Biological Control 59 (2011) 1321

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Biological Control
journal homepage: www.elsevier.com/locate/ybcon

Review

Enhancing pest control in annual crops by conservation of predatory Heteroptera

D. Perdikis a,, A. Fantinou b, D. Lykouressis a
a
b

Laboratory of Agricultural Zoology and Entomology, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece
Laboratory of Ecology and Environmental Sciences, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece

a r t i c l e

i n f o

Article history:
Available online 23 April 2011
Keywords:
Conservation biological control
Predator
Heteroptera
Zoophytophagous
Omnivorous
Vegetable

a b s t r a c t
Conservation biological control (CBC) combines a diverse set of actions aiming to enhance pest regulation
by the provision of pest natural enemies preservation in the crop environment. This is accomplished
through appropriate implementation practices and the creation of infrastructures of non-crop vegetation.
On most annual crops, omnivorous heteropteran predators comprise the main assemblage of native natural enemies. Their populations, when protected from pesticides, have shown a high potential in biological control. Aiming to promote their functioning in CBC, efforts targeted to modify the crop environment
are focusing on the determination of their non-crop host plants that can support the predators persistence as well as the emigration of these predators to the nearby crops. Nonetheless, relatively few studies
seek to collect essential and adequately veried data for the practical implementation of CBC approaches.
In this review, the advances already developed are illustrated, the shortcomings are discussed and the
future research needs are highlighted in an effort to intensify efforts for CBC developments on annual
crops.
2011 Elsevier Inc. All rights reserved.

1. Introduction
Biological control (BC) is the regulation of pest populations as a
result of the activity of their living antagonists natural enemies
(predators, parasitoids and pathogens). BC offers a more sustainable and less expensive alternative to chemicals (DeBach and
Rosen, 1991; Bale et al., 2008). In fact, despite the high number
of releases of BC agents that have been performed globally, very
seldom have adverse effects been recorded (van Lenteren et al.,
2006).
Effectiveness in biological control necessitates conservative
measures in the crop environment targeting to the protection of
the natural enemies for a shorter or longer period. In classical BC,
a natural enemy is imported and released in a new area aiming
to provide permanent control of an invasive pest, whereas in augmentative BC periodical releases are performed. In both types, conservation refers to the protection of the released natural enemies
from adverse effects of pesticides, incompatible cultivation practices, but also favoring their establishment and impact by the
adjustment of the environmental conditions or providing food supplements, when possible.
Conservation biological control (CBC) is realized by the activity
of the natural enemies assemblages that already exist in the area
(Barbosa, 2003). CBC consists of premeditated actions for protecting and maintaining natural enemies (Rabb et al., 1976). In the CBC
Corresponding author. Fax: +30 210 529 4577.
E-mail address: dperdikis@aua.gr (D. Perdikis).
1049-9644/$ - see front matter 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.biocontrol.2011.03.014

implementation, the conservation of certain ecosystem identities

prevail, as any actions to be undertaken have to be associated with
a wider area management in the long term. To achieve this, the
habitats and their elements that support the activity of the existing
natural enemies have to be identied, protected and further expanded through a series of appropriate practices (Bugg and Pickett,
1998; Gurr et al., 2000; Landis et al., 2000).
The main feature in agroecosystems that acts in support of natural enemies is the non-crop vegetation (Gurr et al., 2004). Noncrop plants provide requisites and several benets to the natural
enemies such as alternative food and refuges (Jervis and Kidd,
1996; Landis et al., 2000; Begum et al., 2006; Lundgren, 2009).
The creation of ecological infrastructures such as ecological
paths or strips typically consisting of selected non-crop plants or
their communities, not only provide food sources and overwintering shelters for local natural enemies but also protects them from
pesticide disturbances. CBC is an effective strategy in crops such as
in cereals, cabbage, and pear and other fruit orchards (Gruys, 1982;
Thomas et al., 1991; Dennis and Fry, 1992; Wyss, 1996; Letourneau
and Altieri, 1999; Landis et al., 2000; Woodcock et al., 2007; Jonsson et al., 2008).
Although CBC is primarily targeted in ameliorating a single ecosystem function (pest regulation), its implementation reduces pesticide use and conserves or reintroduces natural vegetation. Thus,
CBC is functioning as a key factor to make possible the enhancement of most of the other ecosystem services such as biodiversity
conservation, landscape aesthetics, provision of clean water, reduce soil water retention or soil erosion.

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D. Perdikis et al. / Biological Control 59 (2011) 1321

High diversity per se was supposed to be desirable for effective

CBC, but early in this process, it became evident that careful diversication is actually needed (Risch et al., 1983; Prokopy, 1994;
Baggen and Gurr, 1998; Gurr et al., 2004). Although increased vegetation diversity may enhance BC, complex environments may provide pests with refuges and natural enemies may face difculties in
locating their prey (Root, 1973; Barbosa, 1998; Finke and Denno,
2006; Hughes and Grabowski, 2006). Thus, a key issue in CBC is
to identify the most effective natural enemies, the mechanisms
responsible for their increased persistence and higher effectiveness
within the ecosystem and then attempt to manipulate the crop
environment and create appropriate infrastructures (Straub et al.,
2008).
Among natural enemies, predators encompass a broad range of
traits that are interesting and intriguing in animal ecology as well
as BC. Among them, their feeding habits largely inuence their ecological identities and consequently their effectiveness in BC. For
example, omnivorous heteropteran predators can utilize food of
different trophic levels (i.e., animal and plant food). Phytophagy
constitutes a common trait which can support at an intermediate
or low rate the development and reproduction of these omnivorous
predators. Its effect in predators performance is largely determined by the host plant species (Cohen, 1996; Naranjo and Gibson,
1996; Coll, 1998; Eubanks and Styrsky, 2005; Lundgren, 2009).
Plant feeding may enable them to remain on the crop during periods when their prey is scarce. From a BC point of view, this is an
important attribute, particularly due to favoring their early establishment on the crop, at the initial phase of pest colonization to reduce the time available for unrestricted pest increase (Settle et al.,
1996; Landis and van der Werf, 1997). Specialist natural enemies
are considered as most promising in BC (Hassell, 1978), but generalist predators may also be of major importance in pest suppression (Rosenheim et al., 1993). Generalist predators may be better
suited than specialists in diverse environments indicating their potential in CBC (Coll and Bottrell, 1996; Tscharntke et al., 2002).
Omnivorous heteropteran predators are well recognized as high
value naturally occurring predators in several crops (i.e., Schaefer
and Panizzi, 2000). However, research for appropriate manipulations and creation of infrastructures to enhance their potential within the context of CBC has been mostly explored in orchards or arable
eld crops (Hellenius, 1998; Fauvel, 1999; Marshall and Moonen,
2002; but see Albajes and Alomar, 1999). We conducted a literature
search using ISI Web of Science and Scopus in the Title/keywords/abstract frame with the terms: conservation biological control and
Heteroptera and 29 studies were recovered. Within them, 4, 12
and 5 were also cited by the terms: vegetable, cotton and tomato respectively. This little evidence underline that despite their high
potential, very few efforts have been dedicated to the purposeful
evaluation of natural vegetation and further to the practical guidance for establishment of infrastructures to enhance involvement
of these predators in CBC crop management systems.
The goal of this paper is to document, summarize and critically
review the available scientic evidence on the potential of zoophytophagous heteropteran predators in CBC on annual crops.
We will illustrate the benets and highlight the shortcomings, discuss the measures for optimization, and attempt to prioritize areas
for future research.

2. Key aspects for CBC potential on annual crops

2.1. Overview of the annual crops as a system for CBC
The annual crops have been traditionally considered as less
suitable for CBC than perennial habitats such as orchards due to
their short cycle, since the periodic destruction of the crop causes

high disturbance in the established populations of the natural enemies (Altieri, 1991). The reduction of the populations of natural
enemies deteriorates BC potential and necessitates the colonization of the new crop from natural sources which may result in
weak or late establishment and nally in failures in pest control.
Additionally, intensication and high input investment on these
crops are not favorable for the natural enemies activity. Annual
crops do have some intrinsic attributes that may favor BC as a
desirable alternative to chemical control: (a) the pests in annual
crops are multivoltine and this increases their inherent potential
to develop resistance to chemicals, particularly in greenhouse
environments and (b) the risk for residual contamination of the
products of annual crops by chemical pesticides is increased since
these crops are harvested frequently at close intervals and their
products are mostly consumed fresh. In comparison to augmentative BC, CBC can be less costly because native natural enemies are
used and also safer because releases of exotic agents used in augmentative BC might be associated with environmental risks (van
Lenteren et al., 2006).
Due to their zoophytophagous feeding characteristics, the predatory Heteroptera may offer control of a wide range of pests and for
a prolonged period. Therefore, these predators have been considered as well equipped to cope with ephemeral crops on which prey
availability is variable in space and time (Pimm and Lawton, 1978;
Coll and Guershon, 2002). These characteristics align also with the
statement of Wiedenmann and Smith (1997) that most suitable
natural enemies on annual crops should keep the numbers of pests
at low levels and prevent their increase, since attempting to reduce
high pest populations would be much less efcient.
2.2. CBC in greenhouses: is it feasible?
Annual crops cultivation also includes the greenhouse environments. The application possibilities of CBC in greenhouses have
been considered as a debated issue because they are closed systems
that may provide barriers against the entry of the native natural
enemy fauna. However, there are some types of greenhouses that
may permit the entrance of natural enemies. For example, the plastic tunnels, as well as the open greenhouses of the Mediterranean
area, allow the indigenous natural enemies to move between the
crops, with positive impact in pest control (Albajes and Alomar,
1999; Bosco et al., 2008). In greenhouses with screened sides, the
entrance of natural enemies can be facilitated when kept open,
i.e., in hot conditions. The nethouses might be more suitable as
their sides can be opened. The greenhouses may also act as source
for predators to move out to colonize other close by crops or to nd
refuges in the surrounding area (Gabarra et al., 2004).
In modern greenhouses where the natural entry is prohibited
due to covering of the openings by insect-excluding nets, compatible measures with CBC could be the introduction of non-crop
plants infested with predators to act as sources or refuges of the
predators in the greenhouse (Sanchez et al., 2003). An alternative
approach could be the intended release of heteropteran predators
collected from the native ora of the neighboring area since they
can survive and reproduce on wild, naturally grown, non-crop
plants (i.e., Yano, 2008). Furthermore, at the end of the crop cycle,
the populations that developed on the greenhouse crop may be
collected and transferred to a newly established (greenhouse) crop.
This management or recycling of the natural enemies reservoir are within the context of CBC where sustainable management
of the natural resources in the wider scale and cooperation among
practitioners should be promoted.
Ultimately, in the greenhouse environments, IPM or BC programs are often disrupted or even collapsed by the introduction
of new, sometimes destructive pests (Desneux et al., 2010). The
heteropteran predators prey on a wide range of pests and have

D. Perdikis et al. / Biological Control 59 (2011) 1321

shown a high potential in reducing populations of new invasive

pests in the area (Roditakis, 1991; Urbaneja et al., 2009). Therefore,
their involvement offers signicant benets for the viability of CBC
programs.
2.3. Selection criteria of the non-crop host plants to be utilized in CBC
The selection of the non-crop host plants for implementation in
CBC schemes primarily focuses on the increased persistence and
augmentation of natural enemies in the infrastructure. In the next
sections, certain key issues in the selection of non-cultivated plants
aiming to utilize predatory Heteroptera in CBC are discussed.
2.3.1. Plant species origin: native or exotic?
In the targeted agroecosystem, host plants of the predators that
are either autochthonous, naturalized or exotic may exist. It is
advisable that exotic plants should not be preferred for CBC implementation to avoid the introduction of new invasive weeds or new
pests in the area or the disruption of other ecosystem functions
(Fiedler et al., 2008).
2.3.2. Non-crop plants as potential pest or disease sources
In any scheme designed to support CBC, a rst priority is to detect the non-crop plants that constitute the main sources of the natural enemies in the agroecosystem and then to evaluate which of
them could be further utilized. The host plants that commonly grow
wild in the vicinity of crops may also act as sources of insect or mite
pests and most importantly as reservoirs of plant diseases or their
vectors (van Emden, 1965). In particular, the vegetable crops may
be harmed by several diseases that may be catastrophic. Therefore,
the use of non-suitable host plants may be a major drawback in the
potential of CBC. However, the mere presence of weed species that
may host diseases does not necessarily result in disease outbreaks.
The potential for an outbreak of disease is also dependent on the
vectors presence and efcacy, abiotic factors, the crop developmental stage at the time of vector colonization but also the crop tolerance. In fact, outbreaks do not occur every year even if suspected
weeds are abundant around the crop elds.
The potential of candidate plants in CBC focusing on omnivorous heteropteran predators has only recently been evaluated in
an integrated way. The disease risk has been considered as the
most important criterion in the decision for inclusion of plants in
further evaluation, even when they were hosted by a high number
of predators (Alomar et al., 2006).
Despite the relatively large number of host plant species on
which predator individuals may be recorded, in most cases only
a few of these plant species are important for the conservation of
a predator. Thus, weighing our decisions largely based on disease
threat might introduce a major disadvantage in our effort to sufciently enhance CBC, due to the exclusion of otherwise suitable
plant species. In fact, it will be extremely difcult to achieve zero
risk when selecting host plants for CBC (Gurr et al., 2005), and thus
selection decisions should rationally balance the risk and the potential of the plants in CBC.
2.3.3. Non-crop plants as food sources
The potential of non-crop plants in CBC is also inuenced by
their ability to act as food sources for the heteropteran predators.
For example, anthocorids are well known as predators that beneted by feeding on pollen (Lundgren, 2009). Therefore, a criterion
for the selection of plant species to support the conservation of
anthocorids would be rstly the production of suitable pollen,
and secondly the length of their owering period that mostly coincides with the pollen availability. In this case, plant species with
extending anthesis may be preferred, otherwise mixtures of species with sequential owering can be proposed.

15

On the other hand, selection of non-crop plants based on their

suitability to support predator numbers may be proved misleading.
In fact, biotypes or highly adapted populations of a predator species may have been developed on these highly suitable plants.
These biotypes or populations may show unwillingness to depart
from the non-crop plant and establish on the crop (Perrin, 1975;
Gonzalez et al., 1979; Olson and Wckers, 2007). According to
Eubanks and Denno (1999), dispersal of the predator Geocoris
punctipes (Say) (Hemiptera: Geocoridae) was reversibly related to
host plant quality. Thus, high-quality, non-crop host plants may
act as a sink rather than a source of natural enemies (Landis
et al., 2000; Olson and Wckers, 2007). Accordingly, the potential
of a predator to move from the non-crop plant species to the crop
should be taken into account in the selection process of non-crop
plants for utilization in CBC.
3. Insight of crop specic studies
3.1. Potato
On potato crops, the Colorado potato beetle (CPB), Leptinotarsa
decemlineata (Say) (Coleoptera: Chrysomelidae), is the most serious and destructive insect pest and is well known for its ability
to rapidly develop insecticide resistance (Alyokhin et al., 2008).
The predatory stink bugs, Podisus maculiventris (F.) and Perillus bioculatus (F.) (Heteroptera: Pentatomidae), are major natural enemies of CPB (Ferro, 1994; Hough-Goldstein, 1998). Natural
predation can be substantial but generally occurs too late in the
season for effective CPB management (Aldrich, 1998). Releases of
nymphs can be effective in small plots (Hough-Goldstein and
Whalen, 1993; Cloutier and Bauduin, 1995). However, the cost of
rearing and releasing them in adequate numbers may prohibit
their eld application (Tipping et al., 1999). Aiming to seek alternative approaches, Aldrich and Cantelo (1999) proposed the conservation of P. maculiventris with the use of pheromone-based
technology. Adults massively trapped in cages in early spring were
protected from parasitoids and could produce offspring that disperse on the plants to control CPB.
Aphids are also important pests on potato crops. Indigenous
predators constitute a diverse assemblage including Orius spp.
(Heteroptera: Anthocoridae) that actively suppress aphid populations. Conservation of the aphid predators in potato elds by insecticide-free cultivation in Hokkaido, Japan, for a 5-year period
resulted in sufcient control (Ito and Furukawa, 2009). In an earlier
study, conservation of predators through the non-application of
pesticides drastically reduced the number of aphids and other
pests (Ito et al., 2005). In both studies, the yield was unaffected
in comparison to the control, insecticide-treated elds.
Although the pentatomids and Orius spp. were effective in the
control of the CPB and aphids, respectively, when these two pests
co-occur, a reduction in the effectiveness of the predators guild
may occur. In particular, the increase of the aphid numbers may
deteriorate the impact on the CPB population densities, as occurred
in the case of the Nabis spp. (Heteroptera: Nabidae) and Geocoris
spp. (Heteroptera: Geocoridae) when acting together (Koss and
Snyder, 2005). In addition to CPB and aphids, the two-spotted spider mite and onion thrips were also successfully controlled by
Orius niger (Wolff.) and Orius minutus (L.) which naturally colonized
potato elds in Iran (Fathi, 2009).
3.2. Cotton
Cotton is infested by a wide range of pests such as lepidopterans, aphids, whiteies and thrips. Predatory heteropterans are
important components for the natural control of these pests. For

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D. Perdikis et al. / Biological Control 59 (2011) 1321

example, Orius insidiosus (Say) was the dominant predator on cotton crops and the most important mortality factor of Helicoverpa
zea (Boddie) eggs in Texas (Sansone and Smith, 2001). Also, Orius
spp. were the most abundant predators consisting 69.5% of the
predator numbers on non-chemically treated cotton (Greenberg
et al., 2009). In another example, Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) is common on cotton in South and Central
America and effective against noctuids in Brazil (Medeiros et al.,
2000; Lemos et al., 2001).
Deraecoris nebulosus (Uhler) (Heteroptera: Miridae) is commonly recorded in high numbers on cotton elds [14 nymphs
and adults/m/row (>137,000/ha)]. In laboratory tests, it readily
consumed cotton aphids and eggs of Heliothis virescens (F.) and rst
instar larvae of Spodoptera exigua (Hbner). Therefore, it appears to
be a naturally occurring predator that can have a signicant impact
on the pest populations on cotton crops (Snodgrass, 1991). In
northern China, the native Orius similis Zheng and Deraeocoris
punctulatus Fall largely supported the suppression of Bemisia tabaci
(Gennadius) (Homoptera: Aleyrodidae) (Lin et al., 2008).
Naranjo et al. (2002) showed that the application of conventional insecticides on cotton highly reduced the populations of major natural enemies, including G. punctipes, G. pallens (Stl), Orius
tristicolor (White), Nabis alternatus Parshley, Zelus renardii Kolenati,
in California and Arizona. The authors recognized that enhancing
the establishment of the predators early in the season is the key
issue in CBC and proposed raising the initial damage threshold to
delay the rst insecticide application, or alternatively, to use more
selective insecticides. Further study proved the compatibility of
selective insecticides with the conservation of natural enemies
on cotton (Naranjo et al., 2004).
G. punctipes acting together with O. insidiosus managed to keep
the populations of the sucking insect pests below the economic injury level at all the phenological stages of the cotton plants. The
major management practice that made this outcome possible
was the non-application of pesticides (Solangi et al., 2008).
The widely recognized importance of heteropteran predators on
cotton crops led to efforts to evaluate their potential in CBC using
other crop or non-crop host plants. Loya-Ramrez et al. (2003)
showed that the interplanted plants: canola (Brassica napus L.), alfalfa (Medicago sativa L.), hairy vetch (Vicia villosa Roth) and sanfoin
(Onobrychis viciifolia Scop.) supported high populations of heteropteran predators accompanied by a signicant migration toward
the intercropped cotton. In particular, Geocoris spp. attained highest densities on hairy vetch that increased towards the end of the
crop season. On the same plant, Nabis spp. were initially favored,
but densities were higher in alfalfa and sanfoin. On alfalfa, Orius
spp. had the highest density during the whole season. In comparison, treated cotton attained the lowest number of predators.
Plantings of Sorghum bicolor (L.) Moench (grain sorghum) beside cotton crops effectively favored the abundance of heteropteran predators but also their timely emigration to the cotton crops
(Fye, 1971). This approach was further explored by Prasifka et al.
(1999). They used marked and recapture methods to record the
movements of the predators including Orius in adjacent plantings
of cotton and grain sorghum. The outcomes revealed that cotton
gained approximately twice as many dispersing predators from
sorghum than those it lost, suggesting that the association is benecial. A mean speed of movement of about 2232 m/day was
estimated, indicating fast moving, showing that relatively large
elds may be colonized by predators ying from the edges, reducing the density of strip of sorghum needed inside the cotton crops
in CBC implementation. Therefore, the sorghum identities were
considered to make this scenario possible since: (a) both plants
share the same predator species, (b) sorghum is tolerant to insect
damage and seldom requires application of pesticides and thus
can act as a source of predators, and (c) cotton received inuxes

of predators near its critical boll formation in both years of the

study.
In conservation-tillage cotton with crimson clover or rye as cover
crops, a signicant drop in damage of lepidopterous pests was recorded in comparison to conventional-tillage cotton without cover
crops. This result was attributed to the buildup of G. punctipes and
predaceous re ants populations in these elds (Tillman et al.,
2004). In contrast, Ruberson et al. (1995) reported that populations
of G. punctipes were lower in conservation than in conventional-tillage cotton eld. In a further study, no differences in G. punctipes populations were detected between crimson clover cotton and
conventional-tillage cotton without a cover crop (Ruberson et al.,
1997). As mentioned by Tillman et al. (2004), the major difference
between their study and the other ones that led to their positive evidence was the maintenance of a strip of live crimson clover as a habitat for G. punctipes within the cotton crop, whereas in the other cases
the crimson clover was completely killed before planting the main
crop.
Evangelista et al. (2003) evaluated the potential of six non-crop
host plant species on the life history characteristics of the predator,
P. nigrispinus. The results outlined that phytophagy on the weeds,
Ageratum conyzoides L., Bidens pilosa L. and Amaranthus hybridus
L., supported the longevity and fecundity of the predator.
In cotton, the CBC potential could be enhanced if combined with
other environmentally friendly pest control strategies such as the
mating disruption to reduce key-pest numbers and/or the application of supplementary foods on the cotton crop to attract and conserve natural enemies (Mensah, 1997; Wade et al., 2008).
3.3. Pepper
Greenhouse and open eld pepper crops may be heavily infested by the thrips, Frankliniella occidentalis (Pergande) and Thrips
tabaci Lindeman (Thysanoptera: Thripidae), or aphids pests. The
major natural enemies against thrips are omnivorous heteropteran
predators of the family Anthocoridae (Funderburk et al., 2000).
Orius are pollen feeders and their effectiveness is increased on
plants that produce pollen, such as peppers.
O. niger and Orius laevigatus (Fieber) can naturally colonize
greenhouses and highly contribute to the control of thrips if not
disturbed by chemical pesticide applications (Tavella et al., 1991;
Delbeke et al., 1997; Silveira et al., 2004). In Northern Italy, O. niger
was the main predator (56% of adult anthocorids in 2002 and 67%
in 2003) naturally colonizing pepper greenhouses, followed by
Orius majusculus (Reuter). On the other hand, O. laevigatus was
present exclusively in the greenhouses where it was released, but
at low percentages and only for a short period. Starting from late
June, O. niger colonized the crops naturally, and compared to the
introduced O. laevigatus, could reproduce and develop throughout
the growing season. O. niger was also prevailing in the wild neighboring ora followed by O. majusculus (76% and 16% of the specimens collected, respectively) (Bosco et al., 2008).
An earlier example of the limited efciency of introduced Orius
species is that of the Nearctic O. insidiosus, which had a much lower
ability to colonize pepper crops than the native O. niger (van de
Veire and Degheele, 1992). Similarly, native populations of O. niger
were effective in colonizing pepper crops in Central and Southern
Greece (Barbetaki et al., 1999). However, natural colonization of
pepper crops by Orius may occur later than the period that thrips
damage and virus transmission occurs and this introduces an
important inefciency in thrips control. For this reason, suitable
manipulation of natural vegetation in the eld surroundings may
be necessary in order to increase the potential of these predators
in biological control on pepper crops (Tavella et al., 2003; Bosco
et al., 2008). This aim has triggered studies to record their non-crop
host plants as potential means to support CBC of Orius.

D. Perdikis et al. / Biological Control 59 (2011) 1321

Tavella et al. (2003) captured O. niger on several non-crop

plants. Tommasini (2004) reported the relative abundance of 6
native Orius species on 5 main non-crop host plants in Italy. O. niger
and O. leavigatus were the main ones recorded on Cirsium, Sinapis
alba L. and Dittrichia viscosa (L.) Greuter. In another study in
north-western Italy, O. niger was sampled on 13 different non-crop
plant species, and each of O. majusculus and O. minutus on 7 plant
species (Bosco et al., 2008). Among these plants, Urtica dioica
L., Sinapis arvensis L. and Matricaria chamomilla L., hosted all three
species. Roditakis et al. (2003) reported that in the natural vegetation in the island of Crete (Southern Greece), O. niger, O. laevigatus
and Orius albidipennis (Reuter) were the most frequently recorded.
The non-crop plants where highest populations occurred were on
Thymaelea hirsuta (L.), Daucus carota maxima, Satureia thymbra
L. and Rosa micrantha Borrer ex Sm. Among them, Th. hirsuta hosted
high numbers of O. laevigatus almost all year round. On this plant,
both adults and nymphs were recorded indicating its potential to
support the predators reproduction. This wild host plant appears
to be valuable in CBC because it can support the predators persistence and increase of its population and has a long owering period that sustains the predator populations for a long period.
In a similar study, Cano et al. (2009) reported that O. laevigatus
was common on 5 non-crop plant species in Almeria, Spain.
Th. hirsuta and Mentha suaveolens Ehrhard were the most prominent. The former plant is a small shrub and was considered difcult
to propagate, and for this reason only the latter species was suggested for possible further implementation within CBC measures.
Similarly, Yano (2008) reported that the conservation of Orius strigicollis (Poppius) on non-crop host plants rich in pollen such as
Verbana and Scaevola aemula had a positive impact on its reproduction and subsequently on the CBC of thrips pests on pepper and
eggplant.
In Greece, Spain, and Japan, the farmers may collect wild Orius
population from non-crop plants for subsequent introduction in
greenhouse pepper crops (Roditakis et al., 2003; Yano, 2008; Cano
et al., 2009).
Alomar et al. (2006) evaluated the comparative suitability of
several non-crop plant species as hosts of Orius populations in
experimental plots. Twelve of the 25 plant species tested bore
the highest Orius numbers. Two of the plants that hosted most predators were not considered further because of their late owering
and the apparent drawback of failure in early crop colonization.
Five other plant species were the most suitable as they owered
early in the season from February to mid-May. Taking further into
account the potential of the plants to act as pest or disease sources,
the authors concluded that Vicia sativa L. and Lupinus hispanicus
Boiss. & Reut. as best suited for conservation of Orius.

3.4. Legumes
On leguminous crops, the conservation of heteropteran omnivorous predators may largely contribute to the control of whiteies
or other pests but their contribution can be signicant against the
highly polyphagous pest, the southern green stinkbug Nezara viridula L. (Heteroptera: Pentatomidae). This pest causes economic
damage in several crops like cotton, tomato or eggplant. The control of N. viridula relies heavily upon insecticides and this is a major
constraint in the IPM programs on these crops (Knight and Gurr,
2007).
The oriental asopine, Amyotea malabarica (F.) (Heteroptera:
Pentatomidae), has demonstrated a strong preference for N. viridula over lepidopterous prey (Singh et al., 1973). A number of other
heteropterans, mainly reduviids, have been noted to act as predators of N. viridula with biocontrol potential (Ambrose, 1999;
Grundy and Maelzer, 2000a).

17

Conserved natural populations of pentatomid predators can be

a promising alternative in the CBC of this pest (Panizzi et al.,
2000). In particular, Pristhesancus plagipennis (Walker) (Heteroptera: Reduviidae) consumes high numbers of the younger nymphal
instars of N. viridula, possibly reducing populations to below economic threshold (Grundy and Maelzer, 2000b). The stink bug, P.
maculiventris, may contribute to suppressing N. viridula outbreaks
particularly in hot spots and its conservation or protection from
pesticides may largely contribute to more effective BC (De Clercq
et al., 2002).
Knight and Gurr (2007) recognized that targeted habitat manipulation can enhance CBC mainly through the maintenance of the
reduviid predators. If applied together with other non-chemical
control methods, this approach could support the control of this
pest. On faba bean, uncropped eld margins supported considerable numbers of Orius spp. with positive evidence in thrips control.
For this reason, the maintenance of these margins was proposed
(Atakan, 2010).
3.5. Tomato
Tomatoes are infested by a wide range of pests such as whiteies, aphids, thrips, mites, leafminers and lepidopterans. Despite
the diverse pest complex, their major natural enemies assemblage
is largely constituted by few predatory omnivorous mirid species.
In the Mediterranean region, Macrolophus pygmaeus Rambur, Nesidiocoris tenuis (Reuter), Dicyphus tamaninii Wagner and Dicyphus
errans (Wolff) and in the North America, Dicyphus hesperus Knight
(Heteroptera: Miridae) are considered to be among the principal
natural enemies of pests on tomatoes.
Mirids are polyphagous, feeding on almost the entire spectrum of
tomato pests (e.g., McGregor et al., 1999; Perdikis and Lykouressis,
2000; Enkegaard et al., 2001; Urbaneja et al., 2005; Fantinou et al.,
2009). They show phytophagous habits that support their development or reproduction to a variable rate depending on the plant
substrate (Perdikis and Lykouressis, 2000, 2004; Sanchez et al.,
2004). They are widely used on commercial scale in releases against
whiteies and other pests on vegetable greenhouse crops (van Lenteren, 2003).
In the Mediterranean region, naturally occurring populations of
Macrolophus and Dicyphus species can colonize eld or greenhouse
tomato crops and keep the pest numbers below the damage
threshold if chemical sprayings are reduced (Malausa et al.,
1987; Casta et al., 1989; Perdikis and Lykouressis, 1996; Albajes
and Alomar, 1999). Casta et al. (2004) and Gabarra et al. (2004)
searched in detail the inout movements of the predators and
showed their high potential for colonization of tomato greenhouses. N. tenuis can also naturally colonize tomato crops and substantially contribute to the control of whiteies (Carnero et al.,
2000).
The assemblage of these predators is also important against the
destructive pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)
which recently invaded the Mediterranean region. This pest originates from South America where the role of the naturally occurring
heteropteran predator Xylocoris sp. (Heteroptera: Anthocoridae)
has been important. It has been proposed that the conservation
of this predator should be a priority in the management strategies
of this pest (Miranda et al., 1998). Macrolophus pygmaeus and N.
tenuis have shown a high potential to prey on the eggs and the
young larvae of this pest in the laboratory (Arn et al., 2009;
Urbaneja et al., 2009). According to Arn et al. (2009), in the tomato elds where the natural populations of these two predatory
species were well established, the damage by T. absoluta was signicantly lower than in the chemically treated elds.
Other heteropteran predators that have been evaluated for the
control of T. absoluta belong to the family Nabidae. Nabis pseudoferus

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D. Perdikis et al. / Biological Control 59 (2011) 1321

Remane is a native natural enemy usually found on tomato crops in

Spain. Experimental evidence showed that its young nymphs can
signicantly reduce the numbers of T. absoluta eggs, indicating its
potential as a promising candidate for the biological control of this
pest (Cabello et al., 2009).
The role of mirid predators is also signicant in the control of
additional pests of tomato. Nesidiocoris tenuis effectively suppress
populations of the tomato fruit borer Helicoverpa armigera (Hbner) (Lepidoptera: Noctuidae) (Devi et al., 2002). Another example
is where the naturally occurring populations of M. pygmaeus were
effective in the control of aphid pests on eld tomato crops in Central Greece (Lykouressis et al., 19992000).
The efcient natural colonization of tomato crops by the mirid
predators indicates their high potential in CBC and stimulated
studies to explore which elements (non-crop plant species) of the
native vegetation could act as a refuge or source of their populations in the crop environment. Alomar et al. (2002) and Casta
et al. (2004) showed that the colonization of tomato crops by native predators was higher in elds surrounded by complex agroenvironments. Similarly, the environmental complexity may substantially inuence the abundance of M. pygmaeus and D. errans
in tomato greenhouses (Ingegno et al., 2009). In fact, although
naturally occurring mirid predators can enter greenhouses, it
may occur too late for sufcient control of the pests. Further developments in CBC should be directed to identify which non-crop host
plants support high numbers of these predators early in the season
(Gabarra et al., 2004). However, the key elements of natural vegetation that support dispersal and natural colonization of tomato
crops by Macrolophus remain unclear (Alomar and Albajes, 2003).
The clarication of systematic aspects has been a fundamental issue since unresolved taxonomic issues may retard BC (Gordh and
Bearsley, 1999; Stouthamer, 2008).
In tomato crops, Macrolophus pygmaeus and M. caliginosus Wagner (a junior synonym of M. melanotoma (Costa)), have been reported to occur. Their close resemblance raised questions about
their identity (Goula and Alomar, 1994; Kerzhner and Josifov,
1999). However, recent studies based on DNA analysis and cross
mating have shown that the Macrolophus specimens examined
from tomato belonged to M. pygmaeus (Perdikis et al., 2003;
Martinez-Cascales et al., 2006).
To identify the non-crop plants that host M. pygmaeus populations in the agroecosystem molecular analyses showed that all
the Macrolophus specimens collected on Solanum nigrum L. (Solanaceae) from West Peloponnese, Greece belonged to M. pygmaeus
(Perdikis et al., 2006). S. nigrum is a major host plant for M. pygmaeus in Greece (Lykouressis et al., 2000; Perdikis et al., 2006). Recent
data have shown that M. pygmaeus can complete development on
S. nigrum without prey and can also reproduce when infested by its
main native aphid pest (Lykouressis et al., 2008). Therefore, this
plant should be evaluated in CBC systems, as a natural reservoir
of M. pygmaeus for tomato crop colonization.
In Crete, these mirids were found at higher numbers on the following non-cultivated plants: Dimorphotheca aurantia, Cistus creticus L., Amaranthus blitum L., and Datura stramonium L. (Roditakis
et al., 2003). In Italy, they were present mainly on Artemisia vulgaris
L. and other (11 in total) non-crop plant species (Ingegno et al.,
2009). Alomar et al. (2006) proposed that Calendula ofcinalis L.
and Ononis natrix L. were the most suitable for the conservation
of Macrolophus. Cano et al. (2009) reported that N. tenuis naturally
occurred on 9 plant species with the most important being D. viscosa and the Pelargonium spp. Specimens from D. viscosa were not
found to host the main viruses that damage tomato.
In greenhouse tomatoes, the use of alternative host plants has
been evaluated as a means to introduce the mirid predator, D. hesperus. This predator was invariably found to be more common in
greenhouses where the alternative host plant, Verbascum thapsus

L., had been introduced, providing also a refuge for the predator
when prey on tomato was scarce. Establishment of the predators
populations on these non-crop plants would largely contribute to
the early colonization of the following greenhouse crop and the
effective control of whitey pests (Sanchez et al., 2003). In tomato
unheated greenhouses, Arn et al. (2000) showed that tobacco
plants can serve as a refuge for the mirid predators during winter
that may enhance the timely and efcient colonization of the next
spring tomato crop.
As a measure within the frame of CBC, it has been also suggested that the farmers could collect predators on crops plants at
the end of the crop cycle or on major non-crop plants for subsequent release in greenhouses (Lykouressis et al., 19992000;
Roditakis et al., 2003; Cano et al., 2009).
3.6. Other crops
Strawberries are infested with several species of thrips worldwide. Coll et al. (2007) demonstrated that releases of O. laevigatus
were not justied in insecticide-free strawberry crops grown in
low tunnels in Israel, since the thrips populations were successfully controlled by native O. niger and O. albidipennis. Bosco et al.
(2009) evaluated the thrips control in plots where articial releases
of Orius bugs were performed in comparison to greenhouses where
chemical control was applied. The results showed that both treatments were equally effective. Furthermore, in the biological control plots, the native O. niger prevailed over the released O.
majusculus. Therefore, native predators play a signicant role in
thrips control on strawberries and should be conserved. In greenhouse roses, introduction of Tagetes plants during their owering
period may increase the effectiveness of the released O. insidiosus
and this technique worth further evaluation (Bueno et al., 2009).
4. Conclusions and suggestions
The omnivorous predators comprise distinct functional groups,
commonly present on annual crops with a signicant contribution
in natural pest control. This evidence lies in support of the view
that effectiveness in pest regulation may not be positively associated with increased complexity but simplied natural enemy communities may be highly effective (Bianchi et al., 2010).
The high potential of heteropteran predators in CBC can be largely attributed to their (a) wide prey range covering almost the entire spectrum of pests and thus, when conserved, they can offer
effective protection of the crop, (b) zoophytophagous feeding habit
so that they can survive for a longer or shorter period on crop
plants without prey and already existing populations can suppress
pest numbers when the pests appear and start to increase, keeping
them below economic threshold, and (c) populations can persist
and increase on certain non-crop plants that act as refuges and natural reservoirs enabling their persistence and the colonization of
the new crop.
Thus far, the high proportion of this encouraging evidence is derived from studies where the only means to enhance the effectiveness of the naturally occurring populations of these predators was
the drastic reduction of pesticide use. Although it reects the high
potential of CBC if these predators are conserved, this is only the
rst step towards the development of CBC implementation
strategies.
Recent research efforts have been devoted to systematically
explore and evaluate non-crop host plants of omnivorous
heteropteran predators as elements of CBC agro-environment
schemes in annual crops. In this regard, evidence from related research highlights the areas where future efforts should be directed
to (a) correctly identify the predator species on each candidate

D. Perdikis et al. / Biological Control 59 (2011) 1321

non-crop plant, (b) evaluate the dispersal ability that determines

the appropriate spatial distribution of non-crop habitats in the
landscape (Tscharntke et al., 2005) with practical consequences
in the realistic design of CBC implementation, and (c) manipulate
the environment to enhance the early establishment on the target
crop and consequently search the role of each candidate plant as a
source to guarantee the timely crop colonization in the eld. Data
acquisition and its verication on this context would enable CBC
researchers to realize the specic benets for each crop, the creation of infrastructures and then, optimize the implementation of
CBC practices (Landis et al., 2000).
There is an urgent need to expand our approaches and consider
additional important prerequisites to quantify and promote the
realistic implementation possibilities of CBC. Although very few
studies have included cost benet assessments of CBC (Cullen
et al., 2008), such approaches need to be undertaken to invariably
assess the economic viability of the methods proposed (taking also
into account the possible benets for the provision of other ecosystem services) and nally to attract the interest of the farmers.
Likely, complementary implementation of CBC with other environmentally friendly and sustainable pest regulation methods such
as mating disruption or food supplement and use of selective pesticides may increase effectiveness and adoption rates by the CBC
practitioners, particularly in certain crops harmed by difcult to
handle key pests. It is envisaged that future research efforts should
ideally focus on the investigation and verication of the above
mentioned aspects in an integrated way. These approaches would
ultimately enable the development of attractive and viable methods to increase the likelihood of adoption of CBC in annual crops
with the aid of the heteropteran predatory bugs.
References
Albajes, R., Alomar, O., 1999. Current and potential use of polyphagous predators.
In: Albajes, R., Gullino, M.L., Van Lenteren, J.C., Elad, Y. (Eds.), Integrated Pest
Disease Management in Greenhouse Crops. Kluwer Academic Publishers,
Dordrecht, The Netherlands, pp. 265275.
Aldrich, J.R., 1998. Status of semiochemical research on predatory Heteroptera. In:
Coll, M., Ruberson, J.R. (Eds.), Predatory Heteroptera: Their Ecology and Use in
Biological Control. Proc. Thomas Say Publ. Entomol. Entomological Society of
America, Lanham, Maryland., pp. 3348.
Aldrich, J.R., Cantelo, W.W., 1999. Suppression of Colorado potato beetle infestation
by pheromone-mediated augmentation of the predatory spined soldier bug,
Podisus maculiventris (Say) (Heteroptera: Pentatomidae). Agriculture and Forest
Entomology 1, 209217.
Alomar, O., Albajes, R., 2003. Habitat management for conservation of the native
predator Macrolophus caliginosus. IOBC/WPRS Bulletin 26 (4), 711.
Alomar, O., Gabarra, R., Gonzlez, O., Arn, J., 2006. Selection of insectary plants for
ecological infrastructure in Mediterranean vegetable crops. IOBC/WPRS Bulletin
29 (6), 58.
Alomar, O., Goula, M., Albajes, R., 2002. Colonisation of tomato elds by predatory
mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agriculture Ecosystems
and Environment 89, 105115.
Altieri, M.A., 1991. How best can we use biodiversity in agroecosystems. Outlook on
Agriculture 20, 1523.
Alyokhin, A., Baker, M., Mota-Sanchez, D., Dively, G., Graus, E., 2008. Colorado
potato beetle resistance to insecticides. American Journal of Potato Research 85,
395413.
Ambrose, D.P., 1999. Assassin bugs. Science Publishers Inc., Eneld, New
Hampshire. 337 pp..
Arn, J., Ario, J., Espaol, R., Mart, M., Alomar, O., 2000. Conservation of
Macrolophus caliginosus Wagner (Het. Miridae) in commercial greenhouses
during tomato crop-free periods. IOBC/WPRS Bulletin 23 (1), 241246.
Arn, J., Sorribas, R., Prat, M., Matas, M., Pozo, C., Rodrguez, D., Garreta, A., Gmez,
A., Gabarra, R., 2009. Tuta absoluta, a new pest in IPM tomatoes in the northeast
of Spain. IOBC/WPRS Bulletin 49, 203208.
Atakan, E., 2010. Inuence of weedy eld margins on abundance patterns of the
predatory bugs Orius spp. and their prey, the western ower thrips (Frankliniella
occidentalis), on faba bean. Phytoparasitica 38, 313325.
Bale, J.S., van Lenteren, J.C., Bigler, F., 2008. Biological control and sustainable food
production. Philosophical Transactions of the Royal Society B 363, 761776.
Barbetaki, A., Lykouressis, D., Perdikis, D., 1999. Predatory species of the genus Orius
recorded in elds of vegetable crops. IOBC/WPRS Bulletin 22 (5), 97101.
Barbosa, P., 1998. Agroecosystems and conservation biological control. In: Barbosa,
P. (Ed.), Conservation biological control. Academic Press, San Diego, CA, pp. 39
54.

19

Barbosa, P., 2003. Conservation Biological Control. Academic Press, San Diego, CA,
USA.
Baggen, L.R., Gurr, G.M., 1998. The inuence of food on Copidosoma koehleri
(Hymenoptera: Encyrtidae), and the use of owering plants as a habitat
management tool to enhance biological control of potato moth, Phthorimaea
operculella (Lepidoptera: Gelechiidae). Biological control 11, 917.
Begum, M., Gurr, G.M., Wratten, S.D., Hedberg, P.R., Nicol, H.I., 2006. Using selective
food plants to maximize biological control of vineyard pests. Journal of Applied
Ecology 43, 547554.
Bianchi, F.J.J.A., Booij, C.J.H., Tscharntke, T., 2010. Sustainable pest regulation in
agricultural landscapes: a review on landscape composition, biodiversity and
natural pest control. Proceedings of the Royal Society B 273, 17151727.
Bosco, L., Baudino, M., Tavella, L., 2009. Management of thrips (Thysanoptera:
Thripidae) on strawberries in north-western Italy: biological control and
damage evaluation. IOBC/WPRS Bulletin 49, 177182.
Bosco, L., Giacometto, E., Tavella, L., 2008. Colonization and predation of thrips
(Thysanoptera: Thripidae) by Orius spp. (Heteroptera: Anthocoridae) in sweet
pepper greenhouses in Northwest Italy. Biological Control 44, 331340.
Bueno, V., Silva, A., Carvalho, L., Moura, N., 2009. Control of thrips with Orius
insidiosus in greenhouse cut roses: use of a banker plant improves the
performance of the predator. IOBC/WPRS Bulletin 49, 183187.
Bugg, R.L., Pickett, C.H., 1998. Introduction: enhancing biological control habitat
management to promote natural enemies of agricultural pests. In: Pickett, C.H.,
Bugg, R.L. (Eds.), Enhancing biological Control. University of California Press,
Berkeley, CA, pp. 123.
Cabello, T., Gallego, J.R., Fernandez-Maldonado, F.J., Soler, A., Beltran, D., Parra, A.,
Vila, E., 2009. The damsel bug Nabis pseudoferus (Hem.: Nabidae) as a new
biological control agent of the South American Tomato Pinworm, Tuta absoluta
(Lep.: Gelechiidae), in tomato crops of Spain. IOBC/WPRS Bulletin 49, 219223.
Cano, M., Vila, E., Janssen, D., Bretones, G., Salvador, E., Lara, L., Tellez, M.M., 2009.
Selection of refuges for Nesidiocoris tenuis (Het.: Miridae) and Orius laevigatus
(Het.: Anthocoridae): virus reservoir risk assessment. IOBC/WPRS Bulletin 49,
281286.
Carnero, A., Daz, S., Amador, S., Hernndez, M., Hernndez, E., 2000. Impact of
Nesidiocoris tenuis Reuter (Hemiptera: Miridae) on whitey population in
protected tomato crops. IOBC/WPRS Bulletin 23 (1), 259.
Castae, C., Alomar, O., Goula, M., Gabarra, R., 2004. Colonization of tomato
greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus
tamaninii. Biological Control 30, 591597.
Casta, C., Bordas, E., Gabarra, R., Alomar, O., Albajes, R., 1989. Progress in the
implementation of IPM programs on protected crops in Catalonia. In: Cavalloro,
R., Pelerents, C. (Eds.), Integrated Pest Management in Protected Vegetable
Crops. A. A. Balkema, Rotterdam, pp. 339346.
Cloutier, C., Bauduin, F., 1995. Biological control of the Colorado potato beetle
Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) in Quebec by
augmentative release of the two-spotted stink bug Perillus bioculatus
(Hemiptera: Pentatomidae). Canadian Entomologist 127, 195212.
Cohen, A.C., 1996. Plant feeding by predatory Heteroptera: evolutionary and
adaptational aspects of trophic switching. In: Alomar, O., Wiedenmann, R.N.
(Eds.), Zoophytophagous Heteroptera: Implications for Life History and
Integrated Pest Management. Entomological Society of America, Lanham, MD,
pp. 117.
Coll, M., 1998. Living and feeding on plants in predatory Heteroptera. In: Coll, M.,
Ruberson, J.R. (Eds.), Predatory Heteroptera: Their Ecology and Use in Biological
Control. Entomological Society of America, Lanham, MD, USA, pp. 89130.
Coll, M., Bottrell, D.G., 1996. Movement of an insect parasitoid in simple and diverse
plant assemblages. Ecological Entomology 21, 141144.
Coll, M., Guershon, M., 2002. Omnivory in terrestrial arthropods: mixing plant and
prey diets. Annual Review of Entomology 47, 267297.
Coll, M., Shakya, S., Inbar, S., Nenner, Y., Steinberg, S., 2007. Decision-making tools
for Frankliniella occidentalis management in strawberry: consideration of target
markets. Entomologia Experimentalis et Applicata 122, 5967.
Cullen, R., Warner, K.D., Jonsson, M., Wratten, S.D., 2008. Economics and adoption of
conservation biological control. Biological control 45, 272280.
De Clercq, P., Wyckhuys, K., De Oliveira, H.N., Klapwijk, J., 2002. Predation by Podisus
maculiventris on different life stages of Nezara viridula. Florida Entomologist 85,
197202.
DeBach, P., Rosen, D., 1991. Biological Control by Natural Enemies. Cambridge
University Press.
Delbeke, F., Vercruysse, P., Tirry, L., De Clercq, P., Degheele, D., 1997. Toxicity of
diubenzuron, pyriproxyfen, imidacloprid and diafenthiuron to the predatory
bug Orius laevigatus (Het.: Anthocoridae). Entomophaga 42, 349358.
Dennis, P., Fry, G., 1992. Field margins can they enhance natural enemy
populationdensities and general arthropod diversity on farmland.
Agriculture Ecosystems and Environment 40, 95115.
Desneux, N., Wajnberg, E., Wyckhuys, K.A.G., Burgio, G., Arpaia, S., Narvaez-Vasquez,
C.A., Gonzalez-Cabrera, J., Catalan Ruescas, D., Tabone, E., Frandon, J., Pizzol, J.,
Poncet, C., Cabello, T., Urbaneja, A., 2010. Biological invasion of European
tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for
biological control. Journal of Pest Science 83, 197215.
Devi, P.K., Yadav, D.N., Anand, J., 2002. Role of Nesidiocoris tenuis reuter (Hemiptera:
Miridae) in natural suppression of tomato fruit borer, Helicoverpa armigera
(Hubner) (Lepidoptera: Noctuidae). Pest Management in Horticultural
Ecosystems 8, 109113.
Enkegaard, A., Brodsgaard, H.F., Hansen, D.L., 2001. Macrolophus caliginosus:
functional response to whiteies and preference and switching capacity

20

D. Perdikis et al. / Biological Control 59 (2011) 1321

between whiteies and spider mites. Entomologia Experimentalis et Applicata

101, 8188.
Eubanks, M.D., Denno, R.F., 1999. The ecological consequences of variation in plants
and prey for an omnivorous insect. Ecology 80, 12531266.
Eubanks, M.D., Styrsky, J.D., 2005. Effects of plant feeding on the performance of
omnivorous predators. In: Wckers, F.L., van Rijn, P.C.J., Bruin, J. (Eds.), Plantprovided food and herbivorecarnivore Interactions. Cambridge University
Press, Cambridge, pp. 148177.
Evangelista, J.R., Walter, S., Gondim, J.R., Manoel, G.C., Torres, Jorge B., Marques,
Edmilson J., 2003. Effect of weeds and cotton plants on development,
reproduction and preference for oviposition of the predatory Bug Podisus
nigrispinus (Dallas) (Heteroptera: Pentatomidae). Neotropical Entomology 32,
677684.
Fantinou, A.A., Perdikis, D.Ch., Labropoulos, P., Maselou, D., 2009. Preference and
consumption of Macrolophus pygmaeus preying on mixed instar assemblages of
Myzus persicae. Biological Control 51, 7680.
Fathi, S.A.A., 2009. The abundance of Orius niger (Wolf.) and O. minutus (L.) in potato
elds and their life table parameters when fed on two prey species. Journal of
Pest Science 82, 267272.
Fauvel, G., 1999. Diversity of Heteroptera in agroecosystems: role of sustainability
and bioindication. Agriculture Ecosystems and Environment 74, 275303.
Ferro, D.N., 1994. Biological control of the Colorado potato beetle. In: Zehnder, G.W.,
Jansson, R.K., Powelson, M.L., Raman, K.V. (Eds.), Advances in Potato Pest
Biology and Management. American Phytopathological Society, St. Paul, MN,
USA, pp. 357375.
Fiedler, A.K., Landis, D.A., Wratten, S.D., 2008. Maximizing ecosystem services from
conservation biological control: the role of habitat management. Biological
control 45, 254271.
Finke, D.L., Denno, R.F., 2006. Spatial refuge from intraguild predation: implications
for prey suppression and trophic cascades. Oecologia 149, 265275.
Funderburk, J.E., Stavisky, J., Olson, S.M., 2000. Predation of Frankliniella occidentalis
(Thysanoptera: Thripidae) in eld peppers by Orius insidiosus (Hemiptera:
Anthocoridae). Environmental Entomology 29, 376382.
Fye, R.E., 1971. Grain sorghum: a source of insect predation for insects on cotton.
Progressive Agriculture in Arizona 23, 1213.
Gabarra, R., Alomar, O., Castae, C., Goula, M., Albajes, R., 2004. Movement of
greenhouse whitey and its predators between in- and outside of
Mediterranean greenhouses. Agriculture Ecosystems and Environment 102,
341348.
Gonzalez, D., Gordh, G., Thompson, S.N., Adler, J., 1979. Biotype discrimination and
its importance to biological control. In: Hoy, M.A., McKelvey, J.J. (Eds.), Genetics
Relation to Insect Management. Rockefeller Foundation, New York, pp. 129
136.
Gordh, G., Bearsley, J.H., 1999. Taxomomy and biological control. In: Bellows, T.S.,
Fischer, T.W. (Eds.), Handbook of Biological Control. Academic Press, San Diego,
pp. 4556.
Goula, M., Alomar, O., 1994. Miridos (Heteroptera Miridae) de inters en el control
integrado de plagas en tomate. Gua para su identicacin. Boletn de Sanidad
Vegetal Plagas 20, 131143.
Greenberg, S.M., Liu, T.-X., Adamczyk, J.J., 2009. Thrips (Thysanoptera: Thripidae) on
cotton in the lower Rio Grande valley of Texas: species composition, seasonal
abundance, damage, and control. Southwestern Entomologist 34, 417430.
Grundy, P., Maelzer, D., 2000a. Assessment of Pristhesancus plagipennis (Walker)
(Hemiptera: Reduviidae) as an augmented biological control in cotton and
soybean crops. Australian Journal of Entomology 39, 305309.
Grundy, P., Maelzer, D., 2000b. Predation by the assassin bug Pristhesancus
plagipennis (Walker) (Hemiptera: Reduviidae) of Helicoverpa armigera
(Hbner) (Lepidoptera: Noctuidae) and Nezara viridula (L.) (Hemiptera:
Pentatomidae) in the laboratory. Australian Journal of Entomology 39, 280282.
Gruys, P., 1982. Hits and misses. The ecological approach to pest control in orchards.
Entomologia Experimentalis et Applicata 31, 7087.
Gurr, G.M., Scarratt, S.L., Wratten, S.D., Berndt, L., Irvin, N., 2004. Ecological
engineering, habitat manipulation and pest management. In: Gurr, G.M.,
Wratten, S.D., Altieri, M.A. (Eds.), Ecological Engineering for Pest
Management: Advances in Habitat Manipulation for Arthropods. Cornell
University Press, New York, NY, pp. 112.
Gurr, G.M., Wratten, S.D., Barbosa, P., 2000. Success in conservation biological
control of arthropods. In: Gurr, G.M., Wratten, S.D. (Eds.), Biological Control:
Measures of Success. Dordrecht, Kluwer, pp. 105132.
Gurr, G.M., Wratten, S.D., Kehrli, P., Scarratt, S., 2005. Cultural manipulations to
enhance biological control in Australia and New Zealand: progress and
prospects, in: Proceedings of the Second International Symposium on
Biological Control of Arthropods, Switzerland, September 1216, 2005, pp.
154166.
Hassell, M.P., 1978. The Dynamics of Arthropod Predator-Prey System. Princeton,
NJ.
Hellenius, J., 1998. Enhancement of predation through within-eld diversication.
In: Pickett, C.H., Bugg, R.L. (Eds.), Enhancing Biological Control: Habitat
Management to Promote Natural Enemies of Agricultural Pests. University
California Press, Berkeley, pp. 121160.
Hough-Goldstein, J., Whalen, J., 1993. Inundative release of predatory stink bugs for
control of Colorado potato beetle. Biological Control 3, 343347.
Hough-Goldstein, J.A., 1998. Use of predatory pentatomids in integrated
management of the Colorado potato beetle (Coleoptera: Chrysomelidae). In:
Predatory Heteroptera: Their Ecology and Use in Biological Control.
Entomological Society of America, Lanham, MD, pp. 209223.

Hughes, A.R., Grabowski, J.H., 2006. Habitat context inuences predator

interference interactions and the strength of resource partitioning. Oecologia
149, 256264.
Ingegno, B.L., Pansa, M.G., Tavella, L., 2009. Tomato colonization by predatory bugs
(Heteroptera: Miridae) in agroecosystems of NW Italy. IOBC/WPRS Bulletin 49,
287291.
Ito, K., Furukawa, K., 2009. Effects of insecticide-free potato cultivation on the
occurrence of aphids, their predators and tuber yield. Japanese Journal of
Applied Entomology and Zoology 53, 4551.
Ito, K., Furukawa, K., Okubo, T., 2005. Conservation biological control of aphids in
potato elds with reduced use of insecticides in Hokkaido, Japan. Japanese
Journal of Applied Entomology and Zoology 49, 1122.
Jervis, M.A., Kidd, N.A.C., 1996. Phytophagy. In: Jervis, M.A., Kidd, N.A.C. (Eds.), Insect
Natural Enemies. Chapman and Hall, London, pp. 375394.
Jonsson, M., Wratten, S.D., Landis, D.A., Gurr, G.M., 2008. Recent advances in
conservation biological control of arthropods by arthropods. Biological Control
45, 172175.
Kerzhner, I.M., Josifov, M., 1999. Cimicomorpha II: Miridae. In: Aukema, B., Rieger, C.
(Eds.), Catalogue of the Heteroptera of the Palaearctic Region. Wageningen, The
Netherlands.
Knight, K.M.M., Gurr, G.M., 2007. Review of Nezara viridula (L.) management
strategies and potential for IPM in eld crops with emphasis on Australia. Crop
Protection 26, 110.
Koss, A.M., Snyder, W.E., 2005. Alternative prey disrupt biocontrol by a guild of
generalist predators. Biological Control 32, 243251.
Landis, D.A., van der Werf, W., 1997. Early-season predation impacts the
establishment of aphids and spread of beet yellows virus in sugar beet.
Entomophaga 42, 499516.
Landis, D.A., Wratten, S.D., Gurr, G.M., 2000. Habitat management to conserve
natural enemies of arthropod pests in agriculture. Annual Review of
Entomology 45, 175201.
Lemos, W.P., Medeiros, R.S., Ramalho, F.S., Zanuncio, J.C., 2001. Effects of plant
feeding on the development, survival, and reproduction of Podisus nigrispinus
(Dallas) (Heteroptera: Pentatomidae). International Journal of Pest
Management 47, 8993.
Letourneau, D.K., Altieri, M.A., 1999. Environmental management to enhance
biological control in agroecosystems. In: Bellows, T.S., Fischer, T.W. (Eds.),
Handbook of Biological Control. Academic Press, San Diego, pp. 319354.
Lin, K., Wu, K., Zhang, Y., Guo, Y., 2008. Naturally occurring populations of Bemisia
tabaci, biotype B and associated natural enemies in agro-ecosystem in northern
China. Biocontrol Science and Technology 18, 169182.
Loya-Ramrez, J.S., Garca-Hernndez, J.L., Ellington, J.J., Thompson, D.V., 2003. The
impact of interplanting crops on the density predation of hemiptera predators.
Interciencia 28, 415420.
Lundgren, J.G., 2009. Relationships of Natural Enemies and Non-prey Foods.
Springer International, Dordrecht, The Netherlands.
Lykouressis, D., Giatropoulos, A., Perdikis, D., Favas, C., 2008. Assessing the
suitability of non-cultivated plants and associated insect prey as food sources
for the omnivorous predator Macrolophus pygmaeus (Hemiptera: Miridae).
Biological Control 44, 142148.
Lykouressis, D., Perdikis, D., Tsagarakis, A., 2000. Polyphagous mirids in Greece: host
plants and abundance in traps placed in some crops. Bollettino del Laboratorio
di Entomologia Agraria Filippo Silvestri 56, 5768.
Lykouressis, D.H., Perdikis, D.Ch., Chaljia, F.Ch., 19992000. The effects of natural
enemies on aphid populations on processing tomato in central Greece.
Entomologia Hellenica 13, 3542.
Malausa, J.C., Drescher, J., Franco, E., 1987. Prospectives for the use of the predacious
bug Macrolophus caliginosus Wagner, (Heteroptera: Miridae) on glasshouse
crops. IOBC/WPRS Bulletin 10 (2), 106107.
Marshall, E.J.P., Moonen, A.C., 2002. Field margins in northern Europe: their
functions and interactions with agriculture. Agriculture Ecosystems and
Environment 89, 521.
Martinez-Cascales, J.I., Cenis, J.L., Cassis, G., Sanchez, J.A., 2006. Species identity of
Macrolophus melanotoma (Costa 1853) and Macrolophus pygmaeus (Rambur
1839) (Insecta: Heteroptera: Miridae) based on morphological and molecular
data and bionomic implications. Insect Systematics and Evolution 37, 385404.
McGregor, R.R., Gillespie, D.R., Quiring, D.M.J., Foisy, M.R.J., 1999. Potential use of
Dicyphus hesperus Knight (Heteroptera: Miridae) for biological control of pests
of greenhouse tomatoes. Biological control 16, 104110.
Medeiros, R.S., Ramalho, F.S., Lemos, W.P., Zanuncio, J.C., 2000. Age-dependent
fecundity and life fertility tables for Podisus nigrispinus (Dallas) (Het.,
Pentatomidae). Journal of Applied Entomology 124, 319324.
Mensah, R.K., 1997. Local density responses of predatory insects of Helicoverpa spp.
to a newly developed food supplement Envirofeast in commercial cotton in
Australia. International Journal of Pest Management 43, 221225.
Miranda, M.M.M., Picano, M., Zanuncio, J.C., Guedes, R.N.C., 1998. Ecological life
table of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Biocontrol Science
and Technology 8, 597606.
Naranjo, S.E., Ellsworth, P.C., Chu, C.C., Henneberry, T.J., 2002. Conservation of
predatory arthropods in cotton: role of action thresholds for Bemisia tabaci
(Homoptera: Aleyrodidae). Journal of Economic Entomology 95, 682691.
Naranjo, S.E., Ellsworth, P.C., Hagler, J.R., 2004. Conservation of natural enemies in
cotton: role of insect growth regulators in management of Bemisia tabaci.
Biological Control 30, 5272.
Naranjo, S.E., Gibson, R.L., 1996. Phytophagy in predaceous Heteroptera: effects on
life history and population dynamics. In: Alomar, O., Wiedenmann, R. (Eds.),

D. Perdikis et al. / Biological Control 59 (2011) 1321

Zoophytophagous Heteroptera: Implications for Life History and Integrated Pest
Management. Thomas, Say Publications in Entomology Proceedings,
Entomological Society of America, pp. 5793.
Olson, D.M., Wckers, F.L., 2007. Management of eld margins to maximize
multiple ecological services. Journal of Applied Ecology 44, 1321.
Panizzi, A.R., McPherson, J.E., James, D.G., Javahery, M., McPherson, R.M., 2000. Stink
bugs (Pentatomidae) pp. 421474. In: Schaefer, C.W., Panizzi, A.R. (Eds.),
Heteroptera of Economic Importance. CRC Press, Boca Raton, FL, 828pp.
Perdikis, D., Fantinou, A., Kourti, A., Paraskeuopoulos, A., Lykouressis, D., 2006.
Establishment of a polyphagous mirid predator in the crop: The importance of
non-cultivated plants. IOBC/WPRS Bulletin 29 (6), 9396.
Perdikis, D., Lykouressis, D., 1996. Aphid populations and their natural enemies on
fresh market tomatoes in central Greece. IOBC/WPRS Bulletin 19 (11), 3337.
Perdikis, D., Lykouressis, D., 2000. Effects of various items, host plants and
temperatures on the development and survival of Macrolophus pygmaeus
(Rambur) (Hemiptera: Miridae). Biological Control 17, 5560.
Perdikis, D., Lykouressis, D., 2004. Macrolophus pygmaeus (Hemiptera: Miridae)
population parameters and biological characteristics when feeding on eggplant
and tomato without prey. Journal of Economic Entomology 97, 12911298.
Perdikis, D.Ch., Margaritopoulos, J.T., Stamatis, C., Mamuris, Z., Lykouressis, D.P.,
Tsitsipis, J.A., Pekas, A., 2003. Discrimination of the closely related biocontrol
agents Macrolophus melanotoma (Hemiptera: Miridae) and M. pygmaeus using
mitochondrial DNA analysis. Bulletin of Entomological Research 93, 507
514.
Perrin, R.M., 1975. The role of the perennial stinging nettle, Urtica dioica, as a
reservoir of benecial nature enemies. Annals of Applied Biology 81, 289
297.
Pimm, S.L., Lawton, J.H., 1978. On feeding on more than one trophic level. Nature
275, 542544.
Prasifka, J.R., Krauter, P.C., Heinz, K.M., Sansone, C.G., Minzenmayer, R.R., 1999.
Predator conservation in cotton: using grain sorghum as a source for insect
predators. Biological Control 16, 223229.
Prokopy, R.C., 1994. Integration in orchard pest and habitat management: a review.
Agriculture Ecosystems and Environment 50, 110.
Rabb, R.L., Stinner, R.E., van den Bosch, R., 1976. Conservation and augmentation of
natural enemies. In: Huffaker, C.B., Messenger, P.S. (Eds.), Theory and Practice of
Biological Control. Academic Press, New York, NY, USA, pp. 233254.
Risch, S.J., Ando, D., Altieri, M.A., 1983. Agroecosystem diversity and pest control:
data, tentative conclusions, and new research applications. Environmental
Entomology 12, 625629.
Roditakis, N.T., 1991. First Record of Frankliniella occidentalis in Greece. Entomologia
Hellenica 9, 7779.
Roditakis, N.E., Perdikis, D., Roditakis, E., Lykouressis, D.P., Papadaki, M., 2003.
Benecial Hemiptera Anthocoridae and Miridae in Crete. 10th Panhellenic
Entomological Congress, Heraklion Crete, 47 November 2003, Book of
Abstracts, p. 93 (in Greek).
Root, R.B., 1973. Organization of a plant-arthropod association in simple and diverse
habitats: the fauna of collards (Brassica oleracea) Ecological Monographs 43, 95
124.
Rosenheim, J.A., Wilhoit, L.R., Armer, C.A., 1993. Inuence of intraguild predation
among generalist insect predators on the suppression of an herbivore
population. Oecologia 96, 439449.
Ruberson, J.R., Phatak, S.C., Lewis, W.J., 1997. Insect populations in a cover crop/strip
till system, in: Proceedings, Beltwide Cotton Conferences. National Cotton
Council, Memphis, TN, pp. 11211124.
Ruberson, J.R., Lewis, W.J., Waters, D.J., Stapel, O., Haney, P.B., 1995. Dynamics of
insect populations in a reduced-tillage, crimson clover/cotton system, in:
Proceedings, Beltwide Cotton Conferences. National Cotton Council, Memphis,
TN, pp. 814821.
Sanchez, J.A., Gillespie, D.R., McGregor, R.R., 2004. Plant preference in relation to life
history traits in the zoophytophagous predator Dicyphus hesperus. Entomologia
Experimentalis et Applicata 112, 719.
Sanchez, J.A., Martinez-Cascales, J.I., Lacasa, A., 2003. Abundance and wild host
plants of predator mirids (Heteroptera: Miridae) in horticultural crops in the
Southeast of Spain. IOBC/WPRS Bulletin 26, 147151.
Sansone, C.G., Smith, J.W.Jr., 2001. Natural mortality of Helicoverpa zea
(Lepidoptera: Noctuidae) in short-season cotton. Environmental Entomology
30, 112122.
Schaefer, C.W., Panizzi, A.R., 2000. Heteroptera of Economic Importance. CRC Press,
Boca Raton, FL. 828 pp.
Settle, W.H., Ariawan, H., Astuti Endah, T., Cahyana, W., Hakim Arief, L., Hindayana,
D., Lestari Alifah, S., Sartanto, P., 1996. Managing tropical rice pests through
conservation of generalist natural enemies and alternative prey. Ecology 77,
19751988.

21

Silveira, L.C.P., Bueno, V.H.P., van Lenteren, J.C., 2004. Orius insidiosus as biological
control agent of thrips in greenhouse chrysanthemums in the tropics. Bulletin
of Insectology 57, 103109.
Singh, Z., White, C.E., Luckmann, W.H., 1973. Notes on Amyotea malabarica, a
predator of Nezara viridula in India. Journal of Economic Entomology 66, 551
552.
Snodgrass, G.L., 1991. Deraecoris nebulosus (Heteroptera: Miridae): Little known
predator in cotton in the Mississippi delta. Florida Entomologist 74, 340
344.
Solangi, G.S., Mahar, G.M., Oad, F.C., 2008. Presence and abundance of different
insect predators against sucking insect pest of cotton. Journal of Entomology 5,
3137.
Stouthamer, R., 2008. Molecular tools. In: van Driesche, R., Hoddle, M., Center, T.
(Eds.), Control of pests and weeds by natural enemies: an introduction to
biological control. Blackwell Publishing, pp. 167180.
Straub, C.S., Finke, D.L., Snyder, W.E., 2008. Are the conservation of natural enemy
biodiversity and biological control compatible goals? Biological Control 45,
225237.
Tavella, L., Arzone, A., Alma, A., 1991. Researches on Orius laevigatus (Fieb.), a
predator of Frankliniella occidentalis (Perg.) in greenhouses. A preliminary note.
IOBC/WPRS Bulletin 14, 6572.
Tavella, L., Bosco, L., Faure, E., 2003. Distribution and population dynamics of Orius
spp. in sweet pepper greenhouses in north-west Italy. IOBC/WPRS Bulletin 26
(10), 153157.
Thomas, M.B., Wratten, S.D., Sotherton, N.W., 1991. Creation of island habitats in
farmland to manipulate populations of benecial arthropods: predator
densities and species composition. Journal of Applied Ecology 28, 906917.
Tillman, G., Schomberg, H., Phatak, S., Mullinix, B., Lachnicht, S., Timper, P., Olson, D.,
2004. Inuence of cover crops on insect pests and predators in conservation
tillage cotton. Journal of Economic Entomology 97, 12171232.
Tipping, P.W., Holko, C.A., Abdul-Baki, A.A., Aldrich, J.R., 1999. Evaluating Edovum
puttleri Grissell and Podisus maculiventris (Say) for augmentative biological
control of Colorado potato beetle in tomatoes. Biological Control 16, 3542.
Tommasini, M.G., 2004. Collection of Orius species in Italy. Bulletin of Insectology
57, 6572.
Tscharntke, T., Rand, T.A., Bianchi, F.J.J.A., 2005. The landscape context of trophic
interactions: insect spillover across the cropnoncrop interface. Annales
Zoologici Fennici 42, 421432.
Tscharntke, T., Steffan-Dewenter, I., Kruess, A., Thies, C., 2002. Characteristics of
insect populations on habitat fragments: A mini review. Ecological Research
229, 239.
Urbaneja, A., Montn, H., Moll, O., 2009. Suitability of the tomato borer Tuta
absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. Journal of
Applied Entomology 133, 292296.
Urbaneja, A., Tapia, G., Stansly, P., 2005. Inuence of host plant and prey availability
on developmental time and survivorship of Nesidiocoris tenuis (Het.: Miridae).
Biocontrol Science and Technology 15, 513518.
van de Veire, M., Degheele, D., 1992. Biological control of the Western Flower
Thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), in
glasshouse sweet pepper with Orius spp. (Hemiptera: Anthocoridae). A
comparative study between O. niger (Wolff) and O. insidiosus (Say). Biocontrol
Science and Technology 2, 281283.
van Emden, H.F., 1965. The role of uncultivated land in the biology of crop pests and
benecial insects. Scientic Horticulture 17, 121136.
van Lenteren, J.C., 2003. Commercial availability of biological control agents. In: van
Lenteren, J.C. (Ed.), Quality Control and Production of Biological Control Agents.
Theory and Testing Procedures. CABI Publishing, pp. 167179.
van Lenteren, J.C., Bale, J.S., Bigler, F., Hokkanen, H.M.T., Loomans, A.J.M., 2006.
Assessing risks of releasing exotic biological control agents of arthropod pests.
Annual Review of Entomology 51, 609634.
Wade, M.R., Zalucki, M.P., Wratten, S.D., Robinson, K.A., 2008. Conservation
biological control of arthropods using articial food sprays: current status
and future challenges. Biological control 45, 185199.
Wiedenmann, R.N., Smith, J.W.Jr., 1997. Attributes of natural enemies in ephemeral
crop habitats. Biological Control 10, 1622.
Woodcock, B.A., Potts, S.G., Pilgrim, E., Ramsay, A.J., Tscheulin, T., Parkinson, A.,
Smith, R.E.N., Gundrey, A.I., Brown, V.K., Tallowin, J.R., 2007. The potential of
grass eld margin management for enhancing beetle diversity in intensive
livestock farms. Journal of Applied Ecology 44, 6069.
Wyss, E., 1996. The effects of articial weed stripes on diversity and abundance of
the arthropod fauna in a Swiss experimental apple orchard. Agriculture
Ecosystems and Environment 60, 4759.
Yano, E., 2008. Recent progress in IPM and biological control in Japan. IOBC/WPRS
Bulletin 32, 261264.