS scavenging capacity.

Glyphosate is not known to scavenge ROS, but

glyphosate exposure was shown to enhance the expres-

sion of genes involved in oxidative stress protection

(Ahsan et al., 2008). Therefore, we investigated

whether glyphosate may require a ROS-promoting

methanol pre-treatment to induce hormesis in a seed

germination assay like the lettuce assay. Furthermore,

we investigated the effect of a ROS-promoting pre-

treatment on hormesis induced by compounds that are

not believed to directly influence ROS levels in plants.

As shown in Fig. 6, the results proved again very

compound specific.

The methanol treatment induced a hormetic response

to glyphosate in three of five experiments and consistently

delayed the hormetic response to parthenin (Fig. 6A and

B), while the methanol pre-treatment did not dramati-

cally affect the hormetic response to PCIB, or the lack of

hormesis in IAA treated seedlings (Fig. 6C andD).While

the methanol induced repression of parthenin hormesis

can be viewed as a result of general growth depression

similar to the response to lowering temperatures (Fig. 5

B), the occurrence of glyphosate hormesis is more difficult

to explain. Whether the response is really related to a

putative influence on ROS scavenging capacity cannot

be answered with our present knowledge of the modes

of action of glyphosate. Nevertheless, the diversity of

response patterns observed here for four proven hormetic

compounds indicates again that the physiological mech-

anism causing the response determines the hormetic

outcome under multiple-stressor conditions. The rather

large differences in hormetic effects with different phyto-

toxins suggest that there are different mechanisms of

hormesis for different compounds. Thus, with some

phytotoxins, hormesis may not be simply a response to

mild stress, oxidative or otherwise.

These examples show that hormetic effects are highly

variable, depending on several influencing factors of

which we have demonstrated just a few. These variations

may put considerable constraints on the reproducibility

of hormesis and, thus, on its commercial use. It is

therefore questionable if phytotoxin-induced hormesis

can ultimately be used to predictably increase crop yield

under the conditions encountered in the field (Belz

& Cedergreen, 2010). The potential might rather be for

glasshouse production, where growth conditions can

be more carefully regulated. On the other hand, the

demonstrated diversity of hormetic effects may allow

selection of compounds inducing reliable, consistent

328 R G Belz et al.



growth stimulation in plants, even if they are exposed to

multiple stressors.

The �unwanted potential� of herbicidehormesis

Theoretically, herbicide hormesis may unintentionally

appear in practice, because of drift deposition, errors in

application, absorption of low doses from soil, especially

after soil degradation or immobilisation, leaf contact of

treated and untreated plants, protection by taller plants

or mulch (Velini et al., 2010), or herbicide resistance.

Although some farmers may occasionally inadvertently

benefit from this phenomena if crops are affected (Velini

et al., 2010), the phenomena is unwanted, as it may

hamper weed management or crop production. Drift-

related hormesis has been reported for 2,4-D (Appleby,

1998) and is also relevant for glyphosate, as drift rates

equate to stimulatory doses (Cedergreen, 2008b). Fur-

thermore, Belz et al. (2009) showed that soil immobil-

isation and degradation of toxic doses of parthenin can

lead to soil concentrations that are stimulatory to

overall plant growth. In terms of �beneficial� after-effectson crop or weeds in the following crop, this may be

relevant for some herbicides as well. For example, Bott

et al. (2011) observed growth-stimulating effects on

soyabean after soil application of toxic doses of

glyphosate, because of re-mobilisation of trace amounts,

but only in soils with a high fixation potential for

glyphosate.

In an ecosystem context, such stimulatory spray drift

events or �beneficial� after-effects may alter competition

between species, as boosted plants may have a compet-

itive advantage over competitors that are not or are

adversely affected (Cedergreen, 2008b). From an agri-

cultural point of view, the case of crops being stimulated

by low doses of herbicides not registered for use seems

to be more important, especially if herbicide residues

contaminate the harvested product. However, recogni-

tion of such potential stimulatory spray drift events or

after-effects under field conditions might be difficult and,

thus, reports on the practical relevance of such effects

are absent. The same is true for effects of recommended

herbicide doses on herbicide-resistant weeds, which is

the focus in the following section.

Herbicide resistance

Hormesis may be of particular importance for the use

of herbicides for which weeds have evolved resistance.

Especially for biotypes with high resistance factors, the

recommended field rate may represent a low dose and,

thus, a potential hormetic dose. Furthermore, Calabrese

and Baldwin (2002a) stated that highly resistant indi-

viduals are especially responsive to hormesis. Therefore,

applying the recommended field rate may not only

directly select resistant biotypes from a sensitive popu-

lation, it may also indirectly promote the success and

spread of resistant biotypes because of hormetic effects.

In doing so, hormetic effects would not directly cause

selection pressure for evolution of resistance, but may

indirectly influence the development of resistance by

making boosted plants more competitive, more repro-

ductive, or more tolerant to a second weed control

A Glyphosate B Parthenin

0

0.5

1

1.5

2

2.5

3

Glyphosate (μmol mL–1)

Roo

t le

ngt

h (

cm)

MeOH pretreatmentStandard assay

Control0

1

2

3

4

5

6


Roo

t le

ngt

h (

cm)

MeOH pretreatment (10 d)MeOH pretreatment (5 d)Standard assay(5 d)

Control

C PCIB D IAA

0

1

2

3

4

5

6

PCIB (μmol mL–1)

Roo

t le

ngt

h (

cm)

MeOH pretreatmentStandard assay

Control0

0.5

1

1.5

2

2.5

3

0.001 1 1000 0.1 1 10

0.01 0.1 1 10 0.001 0.1 10

IAA (μmol mL–1)

Roo

t le

ngt

h (

cm)

Standard assayMeOH pretreatment

Control

Fig. 6 Influence of an initial oxidative

stress on the dose responses of glyphosate

(A), parthenin (B), PCIB (C), and indole-3-

acetic acid (IAA) (D) measured on root

elongation of Lactuca sativa in the lettuce

assay. Seedlings were pre-germinated for

2 days in water (standard) or 5% methanol

(MeOH) (after Chobot & Hadacek, 2009).

Maximum stimulation under standard

conditions was 0% for glyphosate and

IAA, 80% for parthenin and 101% for

PCIB. Pre-treated plants showed 0%

stimulation for parthenin [5 days after

treatment (dat)] and IAA, 40% for

glyphosate, 156% for PCIB and 80% for

parthenin after 10 dat (RG Belz, unpubl.

obs.).




measure. Hence, is hormesis an underestimated factor

in the development of resistance? At the moment, this

question is unanswerable, but recent reports point to the

possibility. Growth stimulation in resistant biotypes,

following application of the herbicide they developed

resistance to, has been recently reported for ACCase

target-site resistant biotypes of Alopecurus myosuroides

Huds. treated with fenoxaprop-P-ethyl (Fig. 7A) or

cycloxydim (Fig. 7B) (Petersen et al., 2008) and a

triazinone-resistant biotype of Chenopodium album L.

treated with metamitron (Fig. 7C) (J Petersen, unpubl.

obs.). The maximum growth stimulation on ACCase-

and triazinone-resistant biotypes ranged between 25%

above control to up to 104%. However, these effects

were induced at doses less than or exceeding recom-

mended field rates. Exposure to doses equalling field

rates increased shoot growth by 0–47% (Fig. 7).

Hence, the field rate does not necessarily represent

the dose causing maximum stimulation, but may still

cause a considerable growth stimulatory effect on

resistant weed biotypes. Therefore, these reports indicate

a substantial potential to promote herbicide resistant

weed biotypes at recommended field rates and suggest

considering herbicide hormesis as a potential factor

boosting the development of herbicide resistant weeds.

Future studies investigating the potential impact of this

phenomenon should, however, consider two important

issues. First, if the use of the stimulating herbicide is

continued despite the occurrence of target-site resis-

tance, it is normally used in mixture with herbicides

that still control the resistant biotype. Second, growth

stimulation may have no long-term impact if boosted

plants are not more reproductive. Nevertheless, the fact

that target-site resistant weed biotypes with altered site

of action seem to be highly responsive to herbicide

hormesis indicates that the phytotoxicity at very high

doses may be because of a different mode of action, as

has been suggested by Cedergreen (2008a). However,

in some cases of target-site resistance, the target site is

still affected by the herbicide, but at higher doses. Thus,

whether the hormetic mode of action is the same as the

one at higher doses and what makes resistant biotypes

especially responsive to hormesis needs to be experi-

mentally examined.

Promoting weed growth at field rates is clearly

undesirable. However, this effect may be turned into a

desired one, as it may be a method for improving the

yield of herbicide-resistant or tolerant crop plants. From

an agricultural point of view, hormetic effects in

herbicide-resistant crops may be one of the most

interesting aspects of herbicide hormesis. This will not

work in cases where the hormetic effect really turns out

to be related to the herbicide target. On the other hand,

there exist respective patents for glutamine synthase

inhibitors (e.g. bialaphos, glufosinate; Donn, U.S. Pat-

ent No. 5,739,082) and glyphosate or derivatives thereof

(Brants and Graham, U.S. Patent No. 6,083,878),

stating that yield increases of up to 50% can be achieved

if crops that have been made resistant ⁄ tolerant to the

respective herbicide are treated with concentrations that

equal those normally used to combat weeds. Provided

that the optimum time of weed control coincides with

the optimum time of growth stimulation, crop enhance-

ment at recommended field rates also has the advantage

that the herbicide does not need to be registered as a

growth stimulator as is the case with the strobilurin

fungicides. Although these patents have not been put

into agricultural practice, they provide a rationale for

combining crop protection with crop enhancement.

Conclusions

Considering the many reports of hormesis induced by

herbicidal compounds, it is clear that hormesis is real

A Alopecurus myosuroides B Alopecurus myosuroides C Chenopodium album

0

0.2

0.4

0.6

0.8

1

1.2

1.4

1.6

Fenoxaprop-P-ethyl (g a.i. ha–1)

Rel

ativ

e sh

oot

biom

ass

Biotype RotHaSensitive biotype

Control

Field rate

00.20.40.60.8

11.21.41.61.8

Cycloxydim (g a.i. ha–1)

Rel

ativ

e sh

oot

biom

ass

Biotype 635Biotype RotHaSensitive biotype

Control

Field rate

0

0.5

1

1.5

2

2.5

1 1000 1 000 000 10 1000 100 000 100 1000 10 000

Metamitron (g a.i. ha–1)

Rel

ativ

e sh

oot

biom

ass

Biotype 177Sensitive biotype

Control

Field rate

Fig. 7 Differential susceptibility of sensitive and resistant biotypes of Alopecurus myosuroides to fenoxaprop-P-ethyl (FEN) (A) or

cycloxydim (B) and of Chenopodium album to metamitron (C) after spray application in greenhouse studies. Biotype RotHa with

ACCase target-site mutation at pos. 1781 (Germany) showed a maximum stimulation of 39% at increased FEN doses and a maximum

stimulation of 54% at reduced cycloxydim doses. Biotype 635 with ACCase target-site mutation at pos. 1781 & 2078 (Germany) showed

a 25% increase by reduced cycloxydim doses. Biotype 177 with suspected triazinone resistance (Germany) showed a maximum stimulation

of 104% at reduced metamitron doses (from data discussed in Petersen et al., 2008; J Petersen, unpubl. obs.).

330 R G Belz et al.



and relevant to the use of herbicides in the field. The

diversity of hormetic effects indicates several potential

approaches to exploit this phenomenon for new plant

production systems. As the achievable increases in crop

traits can be similar or higher to those from breeding

and molecular biotechnology, we have to ask the

question: is hormesis a promising option for the

portfolio of herbicide uses? There have been attempts

to use herbicide hormesis in the past, but none of them

reached commercialisation, other than the use of

glyphosate to enhance sugar production in sugarcane.

As a result of the research progress achieved in this area,

we now know more about the factors affecting the

expression of hormetic responses. We are, however, still

far from completely understanding the mechanisms

underlying chemically induced growth stimulation. At

the moment, the compound specificity of the phenom-

enon indicates that not every phytotoxin or commercial

herbicide showing hormesis is suitable for use. As past

attempts to exploit hormesis have mainly used commer-

cial herbicides that have been selected for efficient weed

control, a hormesis-oriented screening of eligible com-

pounds may help to identify compounds that produce

stable and consistent hormesis, or at least enable an

environmental window for hormesis applications that

can assure a predictable effect. Nevertheless, at the

moment it appears that the hormetic approaches we

have proposed will be limited, because of their sensitivity

to interactions with growth factors. Whether the obvi-

ous risk of not achieving a yield increase is low enough

to justify the cost of the treatment needs to be verified.

On the other hand, farmers may rather ask themselves

what they may lose by omitting a crop enhancing

treatment, rather than if it will pay for itself (Rich,

2008). We suggest that future research will show which

hormetic approaches can be efficiently and reasonably

integrated in new crop production systems and which

will remain only of academic interest.

Acknowledgements

The technical assistance provided by Alexandra Heyn

is greatly acknowledged. Data of herbicide-resistant

weed biotypes are a courtesy of Prof Dr Jan Petersen.

RG Belz was funded by the German Research Associ-

ation (DFG Einzelforderung, project BE4189 ⁄ 1-1). Theauthors sincerely thank two anonymous reviewers for

their constructive comments.

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Herbicide hormesis – can it be useful in crop production?