Annals of Applied Biology ISSN 0003-4746
REVIEW ARTICLE
In the light of new greenhouse technologies: 1. Plant-mediated
effects of artificial lighting on arthropods and tritrophic
interactions
I. Vänninen1 , D.M. Pinto1 , A.I. Nissinen1 , N.S. Johansen2 & L. Shipp3
1 MTT Agrifood Research Finland, Plant Production Research, Jokioinen 31600, Finland
2 Bioforsk Plantehelse, Norwegian Institute of Agricultural and Environmental Research, Hoegskoleveien 7, N-1432 Ås, Norway
3 Agriculture and Agri-Food Canada, Greenhouse and Processing Crops Research Centre Harrow, ON, Canada N0R 1G0
Keywords
Artificial lighting; greenhouse crops; pest
management; plant resistance; primary
metabolites; secondary metabolites;
year-round production.
Correspondence
I. Vänninen, MTT Agrifood Research Finland,
Plant Production Research, Jokioinen 31600,
Finland.
Email: Irene.Vanninen@mtt.fi
Received: 11 March 2010; revised version
accepted: 17 July 2010.
doi:10.1111/j.1744-7348.2010.00438.x
Abstract
This review describes the effects of the current and emerging lighting technologies on plants, and the plant-mediated effects on herbivorous and beneficial
arthropods in high-technology year-round greenhouse production, where light
quality, quantity and photoperiod differ from the natural environment. The
spectrum provided by the current lighting technology, high-pressure sodium
lamp (HPSL), differs considerably from that of solar radiation. The major plantmediated effects on arthropods were predicted to result from (a) extended
photoperiods and lower light integrals, (b) the attenuation of ultraviolet (UV)
wavelengths, particularly UV-B, (c) the high red: far-red (R : FR) ratio and lower
blue : red (B : R) in comparison with solar radiation and (d) the high proportion
of yellow wavelengths during winter months. Of these light factors (a–d) (ceteris
paribus), (a) and (b) were hypothesised to result in increased performance of
herbivores in winter months, whereas the high R : FR ratio decreased herbivore
performance or not affected it, at least when interlights are used. The predictions obtained on the basis of this review are also discussed in relation to the
modifying factors prevailing in these production environments: enriched CO2
levels, high nutrient amounts, optimised irrigation and temperatures optimal
for plants’ needs. Based on the carbon/nitrogen and growth/differentiation
balance theories, these modifying factors tend to produce plants that allocate
most resources to growth at the expense of defensive secondary metabolism
and physicochemical defensive structures. At the end, this review discusses
knowledge gaps and future research prospects, in which light-emitting diodes,
the emerging lighting technology, play an important role by enabling the
targeted manipulation of plant responses to different wavelengths.
Introduction
In greenhouses, it is possible to manipulate light as
well as other environmental factors to improve plant
production and quality (Gruda, 2005). A variety of
desired functional or structural changes in crop plants,
for example increasing photosynthesis, modulating crop
morphogenesis and controlling the timing of physiological events such as induction of flowering, can be
obtained by manipulating light (Moe, 1997). Natural
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daylight quantity and quality can be modified by using
photoselective coverings or by supplemental artificial light
using luminaires. Whereas photoselective coverings are
usually utilised in less sophisticated plastic greenhouses,
artificial light is used mostly in the more technologically
advanced greenhouses that have good control of environmental conditions to optimise plant productivity. This
overcomes the problem of short photoperiods and low
light intensity during winter months, as well as in overcast days in summer, and allows year-round production
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(Moe et al., 2006). Year-round production with artificial
light is mostly used in the greenhouses of boreal and
temperate climatic zones (Scandinavia, Estonia, Russia, Canada) (Dorais, 2003; Moe et al., 2006), but it
is also expanding in countries such as Denmark, the
Netherlands, UK and Germany (Heuvelink et al., 2006).
Herbivorous and predatory arthropods in artificial light
greenhouses in temperate and boreal zones live on host
plants that are provided with high amounts of resources
(light, CO2 , nutrients, water) in an environment characterised by relatively constant, warm temperatures, often
abnormally long photoperiods (depending on the time of
the year and crop), and light spectra that deviate from
that of sunlight. Plants and arthropods that live in this
environment have never encountered such conditions
during their evolution. The light environment created by
a combination of artificial lighting and sunlight, or by the
use of cladding materials that absorb certain wavelengths,
influences arthropods most of the year not only directly
but also via the plants’ physical and biochemical traits.
Because light is central in shaping plant characteristics
(Roberts & Paul, 2006), it is useful to understand how the
greenhouse light environment affects pest herbivores via
the plants and whether such knowledge could be used
for pest management purposes.
This review describes how the biology, behaviour and
ecology of pest and beneficial arthropods are affected by
the light environment created by current supplementary
lighting technologies and regimes, and by the use of
greenhouse covers, the emphasis being on luminairebased lighting conditions. We begin by giving a short
overview of the currently available artificial lighting
sources and cover materials and how they fulfil the
plant’s needs (for a more extensive review on light
quality management in horticulture, see Rajapakse &
Shakak, 2007). Next, we review how arthropods living
on greenhouse plants are affected indirectly by light via
the plant or their arthropod prey or hosts. Finally, we
summarise the identified knowledge gaps and create a
roadmap for future research for pest management in
artificially lighted crops using light as a means to influence
plant quality and characteristics.
Current and emerging artificial lighting technologies
The importance of artificial light for plant photosynthesis
and photomorphogenesis is highest when artificial light
is used as the principal or only light source (Moe, 1997).
In greenhouses of the temperate and boreal zones of the
northern hemisphere, for example in Finland, artificial
light is the dominant source of photons during the winter months from October to February, whereas in the
long days of the northern summer natural daylight is
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supplemented with artificial light only in cloudy days and
in twilight hours (Hovi-Pekkanen & Tahvonen, 2008).
The principal aspects of artificial lighting affecting plant
photosynthesis and growth are the following: (a) light
quality, that is spectral distribution of the emitted or transmitted light with respect to the plants’ needs; (b) light
intensity and light integral (cumulative PPF, or photosynthetic photon flux, density per day) in comparison with
plant requirements and production purposes; (c) duration
of lighting per day (photoperiod) for maximising plant
growth and optimising photomorphogenetic processes
such as flowering and (d) placement of lights either above
or within canopy, or both, to optimise light availability
to all leaves and the plants’ photosynthetic capabilities
and to reduce shade-avoidance responses (Moe, 1997;
Dorais, 2003). In the following, we review the technical
aspects of current and emerging technologies used for
manipulating the light environment inside greenhouses,
with particular attention to the spectral composition that
affects plant metabolic processes.
High-pressure sodium lamps
The light source dominating artificial supplemental illumination at the moment is the high-pressure sodium
lamp (HPSL) (Moe et al., 2006). This lamp type is based
on discharge luminescence, and emits light that is yellow
to the human eye (Tazawa, 1999, for a review of artificial
light sources for plant production). Approximately 40%
of the output photons of HPSLs are in the photosynthetically active radiation (PAR) region (Pinho, 2008), and
most of the PAR photon output is near the peak quantum
yield (the amount of CO2 fixed per absorbed photon) (see
Bugbee, 1994 for illustrations). The energy efficiency is
1.4–1.6 μmol per W for 400 and 600 W lamps, respectively (Dorais, 2003). Early on, the photosynthetic efficacy
of HPSLs was shown to be the highest per unit of power
consumed compared to other lamp types (McCree, 1972).
Using supplemental HPS-lighting in suboptimal daylight
conditions provided significant advantages by enhancing
plant growth, increasing dry biomass and yield, keeping
quality and reducing development time of plants (Demers
& Gosselin, 2002 and references therein; Hovi-Pekkanen
& Tahvonen, 2008).
Some aspects of the spectral distribution of HPSLs can,
however, be problematic for plant metabolic processes.
The spectral distribution of HPSLs differs considerably
from that of solar radiation. The colour-correlated temperature of HPSLs is only 2100 K compared to 6500
K of sunlight (D’Andrade & Forrest, 2004). The emission peaks of standard HPSLs are 51% at 500–600 nm
(yellow-green), 40% at 600–700 nm (red) and only 9%
at 400–500 (blue) (Tazawa, 1999), with the strongest
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peak emission at 569 nm (green-yellow) (Pinho, 2008).
The newer 600 W HPSLs have a higher PAR yield and
even more red light and less blue light compared to
400 W HPSLs (Dorais, 2003). Too long daily photoperiods of blue-deficient lighting disturb stomatal regulation
and cause negative changes in carbohydrate metabolism
and physical symptoms on leaves (Demers & Gosselin,
1999, 2002). This is particularly clear in growth chamber
conditions where HPSLs are not supplemented by natural
daylight (Demers & Gosselin, 2002), a situation essentially
similar to that prevailing in greenhouses during the northern winter months. High-pressure sodium lamps are also
very low in ultraviolet (UV) radiation (<400 nm) (Philips
Lighting Company, 2009). The daily integral of UV light
in the solar radiation reaching latitudes 50–70◦ N ranges
from approximately 5.5–3.7 kJ m−2 in the peak of the
summer down to 0–0.7 kJ m−2 in November–February
(International Arctic Science Committee, 2009). Therefore, in greenhouses of the boreal zone, the availability
of UV wavelengths varies considerably between seasons
(Moe, 1997), being practically nil in the winter when
UV light-deficient HPSLs are the principal light source
during several months. Another difference of the HPSL
spectrum is that the red : far-red (R : FR) ratio can be
as high as 7.1 compared to 1.1 in clear-sky sunlight (for
spectral distribution graphs of solar radiation and HPSLs,
see Cummings et al., 2007).
Besides the spectral unbalance, there are also some
other technical disadvantages of HPSLs that reduce their
utility and economics as artificial light source of plants. No
significant further progress in PAR efficiency is expected
(van Ieperen & Trouwborst, 2008). The operational
temperature of HPSLs is over 200◦ C (van Ieperen &
Trouwborst, 2008), which seriously limits possibilities of
interlighting because of plant damage if lamps are placed
too close to leaves. Control of the radiation quantity
of HPSLs is limited, which reduces the possibility of
pulsed operation, that is intermittent radiation which
is a way to obtain energy savings (Tennessen et al., 1995;
Pinho, 2008). The life span of HPSLs is in the range of
10 000–24 000 h (Pinho, 2008). This is shorter than that
of light-emitting diodes (LEDs), which are of increasing
interest for horticultural lighting.
Light-emitting diodes
Tubular fluorescent lights and, increasingly, LEDs are
used in tissue culture and plant propagation (Fang & Jao,
2000). Light-emitting diodes are also used as the principal
artificial light source in plant factories in Japan (Ono &
Watanabe, 2006). The current status of LEDs in plant
production was recently reviewed by Kim et al. (2005),
Massa et al. (2008), Morrow (2008), Pinho (2008) and
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Greenhouse lighting technologies and plant protection
Yeh & Chung (2009). As individual photoreceptors are
generally tuned to sense specific regions of the spectrum,
narrow-bandwidth light (NBL) produced by LEDs can
be matched to plant photoreceptors for a targeted photosynthetic and/or photomorphogenic response without
wasting energy on nonproductive wavelengths (Massa
et al., 2008; Morrow, 2008). Light-emitting diodes can,
in principle, be configured to produce light levels well in
excess of full sunlight, if desired (Morrow, 2008), they
offer good possibilities for pulsed lighting (Tennessen
et al., 1995), and their life span is 2–10-fold compared to
HPSLs (Morrow, 2008; Pinho, 2008).
The low output of some current LEDs and low electrical
efficiency of approximately 20% (compared to 26–30%
of HPSLs, see Dorais, 2003) are the primary technical
impediments to wider use of LEDs in plant production
at the moment (Morrow, 2008). Recent developments
suggest, however, that the electrical efficiency of LEDs is
improving considerably from the 20% mentioned above,
being now at least 30.5% for white LEDs (Cree Incorporation, 2010) and 40.5% for InGaN-based blue LEDs (Mike
Bourget, Orbital Technologies Corp., Madison, WI, USA,
personal communication). Current LEDs produce more
heat than HPSLs per Watt energy input, but radiated heat
of LEDs is low compared to HPSLs (Hogewoning et al.,
2007) and can be removed from the crop environment by
dissipation via convective cooling systems (van Ieperen
& Trouwborst, 2008). This allows LEDs to be placed
very close to leaves for interlighting purposes without
damage to plants (Massa et al., 2008). The high capital
cost is another important aspect delaying the uptake of
LED technology in horticultural lighting (Pinho, 2008).
Despite this, the technological development of LEDs is
expected to reduce capital and operating costs in the
future (Massa et al., 2008; Morrow, 2008; Pinho, 2008;
Yeh & Chung, 2009).
The technical and operational benefits of LEDs would
be maximised when the exact wavelength combinations
necessary for producing good-quality plants are known
and the daily light integral is minimised (such as with
pulsed operation of LEDs), yet sufficient for production
goals. The effects of blue and red/far red monochromatic
lighting on plant growth and metabolism have been
shown in a multitude of studies, whereas the role of
other wavelengths supplemental to blue and red is less
well known (Massa et al., 2008). The use of NBL and their
combinations for growing tomato, cucumber and lettuce
has been studied by some authors (Okamoto et al., 1997;
Menard et al., 2006; Urbonavičiūtė et al., 2007; Brazaitytė
et al., 2009a,b; Samuolienė et al., 2009; Wang et al., 2009),
and in some cases comparisons have been made with
HPSLs (Pinho, 2008; Brazaitytė et al., 2009a,b).
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Cladding materials
Greenhouse covers change quantitatively or qualitatively
the transmission, reflection and absorption of the solar
radiation when it enters the greenhouse (Kittas & Baille,
1998). Recent developments of plastic films aimed at
manipulating the light environment include UV blocking,
near-infrared (NIR) blocking, fluorescent and ultrathermic films (Espı́ et al., 2006). Such films are principally used
for the benefit of the crop (Hemming-Hoffmann et al.,
2005; Magnani et al., 2008). In northern areas, transmission of the total solar wavelength band (400–2500 nm)
is desirable to maximise heat influx to the greenhouse
during cooler seasons. On the other hand, in the winter low transmission of long-wave radiation (2500–40
000 nm) is desirable to reduce heat loss from the greenhouse (Pearson et al., 1995). For combined plant growth
and energy-saving purposes, the challenge is to develop
cover materials that combine high light transmission and
high insulation values (Bakker, 2008). Examples of such
materials are antireflex glass (Hemming-Hoffmann et al.,
2006), triple layer systems (Bot et al., 2005), Lexan ZigZagTM greenhouse roof (Sonneveld & Swinkels, 2005a) and
micro-V-treated glass (Sonneveld & Swinkels, 2005b).
Incoming light transmission and light quality can also
be modulated by using films containing photoselective
pigments (for a review, see Espı́ et al., 2006). For example,
blue fluorescent film was developed to increase light
transmission as well as to increase the blue range of
the spectrum for transmitted light in northern European
climates (Hemming-Hoffmann et al., 2005).
Plant-mediated effects of light on herbivores and
their natural enemies
Plants monitor the light environment’s total fluence
rate (photons per unit time and area), spectral composition (different wavelengths) and photoperiod with a
series of photoreceptors. These are grouped at least into
three photosystems (PSs): photosynthetic, phytochrome
and cryptochrome, each of which differs with respect
to the types of photosensitive pigments involved, the
wavelengths pigments are sensitive to (Fig. 1) and the
functional tasks they accomplish in plant metabolism
(Sullivan & Deng, 2003) (Table 1). In the photosynthetic PS, chlorophylls and carotenoids are responsible
for light harvesting. The principal photosensory function
of phytochromes is to detect the relative proportions of
red and FR energy in ambient light (Matthews, 2006
and references therein). The photoreceptors of the cryptochrome PS, cryptochromes and phototropins (Sullivan
& Deng, 2003), are in charge of regulating plant responses
to UV-A light (320–390 nm) and blue (390–500 nm).
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I. Vänninen et al.
UV-C < 280
UV-B 280-315
UV-A 315-400
FR 700-800
NIR 800-3000
Photosynthetically Active Radiation
(PAR)
Chls /carotenoids
Chls
Pr and Pfr
250 300 350 400 450 500 550 600 650 700 750 800
Wavelength (nm)
Figure 1 Main photosynthetic and photomorphogenetic photoreceptors
and their action spectra in green plants. The wavelengths between 400
and 700 nm (PAR, photosynthetically active radiation) and those between
700–800 nm (FR, far-red) are useful for photosynthesis, phototropism
and photomorphogenesis (Lambers et al., 2008). The existing lightharvesting antennal pigments are chlorophylls (chls chl-a and chl-b) and
carotenoids (b-carotene, lutein, violoxantin, neoxantin). The two most
important absorption peaks of chls are located in the red (625–675 nm)
and blue (425–475 nm) regions, with additional localised peaks at nearultraviolet (UV) light (300–400 nm) and in the FR region (700–800 nm).
The absorption bands of chls and carotenoids overlap in the blue spectral
region, while only chls absorb in the red region. Phytochromes perceive
red (Pr) and FR (Pfr) light in between 600 and 750 nm (for a review,
see Pinho, 2008; Franklin & Whitelam, 2005). Green light (500–580) is
absorbed by both phytochromes and cryptochromes, but their efficiency
in processing the green light signal is poor.
Cryptochromes also have a green-sensing state (Folta &
Maruchnich, 2007). The existence of a separate UV-B
receptor among plant photoreceptors is also suspected,
because UV-B responses of plants are not triggered by
the known photoreceptors (Chen et al., 2004). Both phytochromes and cryptochromes perceive light intensity,
which modifies the activation state of enzymes involved
in CO2 fixation via PSI and PSII (for a review, see Aphalo
& Ballaré, 1995).
Dynamic acclimation of the photosynthetic apparatus in response to environmental cues, particularly light
quantity and quality, contributes to the tolerance of
plants against stress and helps to maintain optimal photosynthetic efficiency and resource utilisation. Short-term
responses minimise changes due to excess light by rendering some PSIIs nonfunctional, while simultaneously
allowing efficient use of incident irradiance. Long-term
acclimation involves the coordinated reallocation of
resources to achieve and maintain high quantum yields
(amount of fixed CO2 per absorbed photon) under limiting light. It also involves protective strategies under
sustained environmental stress such as high light intensities (for a review, see Anderson et al., 1995). Light
quantity, quality and photoperiod affect herbivores and
natural enemies indirectly via plants in several different
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I. Vänninen et al.
Table 1 Effects of different light wavelengths on plant physiology and morphology because of differential sensitivity of photoreceptorsa
Light Quality
Effects on Plant’s Physiology and Morphology
UV-B 280–300/315/320 nm (putative UV-B
photoreceptor)
The effects can be separated by UV-B dosage. Low doses induce UV-B-specific
photomorphogenetic and developmental responses. High doses result in more general
stress signal transduction.b
UV-A 320–390 nm (cryptochromes, phototropins)
Phototropism, light-induced opening of stomata, chloroplast migration in response to
changes in light intensity and solar tracking by leaves of certain plant species.
Contributes to maximising photosynthetic potential in weak light and preventing
damage to the photosynthetic apparatus in excess light.c
Blue (B) 390–500 nm (cryptochromes, phototropins)
Phototropism, chloroplast relocation, stem elongation (de-etiolation),
photoperiod-dependent flowering induction, resetting the circadian oscillator.d
Maximises photosynthetic potential in weak light and prevents damage to the
photosynthetic apparatus in excess light. Controls stomatal opening at low light levels
(<15 μmol m−2 s−1 )c . Upregulates genes that encode key enzymes in the Calvin cycle.e
Act as a catalytic wavelength for obtaining high quantum yields of photosynthesis and
activates respiration. Strong blue light activates the incorporation of carbon in amino
acids, that is it inhibits starch formation in leaf chloroplasts and increases the
biosynthesis of proteins.f
Green 500–580 nm (cryptochromes, phytochromes)
Tends to temper or negate the effects of blue and red.g Downregulates genes coding for
key enzymes in the Calvin cycle.e In moderate and strong intensities of white light, after
chlorophyll absorbance for red and blue light have become saturated, green light drives
photosynthesis more efficiently than blue or red due to differences in light-absorption
profiles within leaves for blue, red and green light.h
Yellow 580–600 nm (cryptochromes, phytochromes)
Downregulates genes coding for key enzymes in the Calvin cycle.e Suppresses growth of
some greenhouse plants.i
Red (R) 600–700 nm (R-absorbing phytochrome form Pr)
Stem elongation (de-etiolation).j Entrainment of the circadian clock.k Downregulation of
genes encoding for key enzymes in the Calvin cycle.e Activates the photosynthetic
reaction centres PSI and PSII.l In many species, low-fluence red light induces seed
germination.k,m Prolonged exposure to red light eliminates the possibility of the
enhancement of protein biosynthesis by blue light.h
Far-red (FR) 700–800 nm (FR-absorbing phytochrome
form Pfr)
B:R
Often cancels the effects of preceding red light. In many species, inhibits seed
germination.m Stem elongation (de-etiolation).j
Crucial for photosynthetic activity.m
R : FR
Seed germination, seedling establishment, shade-avoidance response, floral induction.d,k
B : R, blue : red ratio; R : FR, red: far-red ratio; UV, ultraviolet.
a Many light responses are mediated by the coordinated action of more than one photoreceptors (Chen et al., 2004).
b
Reviewed and proposed by Brosché & Strid (2003).
c Reviewed by Briggs & Christie (2002).
d Chen et al. (2004).
e
Wang et al. (2009).
f Reviewed by Voskresenskaya (1972).
g Folta & Maruchnich (2007).
h
Terashima et al. (2009).
i Dougher & Bugbee (2001).
j Parks et al. (2001).
k
Sullivan & Deng (2003).
l Bugbee (1994).
m Lambers et al. (2008).
ways mainly through such long-term plant-mediated
effects (Fig. 2). In the following, we review separately
the plant-mediated effects of light quantity, quality and
photoperiod on herbivores and their natural enemies
addressing those aspects that are important to greenhouse
crops illuminated with HPSLs and LED lights.
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Plant-mediated effects of light intensity on
arthropods
Low light intensities stress
synthesis and thus growth,
sities can cause damage to
ratus (Lambers et al., 2008).
plants by limiting photowhereas high light intenthe photosynthesis appaTo give a perspective, the
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Greenhouse lighting technologies and plant protection
Intensity
I. Vänninen et al.
LIGHT
Photoperiod
Wavelength
9
Photosynthesis1,2
C/N ratio1
VOC emission3,4
Trichome density5
Stomatal density6
Leaf toughness1
Secondary metabolites (+/-)1
(extrafloral) Nectar production7
Physico-chemical leaf cuticle
properties8
Flowering
VOC emission10
Leaf injury (tomato)11
Nutrient uptake12
Leaf toughness13
Secondary metabolites23
Photosynthesis14
N content 15
Morphology16,17
Leaf thickness14
Stomatal control14
Phototropism18
VOC emission19
Secondary metabolites20
Quality and quantity of
cuticle wax14
Trichome density16
Growth21
Survival22
Foraging5
Oviposition1
Population
Densities21
Feeding1,21,22
Figure 2 Effects of light intensity, photoperiod and quality (wavelength) on plants and via plants on arthropods. References: 1, Roberts & Paul (2006); 2,
Gruda (2005); 3, Gouinguené & Turlings (2002); 4, Takabayashi et al. (1994); 5, Kennedy (2003); 6, Gay & Hurd (1975); 7, Pacini et al. (2003); 8, Shepherd
et al. (1995); 9, Stack & Drummond (1997); 10, Maeda et al. (2000); 11, Hillman (1956); 12, Mankin & Fynn (1996); 13, Dorais (2003); 14, Teramura &
Sullivan (1994); 15, Lindroth et al. (2000); 16, Jansen (2002); 17, Kakani et al. (2003); 18, Pinho (2008); 19, Kasperbauer & Loughrin (2004); 20, Treutter
(2006); 21, Mazza et al. (1999); 22, Zavala et al. (2001); 23, Kennedy et al. (1981).
instantaneous light intensity of full summer sunlight
ranges from 1600 to 2000 μmol of photons m−2 s−1 .
As a general yardstick, instantaneous intensities less than
200 μmol m−2 s−1 can be considered low (Bugbee, 1994).
When considering ‘low’ and ‘high’ light intensities, it
should be borne in mind that the amount of photons
causing saturation of the photosynthetic apparatus and
determining the compensation point (where carbon fixation equals its release because of photorespiration) differs,
depending on whether the plant is a sun or a shade species
(see Anderson et al., 1995).
Daily plant growth is closely related to the dailyintegrated PPF (mol m−2 day−1 ), and attempts have
been made to rank greenhouse crop species based on
their daily-integrated PPF levels required for optimal
growth (Moe, 1997). At the lower end of instantaneous PAR levels, the photoperiod can be extended to
achieve high enough daily-integrated PPF. Instantaneous
PAR levels of 800 μmol m−2 s−1 are adequate to simulate field daily-integrated PPF levels for both short-day
and long-day plants (Bugbee, 1994). Usual instantaneous
PAR intensities of artificial light used in commercial
greenhouse production in Scandinavia range from 150
to 300 μmol m−2 s−1 PAR, depending on the crop
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species (Moe et al., 2006). The daily-integrated PPF levels
produced by the combination of solar radiation and supplemental artificial light vary considerably between seasons in the temperate and boreal zone greenhouses. For
example in southern Finland (60◦ 23 N), the average total
(natural + artificial) integrated light intensity (PPF) measured in top-canopy lit cucumber crops was 19, 30 and
39 mol m−2 day−1 in winter, spring and summer, respectively. Of these values, 88%, 47% and 29% was artificial
light. There was thus a twofold difference in the amount
of light received by plants between summer and winter, despite the use of artificial light. Measurements over
several years in the same location and with 190 W m−2
artificial light from HPSLs showed that the average weekly
amount of total light energy (solar radiation + artificial light) was 13.3–17.1 MJ m−2 during June–August,
depending on whether the months were sunny or
cloudy, but only 4.7 MJ m−2 in November–February
(Timo Kaukoranta, MTT Agrifood Research Finland, personal communication). This means that there was a
2.8–3.6-fold difference in the amount of light energy
available to the plants between summer and winter.
Physicochemical characteristics of plant surfaces, which
are affected by light, play an important role in
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I. Vänninen et al.
plant–arthropod interactions (Schoonhoven et al., 2006).
For example, plant surfaces can differently influence the
attachment of parasitoids and predators (Schoonhoven
et al., 2006). Increase in leaf toughness (for a review,
see Roberts & Paul, 2006) may affect feeding and, consequently, the growth of herbivore arthropods and their
natural enemies, as well as parasitism rates in species that
oviposit on/in hosts located below the plant epidermis
(Moon et al., 2000). The most documented effects of light
intensity on physicochemical characteristics of plant surfaces refer to trichome density (Nihoul, 1993). Trichomes
can act as an important resistance trait by hindering
arthropod movement, altering feeding behaviour, secreting chemical compounds with repellent, deterrent or toxic
activity as well as glue substances that can entrap arthropods (Schoonhoven et al., 2006). In Lycopersicon species,
glandular trichomes act as an effective resistance trait
against several arthropods including whiteflies, aphids,
lepidopterans, leafminers and spider mites (for a review,
see Nihoul, 1993; Wilkens et al., 1996; Kennedy, 2003;
Simmons & Gurr, 2005). High trichome densities can
negatively affect the performance of natural enemies (for
reviews, see Kennedy, 2003; Simmons & Gurr, 2005).
Light intensity influences glandular trichome density in
tomato resulting in increased entrapment of the predatory
mite Phytoseiulus persimilis (Nihoul, 1993). In cucumber,
high trichome density can hinder the movement of Encarsia formosa (Schoonhoven et al., 2006). Trichome densities
can also be influenced by light quality resulting from
shading (Liakoura et al., 1997).
Light quantity can alter the chemical constitution of the
plant by altering both primary and secondary metabolism
(for a review, see Downum, 1992; Roberts & Paul, 2006).
Of the three most important plant secondary metabolites, terpenoids and phenolics are carbon based, whereas
alkaloids are nitrogen based (Croteau et al., 2008). Plant
defensive chemicals are a subset of secondary metabolites, which also include substances with roles in plant
response to heat, drought and UV light (Theis & Lerdau,
2003; Wink, 2003; Stamp, 2004). Light interacts with
the availability of nutrients and water to produce phenotypic variation in allocation of plant resources to growth
(primary metabolism) and differentiation such as secondary metabolites in response to changing resource
availability [see Herms & Mattson (1992) for a review of
the growth-differentiation balance hypothesis (GDBH),
which predicts that plant defence is premised upon a
physiological trade-off between growth and differentiation processes]. Allocation to differentiation, including
secondary metabolites and physicochemical defences,
includes cost of enzyme production, transport and storage
structures involved in defence. Differentiation products
are involved in the interaction of plants with their
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environment. As such they are inducible by biotic or
abiotic elicitation such as UV light or herbivores (see
Sudha & Ravishankar, 2002). According to Stamp (2004),
it is difficult to test GDBH directly (i.e. experimentally),
in particular regarding the consequences of resource gradients to plant defence. Recently, however, Le Bot et al.
(2009) attempted partial testing of the hypothesis for
agronomically relevant nutrient resource conditions in
combination with modelling to overcome such difficulties using tomato as the model crop. The results of Le
Bot et al. (2009) illustrate the difficulty of inferring the
rate of secondary metabolism from the concentration of
secondary metabolites in plants in relation to nutrient
resources. They also point to the lack of our knowledge
of which carbon resources should be integrated in the
carbon pool that serves as the source of carbon-based
secondary metabolites in plants.
Products of altered primary metabolism that participate
in nutrition and essential metabolic processes inside the
plant can have a role also in plant defence (Schwachtje
& Baldwin, 2008). Plant primary metabolites (sugars and
amino acids) can act as feeding stimulants for insects
(Schoonhoven et al., 2006). In natural environments,
nitrogen concentration is high in leaves in high light
intensities (Roberts & Paul, 2006). Therefore, high light
intensity can indicate a high-quality food source for some
insects. The common hypothesis is, however, that full
sunlight will suppress herbivory, as leaf material from
shade leaves is more suitable for herbivores (Roberts
& Paul, 2006) because of decreased concentrations of
carbon-based secondary metabolites. The effect of shading on plant suitability to herbivores is associated with
reduced R : FR ratio (PSI light) compared to full sunlight and subsequent decrease in defensive substances in
shaded plants. Such allocation to growth (to avoid competition by neighbouring plants) at the expense of defensive
substances is called the shade-avoidance response or syndrome (Franklin & Whitelam, 2005). It is inducible even
by exposing plants to laterally given FR light in the
absence of actual competitors. This has been shown, for
example, in tomato (Jansen & Stamp, 1997), tobacco
(Izaguirre et al., 2006) and Arabidopsis (Moreno et al.,
2009), where the performance of caterpillars increased in
FR-treated or physically shaded plants. In all these cases,
increased herbivory of shaded leaves was associated either
with smaller concentration of defensive allelochemicals,
downregulation of chemical defences or strong reduction
of plant sensitivity to jasmonates, the key regulators of
plant immunity to biotic aggressors. In two cucumber
types lacking the defence chemical cucurbitacin and one
of them expressing constitutively the shade-avoidance
response, the latter had 93% more herbivory by specialist
beetles compared with wild types, apparently because of
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Greenhouse lighting technologies and plant protection
lower number of trichomes (McGuire & Agrawal, 2005).
Thrips also have been shown to prefer a tomato mutant
that lacks functional phytochrome B (the photoreceptor that mediates red and FR responses), and, therefore,
has the phenotype of an FR-exposed (i.e. shaded) plant
even when grown in full sunlight (Izaguirre et al., 2006).
It must be noted, however, that the shade-avoidance
response is not evoked only by the R : FR ratio, which
is sensed by phytochromes, but, depending on conditions
and plant species, involves multiple signals and photosensory systems, including blue light signals coming
from the gaps between neighbouring plants. Elimination or attenuation of such blue light signals attenuates
the shade-avoidance response of projecting new growth
towards canopy gaps. Furthermore, some aspects of the
shade-avoidance phenotype, such as promotion of elongation, can be induced by lowering the UV-B component
(reviewed by Ballaré, 1999).
In tomato, light intensity and photoperiod correlate positively with the concentrations of phenolics and
methyl ketone 2-tridecanone, which increases mortality
of Manduca sexta caterpillars (for a review, see Kennedy,
2003). While elevated concentrations of phenolics have
been suggested as a possible insect growth inhibitor,
2-tridecanone has a toxic effect against several herbivores
(Kennedy, 2003). Wilkens et al. (1996) showed that in
high light intensity (30% of shading inside a greenhouse)
tomato plants produced more soluble phenolics (in percentage of dry mass) than in low light intensity (73% of
shading) at both low and high levels of nitrogen fertilisation. Interestingly, low nitrogen availability did not inhibit
allocation to soluble phenolics in high light. Wilkens et al.
(1996) speculated that this may have been because in
the high light treatment plants were exposed to UV light,
and therefore needed to produce phenolic substances to
protect cells from being damaged by increased UV light.
The change in the amount of secondary metabolites with
respect to light availability may also depend on their type
(Wilkens et al., 1996). Some glucosinolates, for instance,
decrease in the presence of light (Bennett et al., 1997).
Indirect defences, which allow the plant to offer food
or shelter to predators and parasitoids that in return control herbivores (Heil, 2008), include the constitutive and
induced secretion of extrafloral nectar, the production of
cellular food bodies and (acaro-) domatia as well as the
induced emission of volatile organic compounds (VOCs)
(for a review on indirect defences, see Heil, 2008). Some
of these defences can be costly for the plant, and therefore
limited by resources such as light (Heil, 2008). The major
evidence from the effect of light on indirect defences
comes from studies conducted on the inducible emission
of VOCs and the orientation of predators. Reduced
light (because of either lower light intensity or shorter
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I. Vänninen et al.
daylength) leads to a decrease in the emission of inducible
VOCs (Takabayashi et al., 1994; Gouinguené & Turlings,
2002), and so does the absence of light (Maeda et al.,
2000). This in turn can affect negatively the orientation
of predatory mites (Takabayashi et al., 1994; Maeda et al.,
2000). Reduced amounts of terpenoid VOCs in transgenic tomato plants (although not associated with light
levels in this case) have been shown to increase considerably the attractiveness of plants as the egg-laying host of
Bemisia tabaci, although development times and mortality
of nymphs were not affected (Sánchez-Hernández et al.,
2006). The authors proposed that the insects responded
to the decreased emission of VOCs, which indicates lower
attraction of natural enemies to the plants.
Plant-mediated effects of photoperiod
on herbivores
Photoperiod is well known as a factor regulating initiation
of flowering in plants, but it also influences VOC emission, levels of leaf injury (in tomato), nutrient uptake
and leaf toughness. Photoperiods used to grow long-day
or daylength neutral plants, such as tomato and cucumber
in artificially lighted greenhouses, are usually between 16
and 22 h, and some plant species such as roses and lettuce tolerate continuous 24-h lighting (Dorais, 2003; Moe
et al., 2006). The longest photoperiods are out of the natural range of most plants, herbivores and natural enemies
living in greenhouses. The major vegetable crops tomato,
cucumber, sweet pepper and lettuce are day-neutral
plants, that is they do not require a critical daylength to
initiate flowering (Danielson, 1944; Hillman, 1956). Their
growth processes, particularly those of tomato, however,
respond to daylength, as do morphological features such
as leaf thickness in cucumber (Dorais et al., 1996). In
tomato, too long daylengths induce leaf chlorosis (Hillman, 1956; Demers et al., 1998) because of accumulation
of starch and sugar in leaves (Demers et al., 1998),
whereas in cucumber leaf chlorosis seen in continuous
light is not associated with starch accumulation (Wolff
& Langerud, 2006). In long day, total soluble sugars,
polysaccharides and carbohydrates increase in cucumber
leaves (Danielson, 1944). Whether such changes in primary metabolism are conducive or inhibitive to herbivore
performance has not, to our knowledge, been studied. In
roots of cucumber grown in long photoperiod (14 L : 10
D) as compared to short photoperiod (10 L : 14 D), the
number of organic acids and their exudation rates were
higher, even to such extent that these compounds were
autotoxic to cucumber (Pramanik et al., 2000).
Strawberry (Fragaria × ananassa Duch.) grown in short
or long daylength shows dissimilar patterns of resistance
to herbivory. Strawberry plants that were first grown
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in short daylength and were susceptible to Tetranychus
urticae increased their resistance when transferred to long
daylength and vice versa (Patterson et al., 1994). It was
concluded that the increased amount of light received by
plants in long days resulted in the production of defence
compounds such as phenolics in the plant leaves. In
tomato Lycopersicon hirsutum, long daylength with both
low and high light intensities (produced by cool fluorescent daylight tubes and incandescent bulbs) induced
production of greater amounts of tridecanone, which
is toxic to the Lepidopteran M. sexta larvae (Kennedy
et al., 1981). On the other hand, mortality of the potato
tuber moth (Phthorimaea operculella) on tomato plants
(L. hirsutum × Lycopersicon esculentum) was not related to
the daylength (Gurr & McGrath, 2001). Resistance of
tomato against P. operculella is considered to be trichome
based and associated with 2-tridecanone; however, the
density of different trichome types has varying effects on
biological and behavioural parameters of the pest (Simmons et al., 2006). In fact, trichomes appear to have a
higher impact on the moth’s parasitoids than on the moth
itself (Mulatu et al., 2006), thus the effect of daylength
on P. operculella in tomato might be revealed only when
studying tritrophic interactions.
Plant-mediated effects of light quality on herbivores
The spectral distribution of light plays a crucial role for
various plant processes because of differential sensitivity of photoreceptors to different wavelengths (Table 1).
Light quality has a multitude of effects on plants. Here,
we concentrate on two aspects of spectral composition
that can have effects on herbivores via the plant: the
presence/absence of UV wavelengths in the spectrum,
and the effects of monochromatic light on plants and,
subsequently, on arthropods. The latter are of interest
because LEDs can be used to tailor the spectral composition according to plant needs.
Ultraviolet wavelengths
Light environment produced by HPSLs is practically
devoid of UV light in winter months in the northern
latitudes, and even in the summer the availability of
UV wavelengths inside greenhouses can be lower than
outdoors, depending on the cladding material. Filtering
out UV wavelengths from the incoming radiation can
disrupt insect orientation (Antignus, 2000), but UV light
also influences plant biology and may offer possibilities of
manipulating herbivores indirectly as suggested by Paul
& Gwynn-Jones (2003).
Studies prompted by the concern of ozone depletion provide insight to plant effects of UV-B light. Plant
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responses to UV-B radiation have been assessed at the
morphological (Krizek et al., 1997; Jansen, 2002; Shinkle
et al., 2004), physiological (for a review, see Teramura
& Sullivan, 1994) and lately at the molecular level
(Ulm & Nagy, 2005 and references therein). Effects on
plants’ primary and secondary metabolism have also
been investigated (for a review, see Kakani et al., 2003).
Enhanced UV-B light can lead to changes in the quality and quantity of epicuticular waxes and increases in
leaf thickness and trichome densities (for a review, see
Teramura & Sullivan, 1994). It can alter N content as well
as available carbohydrates (large soluble carbohydrates
and starch) and fibre content (hemicelluloses, cellulose
and lignin) (Lindroth et al., 2000 and references therein),
reduce stomatal conductance, resulting in changed photosynthetic activity (Kakani et al., 2003), and activate
phototoxins (Downum, 1992). The effect of UV-B light
on plants is mediated by light intensity as shown by bean
plants grown under high, medium and low light conditions: upon prolonged UV-B light exposure, plants grown
in high PAR intensity (700 μmol m−2 s−1 ) were the most
resistant to UV-B radiation (Cen & Bornman, 1990). Blue
light and UV-A (315–400 nm) radiation can mitigate
UV-B radiation damage in plants by the induction of protective countermeasures, such as photolyase-mediated
repair processes of the pyrimidine dimers (Britt, 1996).
The effects of UV-B radiation on higher plants are
usually perceived as negative, but some effects are nondamaging or positive, depending on the perspective and
other environmental factors that play a role in plant biology (Holmes, 2006). Plants exposed to ambient solar UV-B
light often show an increased resistance to herbivorous
insects compared with control plants grown under UV-B
radiation filters (Ballaré et al., 1996). This phenomenon
corresponds with a significant overlap in gene expression
between the UV-B light and the wounding/herbivory
response (Stratmann, 2003). Recent studies have begun
to elucidate the signalling pathways and gene expression
induced by UV-B radiation (Ulm & Nagy, 2005 and references therein). UV-B radiation stimulates the production
of reactive oxygen species (ROS), which act as signalling
molecules that trigger plant responses to different abiotic
and biotic stresses, and the induction of genes involved
in plant defence responses (for a review, see Rozema
et al., 1997; Ulm & Nagy, 2005). One of the most common responses of plants to enhanced UV-B light is the
accumulation of UV-screening phenolic metabolites, such
as flavonoids and related phenolic compounds (Paul &
Gwynn-Jones, 2003; Lambers et al., 2008, pp. 237–239).
These substances act as a defensive mechanism against
UV radiation damage, but also as important antifeedants,
digestibility reducers or toxins against insects (Treutter,
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Greenhouse lighting technologies and plant protection
2006). They can act as attractants for adapted species as
well (Treutter, 2006).
Among the major greenhouse crops, tomato shows
intermediate sensitivity to UV-B radiation (Rozema et al.,
1997). For example, tomato plants grown under films
transmitting ambient UV light have increased the contents of phenolic acids, compared with those grown under
films that block UV radiation (Luthria et al., 2006). To our
knowledge, there are no studies correlating the UV-B
irradiation response to herbivore response on tomato.
Cucumber is more sensitive to UV-B light effects than
tomato, and also shows intraspecific differences in UV-B
light sensitivity. Therefore, it has been used as a model
plant to study UV-B light effects (Krizek et al., 1997 and
references therein). In cucumber, wavelengths of 280
and 290 nm cause visible damage symptoms in cotyledons, depending on the exposure time (Kondo, 1994).
Furthermore, the exposure to UV-B radiation increases
flavonoid and phenolic content of leaves (Adamse & Britz,
1992; Kondo & Kawashima, 2000), decreases the content
of protein, organic acids and total sugars in cotyledons
(Takeuchi et al., 1989), induces morphological changes
in sharp-headed trichomes of leaves and increases lignin
content and accumulation of phenolic compounds in
the trichomes (Yamasaki et al., 2007). Whether such
responses are reflected in insect resistance levels is not
known. Decreased disease resistance has been observed,
however, as cucumber cotyledons predisposed to UVB radiation were more susceptible to pathogens than
plants having not been exposed to such radiation (Orth
et al., 1990).
Ultraviolet-B light-induced changes in plant chemistry are not necessarily mirrored in the behavioural
responses of herbivorous insects, although for some
plant–herbivore combinations plant responses to UV-B
radiation may indirectly affect arthropod performance,
oviposition and feeding behaviour, and intraplant distribution (Zavala et al., 2001 and references therein).
Ultraviolet-B light does not induce all secondary chemicals that are considered important in plant defence against
herbivores (Kuhlmann & Müller, 2009a). Furthermore,
UV-B light induces, for example, phenolics that are
not induced by herbivory (Izaguirre et al., 2007). Plant
responses can be dependent not only on plant species and
specific metabolites but also on plant growth stage and leaf
age (Tegelberg et al., 2004), type of herbivory and length
of UV-B light pretreatment periods of seedlings, as shown
in Broccoli for phloem-content and cell-content feeders
(Kuhlmann & Müller, 2009b). For the cabbage whitefly
Aleyrodes proletella, the key environmental cue influencing
their behaviour was concluded to be the direct effects of
the radiation composition, rather than plant quality itself
(Kuhlmann & Müller, 2009b).
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I. Vänninen et al.
Narrow-bandwidth lighting
Available studies on the effect of specific wavelengths on
plants show that the photosynthesis, photomorphogenesis, germination, flowering, accumulation of biomass
and the phytochemical composition of crops can be
controlled and optimised by utilising supplemental lighting provided by LEDs (reviewed by Massa et al., 2008;
Pinho, 2008, Yeh & Chung, 2009). Higher photosynthetic pigment content and photosynthetic activity of
LED-illuminated plants have been observed in some, but
not all, experiments (for reviews, see Massa et al., 2008;
Pinho, 2008); the effect depends also greatly on which
wavelengths are used (Wang et al., 2009). The use of
specific wavelengths can result in altered relative contents of sugar types in leaves (Pinho 2008; Brazaitytė
et al., 2009a; Urbonavičiūtė et al., 2009), changes in the
activity of nitrate reductase and, consequently, nitrate
contents of leaves (Pinho, 2008), and increased greenness
(amount of chlorophyll) of fruits (Lin & Jolliffe, 1996).
Such changes may also have importance for herbivory,
as primary metabolites affect the nutritive value of the
plant material for insects (Schoonhoven et al., 2006), and
induced changes in primary metabolism could themselves
be defensive (Schwachtje & Baldwin, 2008).
Studies in Lithuania have looked at the effects of
blue, red and far red LEDs in combination with supplemental UV-A, green, yellow and orange wavelengths.
Yellow (596 nm) decreased cucumber transplant development and growth (Brazaitytė et al., 2009a), and tomatoes receiving yellow (596 nm) or orange (622 nm)
during transplant stage had lower yield in the greenhouse (Brazaitytė et al., 2009b). In the study of Wang
et al. (2009), monochromatic green (522.5 nm), yellow
(594.4 nm) and red (628.6 nm) affected all measured
photosynthetic parameters of young cucumber plants
negatively in comparison with white light, whereas
purple and blue had positive impacts. Based on gene
expression studies, the authors concluded that purple and
blue light upregulate most of the genes that encode key
enzymes in the Calvin cycle, whereas green, yellow and
red downregulate them. In lettuce, adding supplemental
yellow (594 nm) to the light spectrum consisting of natural daylight and supplemental monochromatic blue and
red components increased the number of leaves (Pinho,
2008), whereas Dougher & Bugbee (2001) traced the
suppressed growth of lettuce plants under HPSLs as compared to metal halide lamps to the negative effect of
yellow (580–600 nm). The discrepancies concerning the
effect of green and yellow wavelengths on plant growth
are an example of how the effects of certain monochromatic light treatments on photosynthetic processes are
only being revealed, whereas the mechanisms behind the
effects are less well known.
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Other changes attributed to the effects of NBL concern antioxidant activity, phenolics, vitamins, flavonoids,
anthocyanins, tannins, and other secondary metabolite
contents that either increase or decrease depending on
the wavelength selection, ratio of different wavelengths
such as UV-B, blue, yellow and R : FR (see Tegelberg
et al., 2004; Wu et al., 2007; Urbonavičiūtė et al., 2009).
The role of such NBL-induced changes for herbivores and
their natural enemies has not been studied so far. The first
challenge is in designing an optimum plant lighting system with wavelengths essential for specific crops (Massa
et al., 2008). Once this problem has been solved and plant
composition can be reliably influenced by the spectral
composition of artificial light sources, the consequences
of NBL-induced secondary metabolites for herbivory are
easier to investigate. The study by Hong et al. (2009)
shows one way of advancing such understanding. The
authors engineered a transgenic Artemisia annua to overexpress the blue light photoreceptor cryptochrome 1
obtained from Arabidopsis. As a result, the engineered
plants increased the production of a valuable antimicrobial secondary metabolite, artemisin, by 30–40%.
Light also affects the synthesis and emission of VOCs
by plants (Peñuelas & Llusià, 2001) and light quality
seems to contribute to determining the VOC profile as
shown in VOCs emitted by cotton plants grown over
different colour mulches of polyethylene (Kasperbauer &
Loughrin, 2004). Plants that received mulch-reflected
light with reduced R : FR ratio in comparison with
ambient sunlight emitted more insect-attracting volatile
monoterpenoids. The quantity and composition of the
plant VOC blends are important for host location of
herbivores as well as for host/prey location of natural
enemies (Schoonhoven et al., 2006).
Discussion, knowledge gaps and future research
perspectives
We have reviewed how light intensity and light integral,
spectral composition and photoperiod influence plant
morphology and biochemical composition in ways that
may have importance for herbivores and beneficial
arthropods. These effects are summarised in Table 2 by
addressing separately the selected light components that
prevail in greenhouse crops illuminated with HPSLs.
We saw that light intensity and light spectrum differ
considerably between the mid-summer and mid-winter
conditions of the HPSL-illuminated greenhouses at high
latitudes. Our main prediction from the review is that
the plant quality of winter crops is better for herbivores
than that of summer crops because of the lighting
conditions (ceteris paribus). We predict that two important
factors in the HPSL-based winter light environment make
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plants more susceptible to pests than in the summer:
(a) lower light integrals than in the summer, despite
equally extended photoperiods, and (b) the attenuation
or complete lack of UV wavelengths, particularly UV-B.
These factors are predicted to reduce the production
of plant secondary metabolites and physicochemical
defences such as trichomes and leaf toughness in winter
compared to summer crops. Observations by de Kogel
et al. (1997) strongly support the prediction concerning
differences in plant resistance to herbivores in winter and
summer. They grew two chrysanthemum cultivars in the
greenhouse for 1.5 years, with daylength extended to 14 h
in winter time using artificial light (luminaire type and
light intensity not specified). In these conditions, thrips
damage capacity and reproduction were both increased
in winter months compared to summer. Differences in
resistance between the two cultivars became evident only
in reduced light conditions in winter or under shade in
summer. Therefore, the prediction we made above must
be modified by taking into account plant cultivar and
species. In actual greenhouses, the ceteris paribus principle
is further relaxed by the fact that greenhouse temperature
and its daily dynamics necessarily change to some extent
depending on the time of the year. The combination
of temperature and light conditions affects the amount
of water and nutrients given to the greenhouse-grown
plants, as well as the growth and population dynamics
of herbivores and their natural enemies directly. Despite
this, our hypothesis is that if leaves of winter-grown
and summer-grown plants were to be removed and kept
in standardised light and temperature conditions in a
common environment, for example a growth chamber,
the herbivores will show better performance when
feeding on leaves of winter-grown plants. This is partly
because of the effects of winter light environment that the
plants were exposed to in the greenhouse before bringing
them or their leaves to standardised conditions.
On the other hand, the use of interlights in the HPSLbased light environment is predicted not to reduce the
production of defensive compounds or structures, as
interlights retain a higher R : FR ratio within the canopy,
which can be considered to alleviate the induction of
shade-avoidance responses in plants. This is not to say
that the increased R : FR ratio necessarily increases the
production of defence compounds, although red-biased
light sources increase leaf carbohydrate levels in comparison with plants grown in a wider light spectrum
(Britz & Sager, 1990). The predicted reduction of the
shade-avoidance response because of reduced FR and
increased red is taking place in a light environment that
is deficient in blue wavelengths. In some plants, reduced
blue or the absence of blue light also results in plant phenotypes displaying shade-avoidance responses (Britz &
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Greenhouse lighting technologies and plant protection
I. Vänninen et al.
Table 2 Predictions for plant-mediated effects of artificial light based on high-pressure sodium lamps (HPSLs) in year-round greenhouse cropsa
Characteristics of Artificial Lighting
Predicted Effect on Plant Secondary Metabolismb
Predicted Plant-Mediated effect on Herbivores
Extended photoperiods
More potent or more allelochemicals and
physicochemical defences with increasing light
intensity, light integral or long photoperiods.
Increased VOC production.
Depending on the plant species, plants may be less
palatable to herbivores in extended daylengths or
continuous light.
Lower daily light integrals in winter
Less photostress to plants in winter, therefore lower
levels of secondary metabolites and less
physicochemical defences such as trichomes and
leaf toughness.
Plants may be more palatable to herbivores in winter.
Decreased induction of VOCs may interfere with the
orientation of natural enemies in winter.
Attenuated/absent
UV-B
Less photostress by short wavelengths, therefore
less protective compounds such as phenolics.
Plants are more palatable to herbivores particularly in
winter. Effect may depend on the feeding habit (sap
feeding versus tissue feeding) and host range of the
herbivores and is modulated by CO2 concentration.
Higher red and R : FR ratio than in
solar radiation
Red-biased light sources increase leaf carbohydrate
levels (Britz & Sager, 1990 and references therein),
and red light is more conducive to production of
secondary metabolites than, for example, blue.
With interlights, less cues of self-shading and
mutual shading because of higher R : FR ratio;
therefore, investment to defence is less limited by
shade-avoidance responses than in top-lit
canopies.
With interlights, plants are less palatable to
herbivores in comparison with plants grown
without artificial light or plants grown with only
top-canopy lights.
Attenuated blue
Complex inter-relationships are likely between the
effect of blue-deficient light on carbohydrate
formation (Voskresenskaya, 1972) and
shade-avoidance response in plants (Britz & Sager,
1990; Ballaré, 1999) . Whether these phenomena
and their inter-relationship result in altered
allocation to secondary metabolites is not known.
No evidence is available on the effect of depleted or
supplemented blue light on plant-mediated
arthropod performance.
High yellow
Yellow portion of HPSL suppresses growth of some
greenhouse plants that may indicate allocation to
defence in a species-dependent manner (Loughrin
& Kasperbauer, 2001).
No evidence available on whether potential defence
compounds induced by yellow light have an effect
on herbivores or the third trophic level.
LED, light-emitting diode; R : FR, red: far-red ratio; UV, ultraviolet; VOC, volatile organic compound.
a The predictions are for individual light-related factors. The relative strength of the predicted effects must be considered with respect to the modulating
factors of enhanced CO2 , high amount of nutrients and water as well as the temperature, which is adjusted to the plants’ needs and light and CO2 levels.
The combined effect of the individual light-related factors is less easy to predict and deserves investigation. The predictions concerning effects of specific
wavelengths and their combinations can be extended to light environments created by narrow-bandwidth LED lights.
b Based on the reviewed literature.
Sager, 1990). Whether the effects of reduced FR, increased
red and reduced/deficient blue on plant metabolism
are similar in terms of plant defence is not known. At
the same time, the effects of reduced/deficient blue on
carbohydrate formation in plants must be considered
(Voskresenskaya, 1972). A fourth prominent characteristic of HPSLs, a high proportion of yellow light, may also
have a role to play in plant secondary metabolism, but
at the moment little evidence is available to support such
prediction (Table 2).
To our knowledge, little has been done to assess the differences between summer and winter crops grown with
artificial light in terms of their suitability to herbivores.
404
In what follows, we consider the effects of the four
HPSL-related light factors in isolation of other factors
affecting plants in the greenhouse to see what evidence
is available to support our predictions (Table 2).
Extended photoperiods and plant-mediated effects on
herbivores and beneficial arthropods
Extended photoperiods – either alone or in combination with the accumulated daily light integral – may
result in photostress and concomitant changes in plant
biochemistry and physicochemical characteristics. The
relative effect of the photoperiod alone and daily light
integral is likely dependent on plant species and the
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I. Vänninen et al.
plant characteristic in question. There are observations
from more southern areas that greenhouse-grown plants
are less resistant to pests in winter than in summer,
a response that may involve daylength as a contributing factor. According to Kennedy et al. (1981), tomato
plants grown in the greenhouse under natural light from
November through February were less resistant to M.
sexta caterpillars than were the plants grown from April
through June. In identical experiments conducted in June
and January, larvae that were fed excised foliage from
a single vegetatively propagated, highly resistant tomato
(accession) suffered an average mortality of 87% in the
summer, but in the winter the mortality was only 8%
(Kennedy et al., 1981). The role of light intensity, photoperiod or amount of UV light for this difference was not
discussed, but the daylength must have been shorter and
light levels lower in winter than in summer as only natural daylight was available for plants during their growth.
The quantity and quality of physicochemical defences
in artificial light greenhouse crops at high latitudes have
not been studied so far. There might be differences in the
density and allelochemical potential of trichomes between
winter and summer crops of, for example, cucumber,
which is grown in four to five successive crop cycles during the year. It can be predicted also that the production
of VOCs would decrease in winter months compared to
summer. An undamaged plant maintains a baseline level
of volatile metabolites that are released from the surface of the leaf and/or from accumulated storage sites in
the leaf, and the baseline levels are decreased by reduced
light (Paré & Tumlinson, 1999). On the other hand, young
leaves tend to contain higher amounts of VOCs than older
leaves (Takabayashi et al., 1994). Because young leaves
in the top of the plants are closer to the artificial light
sources and thus exposed to the highest amount of light
in all seasons, the suggested difference in VOC production between summer and winter crops may not be of the
same degree in all plant parts.
Depleted UV-B light and plant-mediated effects on
herbivores and beneficial arthropods
From tritrophic model systems composed of a plant,
a herbivore and a parasitoid, we can predict some
consequences of UV light-depleted environments in
greenhouses in winter. In a UV light-depleted treatment,
one herbivore (Plutella xylostella) laid significantly more
eggs, the larvae consumed more leaf area and gained
significantly higher pupal weight. On the other hand,
female parasitoids (Cotesia plutellae) chose significantly
more often plants from UV light-supplemented treatment
(Foggo et al., 2007). In another model system, there were
neither effects on performance or feeding of another
Ann Appl Biol 157 (2010) 393–414 © 2010 The Authors
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Greenhouse lighting technologies and plant protection
herbivore (Spodoptera frugiperda) nor on parasitoid (Cotesia
marginiventris) orientation. In this latter case, the
herbivore was a generalist, however, which may be more
tolerant to differences in host plant chemistry and thus
not affected by the chemical changes caused by UV light
treatment (Winter & Rostás, 2008). These results suggest
that in a UV light-depleted environment (a) herbivores
would benefit or parasitoids may be adversely affected
by plant effects or (b) neither herbivores nor parasitoids
would be affected. The attraction of parasitoids to UV-B
light-treated plants could be explained by the fact that
UV-B light treatment upregulated oxylipin biosynthesis
genes, involved also in jasmonic acid production, similarly
as induced by insect damage in Nicotiana attenua (Izaguirre
et al., 2007). The upregulation of the above-mentioned
genes could lead to an increased emission of parasitoidattracting volatiles from UV-B light-treated plants. In
sweet basil (Ocimum basilicum), an increase in constitutive
VOCs was observed in the essential oils of UV-B lighttreated plants (Johnson et al., 1999). In some other plants,
however, induced VOC emissions as a consequence of UV
light treatment were not observed (Winter & Rostás,
2008). Thus, the indirect consequences of UV light
depletion of the light spectrum for higher trophic levels
may be species specific.
Thrips have been shown to favour UV light-depleted
environments because of both direct negative effects
of UV light on the insects and plant-mediated effects
(Mazza et al., 1999; Kuhlmann & Müller, 2009b). Variations in UV-B light exposure under natural conditions
have also been shown to cause significant behavioural
effects on insects by altering plant chemical traits that
adult female insects use as cues during host selection for
oviposition (Caputo et al., 2006). Previously, high phenolic concentration in peppermint leaves was found to
decrease the number of eggs laid by T. urticae and lengthen
its developmental time (Larson & Berry, 1984). If phenolic concentrations of greenhouse plants are reduced by
depleted UV-B light, the UV light-deficient conditions in
the winter would enhance population development of
T. urticae compared to summer conditions, assuming that
the phenolics in question will affect also the herbivore.
If it will be shown that the attenuation of UV wavelengths in winter months indeed results in decreased pest
resistance in plants, this would suggest the possibility of
influencing plant chemical composition by supplemental
UV light with the aim of reducing pest performance.
The suggested approach employing supplemented
UV-B light, however, has several challenges, that is
finding right combination of dosages and exposure
times that would not reduce crop yield and overall
plant quality, and that do not have adverse effects on
human health. Furthermore, screening for the right
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Greenhouse lighting technologies and plant protection
defensive metabolites as well as species specificity of
plant–arthropod interactions should also be considered.
First, as previously explained, not all compounds induced
by UV-B light give protection against herbivores. Thus,
understanding the direction of the UV-B light effects
on metabolites, on one hand, and the plant-mediated
effects on herbivores, on the other hand, should be
assessed. Second, the optimal combination of UV light
dosage and exposure time to induce targeted defensive
compounds should be determined, as plant response to
UV-B at the molecular level is proposed to depend on
dosage (Brosché & Strid, 2003). In silver birch seedlings
exposed to supplemental monochromatic UV light and
red and FR light, all compounds belonging to the same
phenolic class did not respond to light signals in a similar
way or magnitude (Tegelberg et al., 2004). In addition,
plants exposed continuously to ambient UV-B light levels
have been shown to be more tolerant to supplemental UV
light doses than plants grown without previous exposure
to UV-B light (Takayanagi et al., 1994). This suggests
that plants should be exposed to appropriate UV-B light
levels and dosages continuously instead of, for example,
occasional pulses in order to prevent damages. Third,
UV light exposure often increased plant resistance to
herbivores, but not to all herbivore species, therefore,
augmented UV-B light could reduce the performance of
some pest arthropods, but benefit others.
It might be particularly challenging to manage
whiteflies and other sap-feeding insects via plant traits
induced by augmented UV light. Sap-feeding insects are
able to avoid most of secondary metabolites if they are not
present in vascular tissues (Gatehouse, 2002). Likewise,
monoterpene content of peppermint leaves was assumed
not to affect spider mites because the compounds are
sequestered in cells not fed by spider mites (Larson
& Berry, 1984). In cotton, high phenolic concentration
has, however, been suggested to have negative effects
on whitefly populations (Butter et al., 1992) and
flavonoids and phenolics have shown feeding deterrency
against some aphids (Dreyer & Jones, 1981), but such
effects may be specific only to some plant–herbivore
species complexes. Moreover, direct responses of some
herbivores, which exploit UV wavelengths for orientation,
introduce another challenge of the proposed UV
light augmentation approach. Disruption of whitefly
orientation is used as a pest management tool by
removing UV light from the greenhouse with UV lightabsorbing covers, many of which block wavelengths
below 380 nm (Dı́az & Fereres, 2007). It is not known
to which extent the UV light-depleted environment
interferes with whitefly orientation in the artificial
light greenhouses at high latitudes and which way of
manipulating the UV-B component would affect whitefly
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I. Vänninen et al.
population performance more: completely removing it
to interfere with whitefly orientation or augmenting it
to induce plant defences against whiteflies. There might,
however, be a window of opportunity to achieve both
goals. The important greenhouse pests have their spectral
efficiency peaks between 340 and 400 nm, that is in the
UV-A light area (Matteson et al., 1992; Mellor et al., 1997).
Thus, removing UV-A light, but keeping or reintroducing
UV-B light, might result in double benefit: interference
with pest orientation and increased plant resistance to the
pests. This hypothesis requires testing and closer screening
of both arthropod and plant responses to UV wavelengths.
Higher R : FR ratio, and lower blue : red (B : R) ratio in
comparison with solar radiation, coupled with the use
of interlighting
The usual attenuation of blue and red wavelengths
within the canopy of overhead-lighted plants is less
in interlighted canopies (Frantz et al., 2000). Therefore,
it can be predicted that interlighting would reduce
plant investment to shade-avoidance response (growth)
compared to top-lit canopies. In interlighted canopies, the
R : FR ratio would not be reduced as radically as in toplit canopies, where red light is preferentially absorbed
by leaves whereas FR is transmitted through leaves.
Thus, competition for light among leaves would be lower
in interlighted canopies. At the moment, the evidence
supporting this prediction comes from systems where
natural daylight is reduced either by artificial shading or
self-shading of plants. To our knowledge, no studies of
interlight effects on secondary metabolites or defensive
structures are available from artificial light systems. If
delivering augmented UV light to plants is found to benefit
pest management, interlighting could be particularly
useful for delivering UV light as it might combine
the mitigated shade-avoidance response with enhanced
production of secondary metabolites or physiochemical
defences due to UV-B, both of which would work towards
the higher production of defensive compounds in leaves.
There is no information available on the effect of
blue light on plant secondary metabolites and concomitant higher trophic level responses. At the plant
level, the few available studies suggest that blue light
either does not directly enhance accumulation of secondary metabolites or that it affects their production
less than red light or the combination of red and blue
(Kubasek et al., 1992; Shohael et al., 2006; Shiga et al.,
2009). This suggests that the low relative amount of
blue wavelengths in HPSLs does not play an important
role for plant defence compounds or structures. On the
other hand, strong blue light enhances protein formation in plants and inhibits incorporation of carbon to
Ann Appl Biol 157 (2010) 393–414 © 2010 The Authors
Annals of Applied Biology © 2010 Association of Applied Biologists
I. Vänninen et al.
some carbohydrates (Voskresenskaya, 1972). Whether
altered allocation to carbon-based secondary compounds
would be seen in blue-deficient/supplemented light is not
known. Furthermore, the above phenomena of photosynthate partitioning and its possible effects on secondary
metabolism in blue light-deficient environments need to
be considered also in respect to the role of blue light
in causing shade-avoidance responses in plants (Britz &
Sager, 1990; Ballaré, 1999).
The high proportion of yellow and plant-mediated
effects on arthropods
We found some evidence in the literature that the yellow
portion of HPSL suppresses growth of some greenhouse
plants, which may indicate allocation to defence or,
alternatively, interference of primary metabolism. There
is some evidence that photostress due to supplemental
yellow (596 nm) may influence antioxidant and phenolic
concentrations in a species-dependent manner (Loughrin
& Kasperbauer, 2001). Whether the high proportion of
yellow wavelengths in HPSLs compensates for the lack
of UV-B in terms of secondary metabolite production,
and whether the high proportion of yellow is reflected to
any extent in the biology of herbivores or their natural
enemies awaits testing, as we found no information
on plant-mediated effects of yellow wavelengths on the
higher trophic level.
Earlier lighting conditions can modulate plants’
response to the current (ambient) lighting conditions,
which can be seen for weeks as an after-effect in plant
growth (Brazaitytė et al., 2009a,b). Gussakovsky et al.
(2007) propose that plants possess a long-term colour
memory of immediate light susceptibility, which is highest
in the red-enriched illumination during growth, and also
propose a mechanism for the colour memory. If this is
the case, it brings an additional complexity derived from
plants’ growing conditions to the responses of herbivores
and their natural enemies. Such a situation may arise if it
will become possible to retail optimal lighting conditions
for different stages of plant growth (e.g. seedling and yield
production) by LEDs.
Other growth factors as modulators of plant-mediated
effects of artificial light on arthropods
Enhanced CO2 up to 1000 ppm, high temperatures, and
high-nutrient and water levels used in greenhouse crops
have the potential of modulating the light plant-mediated
effects on arthropods. For instance, plant responses to
augmented UV-B light – even when the doses are in the
ambient range of solar radiation – are likely to depend
on modulating factors of the greenhouse environment.
Ann Appl Biol 157 (2010) 393–414 © 2010 The Authors
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Greenhouse lighting technologies and plant protection
Elevated CO2 concentrations may work against induced
UV-B light effects in plants as shown by Lavola et al.
(1998) for birch leaves. Elevated CO2 levels particularly
may modify the profiles of secondary metabolites and
influence herbivore performance negatively (Lambers,
1993; Matros et al., 2006). On the other hand, increased
C : N ratio can even increase the consumption of
plant material by herbivores because of lower nutritional
quality of leaf material, which results in the compensatory
feeding of herbivores (Lambers, 1993 and references
therein). Even sap-feeding insects such as aphids and
whiteflies have been reported to benefit from elevated
CO2 (Awmack et al., 1997; Grodzinski et al., 1999).
The carbon/nutrient balance hypothesis (CNBH) and
growth differentiation balance hypothesis (GDBH) can
be used as the theoretical background against which the
effect of light, in combination with other environmental factors in artificial light crops, can be considered (see
Herms & Mattson, 1992; Stamp, 2004). GDBH predicts
that plants with high water and nutrient resources should
not be limited by photosynthesis or growth, and so they
should allocate a greater proportion to growth than to differentiation (Herms & Mattson, 1992). Not all secondary
metabolite compounds conform, however, to the GDBH
(Stamp, 2004). In the context of these theories, light as a
resource occupies a special position, because it influences
photosynthesis more than growth (unlike nutrients that
influence growth more than photosynthesis). Therefore,
with increasing light, secondary metabolites are theorised
to increase proportionally with growth (Stamp, 2004).
On the other hand, when plants experience damage, for
example by herbivore feeding, the production of defence
compounds may be favoured in both low-nutrient and
high-nutrient conditions.
Considering the isolated spectral aspects of the artificial
light environment in combination, their net effects on
arthropods via plants are complex. Studies on a model
plant species, whose basic biochemistry and responses
to different light aspects are well known, are likely to
increase a more thorough understanding of such interactions. So far, little or no information is available on
the role of NBL-induced changes in plant biochemical
characteristics for herbivores and their natural enemies.
As NBL technologies enable separating the effects of different wavelengths on plants, LEDs could be used to
assess, for example, the effects of blue, green and yellow wavelengths on the secondary metabolism of plants.
They also would offer a possibility to study the effect
of interlighting decoupled from increased temperatures
near the interlights because of the lower radiation heat
in comparison with HPSLs.
An interesting question is whether NBL could be
used to manipulate plant quality simultaneously for both
407
Greenhouse lighting technologies and plant protection
human nutritional and pest management benefits in a
wavelength-dependent and dose-dependent manner. The
possibility of increasing secondary metabolite concentrations in major horticultural crops with various means
for human nutritional benefits is increasingly addressed
(Schijlen et al., 2006; Dorais et al., 2008; Tsormpatsidis
et al., 2008; Kim et al., 2009). Another aspect to consider in this context is the observed seasonal variation in
nutritionally beneficial plant metabolites in greenhouse
vegetables in areas that rely only on natural solar radiation (Slimestad & Verheul, 2005; Raffo et al., 2006). If
the same variation takes place also in artificial light crops,
could the concentration of useful compounds be kept at
desired levels constantly by adjusting wavelength compositions and light intensity levels inside the greenhouse
throughout the year by using artificial light technologies
or suitable cladding materials? At the same time, such
approach could, in some instances, also improve pest
management via plant-mediated effects of artificial light.
The sheer number of secondary metabolites (Croteau
et al., 2008) is, however, likely to make the matching
of human nutritional and pest management benefits
challenging. The effects of plant secondary metabolites
and of structural defence mechanisms in artificial light
crops grown with HPSLs or other lighting technologies
have been studied hardly at all compared to research on
growth and yield processes. Now when LED lights are
emerging as an artificial lighting technology, it would
be topical to study both plant primary and secondary
metabolism that can be affected by NBL and their combinations. Lastly, an important issue is the scant availability
of cultivars for current artificial light conditions. Wider
number of cultivars might offer the possibility of selecting the most responsive ones to artificial light quality,
intensity and photoperiod in terms of inducing desired
secondary metabolites and defensive structures with the
aim of improving pest management.
Concluding remarks
High-pressure sodium lamps are the current artificial light
technology used in greenhouse at high latitudes, and fulfil
to a certain extent the plant needs. The extended photoperiods used during winter months with the characteristic
light spectra of HPSLs may, however, result in differences
in plant resistance traits between summer and winter
crops. This consequently may lead to differences in population dynamics of pests and their natural enemies. With
this review, we intended to show that current artificial
light conditions during winter might not be the best in
terms of plant protection. Deepening the knowledge of
effects of light on the secondary metabolism of plants and
the plant-mediated effects of light on arthropods could
408
I. Vänninen et al.
improve greenhouse artificial lighting conditions to harmonise crop yield and quality with herbivores and natural
enemy populations, particularly during winter months.
Besides, increased knowledge in this research area will
make us better prepared to evaluate the possible effects
of future lighting technologies on plant protection.
Acknowledgements
We thank Yrjö and Maija Rikala’s horticultural foundation and the Horticultural foundation of the Finnish
Greenhouse Growers’ Association for financial support
for this study. Our thanks are also to Mike Bourget and
Bob Morrow, Orbitec Inc., USA, for clarifying us some
newest developments of LED lighting. We are grateful to
Prof Paula Elomaa at the Department of Applied Biology,
University of Helsinki, for reading and commenting on
an earlier version of the manuscript. Last, our thanks are
to two anonymous reviewers whose comments greatly
improved the manuscript.
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