agronomy

Review
Almeria’s Green Pest Management Revolution: An Opportunity
That Arose from a Food Safety Alert
Miguel M. Acebedo 1 , Fernando Diánez 2, * and Mila Santos 2

1 Consejería de Agricultura, Pesca y Desarrollo Rural Delegación Territorial de Almería, c/Hermanos Machado,
04004 Almeria, Spain; martinm.acebedo@juntadeandalucia.es
2 Departamento de Agronomía, Escuela Superior de Ingeniería, Universidad de Almería, 04120 Almeria, Spain;
msantos@ual.es
* Correspondence: fdianez@ual.es; Tel.: +34-(95)-0214108

Abstract: Almería, a province of Spain, is the leader in horticultural production on a Spanish and
European scale. The specific conditions of greenhouse cultivation favor plant development, but
also the proliferation of pests. This high incidence of pests was controlled in the past mainly by
means of chemical phytosanitary treatments. The aim of the present work has been to analyze
the tools facilitated by the Andalusian Government (Junta de Andalucía) to replace the usual pest
management process, taking advantage of the context of the food safety alert arising from the
detection of isophenphos-methyl in peppers from the province of Almeria in December 2007. The
results illustrate that, unlike many programs of public subsidies which involve long-term expenditure,
the aid in question took advantage of the socioeconomic situation following the food safety alert. The
program led to substantial economic savings and met its objectives swiftly, achieving excellent results
in terms of removing most of the pesticides used in the “conventional production system”. In the
2006–2007 season, only 515 hectares in Almería used biological control organisms, four years later,




it reached 20,081 hectares, and the average area during the last ten years was 24,953 hectares. This

 shows that Almeria’s green pest management revolution had been consolidated.
Citation: Acebedo, M.M.; Diánez, F.;
Santos, M. Almeria’s Green Pest Keywords: biological control; chemical control; pest management; isofenphos-methyl residues;
Management Revolution: horticultural crops
An Opportunity That Arose from
a Food Safety Alert. Agronomy 2022,
12, 619. https://doi.org/10.3390/
agronomy12030619
1. Introduction
Academic Editor: Gavin Ash Almería is one of the eight provinces that make up the autonomous community of
Received: 4 February 2022
Andalusia in southern Spain. Over 32,554 hectares of this province are currently dedicated
Accepted: 28 February 2022
to greenhouse crops production (52,350 hectares cultivated in 2020/21 growing season, in
Published: 2 March 2022
60.8% of the area, two crops are grown per year), mainly watermelon 12,575 ha, pepper
12,310 ha, tomato 8423 ha, zucchini 8061 ha, cucumber 5280 ha, melon 3205 ha, eggplant
Publisher’s Note: MDPI stays neutral
2277 ha, and green bean 219 ha. Over the 2020/21 growing season, total greenhouse
with regard to jurisdictional claims in
crops production reached 3,509,459 t (73.8% of which was exported with a sale value of
published maps and institutional affil-
2803 million euros), which provided greenhouse growers with a total of 2121.3 million
iations.
euros. Almería is undoubtedly the leader in greenhouse horticultural production on both
the national and European scale [1].
The specific conditions of greenhouse cultivation favor plant development, but also
Copyright: © 2022 by the authors.
the proliferation of pests. This high incidence of pests was controlled in the past by means
Licensee MDPI, Basel, Switzerland. of phytosanitary treatments, producing harmful effects on the health of handlers as well
This article is an open access article as environmental and eco-toxicological damage [2,3]. This scenario, combined with the
distributed under the terms and drastic reduction of active substances allowed by the European Commission and additional
conditions of the Creative Commons restrictions imposed by the market, meant that numerous pests became more resistant to
Attribution (CC BY) license (https:// pesticides. This resistance is particularly relevant in the case of thrips and whitefly, which
creativecommons.org/licenses/by/ are present in all protected crops, and which act as vectors of several viruses which are
4.0/). especially aggressive towards certain crops.

Agronomy 2022, 12, 619. https://doi.org/10.3390/agronomy12030619 https://www.mdpi.com/journal/agronomy

Agronomy 2022, 12, 619 2 of 13

Given these circumstances, as well as adjustments to food safety parameters due to

increasing awareness and a greater demand for food quality (both at origin and particularly
at the destination markets), it was merely a question of time before food safety alerts arose
due to the presence of pesticide residues.
This moment arrived on 27 December 2006, when the European Commission’s Rapid
Alert System for Food and Feed (RASFF) sent the Spanish Agency for Food Safety (AESA)
data from Germany informing of the detection of isofenphos-methyl residues in 9 of
the 15 fresh pepper samples analyzed. This non-authorized substance was subsequently
detected in fresh peppers in the United Kingdom, the Netherlands and Finland, among
other countries. This organophosphate pesticide, banned for several years in the UE, had
been used in Almería to control Frankliniella occidentalis (Pergande), the main virus vector
in pepper, which at the time was seriously affected by TSWV (Tomato spotted wilt virus).

The Opportunity for a Change

The presence of isofenphos-methyl in peppers cultivated in Almería on December 2007
received widespread media coverage, giving rise to considerable concern in the sector, and
of course, in Spanish and European consumers. The main distribution chains penalized
Almería’s growers, and as a result, imports of Spanish pepper to the UE fell by 20% to
324,000,000 kg (almost 108 t less than had been exported in 2002), putting an end to the
upward sales trend since 2004. Shortly afterwards, other emerging markets, such as Russia,
also announced that they were closing their frontiers to the import of pepper from Spain.
At the time of this phytosanitary alert, only 1.9% of the surface area of horticultural
crops in Almería controlled pests by means of biological control organisms, but four years
later, this figure had increased to 54% (92% in the case of pepper crops). After suffering
this food safety alert, the entire sector, including the auxiliary companies, research centers
and the Administration (Regional Government of Andalusia), did a big effort for the indis-
pensable change from the traditional chemical control of pests and diseases to Integrated
Production methods (IPM). This process is known as the “Green pest management revolu-
tion”, turning the province of Almería into a Mediterranean and Worldwide reference about
the successful application of Biological Control strategies [4]. Juntti and Downward [5]
refer to IPM evolution in Almeria as one of the successful moves to “green” Almeria’s
horticultural production, driven by market demands.
Currently, fourteen years later (2020/2021 season), the cultivated area in which biolog-
ical pest control is carried out is around 26,288 hectares, although with well-differentiated
situations between crops. The pepper is the crop with the largest area under biological
control 12,260 ha (99.6% of the crop area), followed by tomato 5372 ha (63.8%), cucum-
ber 3637 ha (68.9%), aubergine 1704 ha (74.8%), zucchini 1407 ha (17.2%), watermelon
1285 ha (10.2%), melon 595 (18.6%) and green bean 28 ha (12.8%) [1].
The aim of the present work has been to analyze the tools facilitated by the Andalusian
Government (Junta de Andalucía) to replace the usual chemical pest management process,
taking advantage of the context of the food safety alert arising from the detection in
international markets of isofenphos-methyl in fresh produce from the province of Almería.

2. How to Modify the Agrosystem

From 1980 to 1985, long before the aforementioned food safety alert arose and brought
about the market crisis, the need to improve pest control systems and to seek viable alter-
natives was put forward. It was around this period that the Department of Agriculture
and Fisheries for the Regional Government of Andalusia promoted a series of studies and
trials in conjunction with phytosanitary enterprises, companies specializing in the produc-
tion of organisms for the biological control of pests and especially agrarian associations,
technicians and growers who were prepared to take the risk of applying these new tech-
niques, thus laying the foundations for their subsequent development. This collaborative
effort came to fruition in 2000, when the first Specific Regulations of Integrated Production
(including Integrated Pest Management, or IPM) were published for several species of

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Agronomy 2022, 12, 619 3 of 13

greenhouse horticultural crops [6]. In their section on pest control, these regulations listed
both the autochthonous biological control organisms to be respected and the commercial
ones that could be used, while stressing the importance of prioritizing the use of these
organisms rather than phytosanitary products. Consequently, there was a sound base of
technical knowledge on which to build up a system of pest control in which pesticides
played a secondary role [7], allowing the creation of a public database on biological control
organisms to control pest training use [8]. However, until the 2006/07 growing season, the
farms which took advantage of this knowledge were like isolated “islands” which were
seriously affected by the sea of neighboring farms surrounding them which continued to
employ chemical substances for pest control.
This scenario changed drastically from 2007 onwards, when as a result of the
isofenphos-methyl food safety alert [9], a legal framework was set up which allowed
public subsidies to encourage growers to adopt biological pest control, particularly to
control insect vectors of viruses in protected horticultural crops.
Indeed, in 2007, the Spanish government procured authorization from the European
Union (no. 273/2007) to provide public funding to implement the compulsory measures
foreseen in the national program for the control of insect vectors of viruses in horticultural
crops which had been passed in 2004 [10]. This program was included in the decree which
identified insect vectors as the principal phytosanitary problem and deemed their control
to be in the public interest. The difficulty in controlling one of these insects, namely western
flower thrips (Frankliniella occidentalis), had been at the origin of the food safety alert.
In this context, the Andalusian Department of Agriculture and Fisheries implanted
two lines of aid to growers’ associations: one aimed to foment the purchase of biological
control organisms [11] as a means of controlling the insect vectors of viruses in the crops,
subsidizing 50% of their cost; and another one whose purpose was to encourage quality
production [12,13] by subsidizing the contracting of Pest Control Advisors for Integrated
Production Groups (IPG), set up by growers with a view to obtaining high quality agricul-
tural produce by applying the Regulations of Integrated Production (IPM programs).
The regulations on subsidies were drawn up to include a series of points aimed at
attaining efficacy and efficiency in line with the public spending involved. These points
and the measures implemented to ensure they are fulfilled are described below.

2.1. Establishment of Homogeneous Crop Areas

Ensuring homogeneous crop areas of sufficient size allows effective biological control
(BC) of the insect vectors without interference from the use of chemical substances. Given
the small size of horticultural farms in Almería, it proved crucial to involve growers that
were grouped together in a variety of associations, mainly Agrarian Cooperatives (SCA)
and Agricultural Processing Companies (SAT). Those growers that did not belong to such
associations were given the opportunity to constitute an Integrated Production Group (IPG),
an Integrated Treatments in Agriculture Group (ITAG), or an Ecological Production Group
(EPG). In order to achieve this fundamental objective, subsidies were refused to individual
growers who did not apply for aid as a member of one of the above-mentioned associations.

2.2. Pest Control Adviser (PCAs) Training

Technical training of a large number of “pest control advisers” (PCAs) was established
over a short period of time, preparing them in methods of biological control in order to
minimize mistakes in decisions on effective pest control. To this end, the administration
commissioned the Andalusian Institute for Research and Training into Agriculture, Fish-
eries, Food and Ecological Production (IFAPA) to prepare and impart training courses.
This organization had proven experience in this topic as well as suitable facilities in the
province of Almería, and they were chosen due to the awareness that any credible and
effective plan of biological pest control depended on suitable preliminary training. The
training programs involved experts from the administration and the University of Almería,
as well as the special collaboration of companies that produce and market biological control

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Agronomy 2022, 12, 619 4 of 13

organisms (BCOs). Every PCA that passed the course and was willing to serve in the control
programs of insect vectors of viruses was required to register on an official government list
for subsequent monitoring and control.
To supplement the limited information available about GIP in protected crops, the
Department of Agriculture and Fisheries published manuals and control over the use of
BCOs of interest for technicians and producers [14]. It did this by taking advantage of
important Internet coverage in rural areas which made it possible to develop online IPM
manuals available at https://www.juntadeandalucia.es/agriculturapescaydesarrollorural/
raif/manuales-de-campo (accessed on 1 February 2022).

2.3. Scope of the PCAs

In Almería, all growers have access to PCAs. However, these advisors do not all have
the same aims, nor do they dedicate the same amount of time to the monitoring of crops.
As a result, there are often major differences in the crop surface that they supervise. To
minimize possible differences in the application of control plans, it was decided to set
a maximum crop area for each PCA (supplier-affiliated or independent), depending on the
type of crop and the average size of the greenhouses that they were to assess. Limit criteria
were established to avoid sampling errors due to work overload, especially if the cultivation
area supervised by each advisor was very large and the size of the greenhouses was small.
The maximum area was set at 50 hectares for PCAs belonging to grower associations with
an average surface area per greenhouse of less than 7500 m2 , and 80 hectares when the
average surface area per farm was over 15,000 m2 . This limitation was intended to avoid
differences in the monitoring of crops, such as those detected in California for almond
crops, where supplier-affiliated PCAs managed a mean of 94.4 almond-bearing hectares,
while independent PCAs managed a mean of 124.3 [15].
Since this limiting factor was liable to give rise to additional assessment costs for
producer associations, they were offered the chance to set up an IPG, as this would allow
them access to public subsidies to offset expenditure on PCAs.

2.4. Control and Monitoring

While the regulations on integrated production (IPM programs) were based on scien-
tific and technical criteria, provision was made for adjustments according to the different
requirements of crops and zones. An additional factor that might lead to diversity is
whether the PCA is affiliated, for instance, to a supplier or rather is contracted by a growers’
association (Independent PCA). This may result in differences in decision making that
could have a bearing on the efficacy of plans, as happened in California in the cultivation
of the almond tree where independent PCAs communicated more frequently with growers
than PCAs who are employed by agricultural product suppliers. Growers who use inde-
pendent PCAs tend to feel more knowledgeable about integrated pest management (IPM)
and report the use of more complex pest-monitoring techniques and control practices [15].
Consequently, all PCAs are obliged to carry out the control of the production process and
to fill out the farm logbook, in which they must note down all operations: release of BCOs,
doses, application of phytosanitary products, pruning, etc. These logbooks are used to
build up a database for establishing future adjustments and improvements to the plans,
and all growers are obliged to follow the technical recommendations of their PCAs.
A sample of the farm logbook from four farms of each PCA must be sent weekly via
a software program named TRIANA to a centralized database which determines the extent
to which the plans are being put into practice and the effects they are having.
Another of the aims of TRIANA that has been maintained over time is the acquisition
of knowledge of the phytosanitary state of crops and the building up of a series of records.
The results have been published on the Department of Agriculture and Fisheries web-
site: https://www.juntadeandalucia.es/agriculturapescaydesarrollorural/raif/informes-
historicos1 (accessed on 1 February 2022).

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Agronomy 2022, 12, 619 5 of 13

2.5. Production Capacity and Price of BCOs

Exponential demand was expected, and there were doubts as to the capacity for large-
scale production of BCOs. The production of insectaries requires suitable planning, and the
experience acquired over previous cycles is therefore essential.
Prior to 2007, the demand for BCOs from the entities that participated in the control
program of insect vectors of viruses in horticultural crops in the province of Almería was
practically negligible. For a pepper crop surface area of 330 hectares under biological
control, in the 2006/07 season (plan for control of insect vectors), 13-million-minute pirate
bugs (Orius laeviegatus) were required to be released. If biological control methods were
to be implemented in 50% of the pepper crop surface, demand for Orius would run
to 164 million insects, which would have to be produced in few months. Prior to the
2006/07 cycle, production, and marketing of BCOs was in the hands of a few enterprises.
Experience gained elsewhere with advanced IPM programs showed that although the
periodic release of natural enemies has often been considered the most suitable of the three
approaches to biological control in annual cropping systems [16], in fact there are few
examples of the successful use of commercially produced natural enemies in field and row
crops. Possible reasons for the lack of success include the high cost of commercial natural
enemy production, economic feasibility, and the misconception that mass-reared natural
enemies can be used as insecticides.
It was hoped that public subsidies for the purchase of BCOs would lead the powerful
auxiliary industry in Almería to seize the opportunity to exploit a new market. The subsidy
policy was expected to offset the initial outlay which had been one of the factors in the
failure of other experiences involving the release of BCOs. The influx of new enterprises
and the involvement of supplies companies were to play a fundamental role in balancing
supply and demand, and therefore, in adjusting prices accordingly.

2.6. Maintaining the System over a Minimum Number of Cycles

This was necessary in order that the implantation should prove efficient and sustain-
able over time. Attaining a considerable crop surface area under biological control alone
was not enough. It was important to maintain it to encourage other growers to join the
movement. In such a limited production area, based principally on family farming, the best
marketing ploy is undoubtedly “word of mouth”. Once the control plans were running
successfully, it was hoped that other growers would embrace this new form of pest control.
In principle, the European Commission’s authorization for subsidies on the purchase of
BCOs would extend to 2011, and so this was the initial horizon that was contemplated.
Subsidies were applied for on an annual basis and growers committed themselves to em-
ploying biological control methods on all crop cycles during the respective year. As regards
subsidies to Integrated Production Groups to obtain quality production and contract PCAs,
the duration was to be limited to five years, terminating at the end of the 2011/12 season.
Unlike the subsidies for the purchase of BCOs of insect vectors, the IPG subsidies required
a 5-year commitment, and if any group should not fulfill their obligation, all quantities
received were to be repaid.

3. Results: The Success of “Almería’s Green Pest Management Revolution”

3.1. Establishment of Homogeneous Crop Areas through Growers Associations
The data shown reflect the results of the plan for subsidies for the control of insect vec-
tors of viruses in protected horticultural crops in the province of Almería over the 2007/08,
2008/09, 2009/10 and 2010/11 seasons. A total of 77 grower associations from three areas of
the province took part. The municipality of El Ejido accounted for 32 enterprises (41.56%)
and 42.57% of the greenhouse crop area.
Thirty-five of the 77 entities that benefited from the subsidies were producer associa-
tions (P.A.), 24 were Agricultural Processing Companies (S.A.T.) and 17 were Andalusian
Cooperative Societies (A.C.S.). It should be mentioned that 19 of the 35 producer associa-
tions were set up around suppliers who committed themselves fully to the marketing of

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Agronomy 2022, 12, 619 6 of 13

BCOs to offset the fall in sales of phytosanitary products and offer a full range of products
for pest control. This fact is significant in that the priority of all their PCAs shifted from
recommending insecticides and acaricides to promoting sales of BCOs. This avoided, to
a great degree, the danger that some PCAs affiliated to agricultural product suppliers
would have a conflict of interest in recommending biological control methods. While these
suppliers affiliated PCAs provide pest monitoring and consulting services for free, their
employers stay in business by selling pest control products.

3.2. Pest Control Adviser (PCAs) Training

Between 2007 and 2008, 603 PCAs were trained in biological control, and the IFAPA
ran 25 specific courses in Almería in which 335 PCAs participated directly in the pro-
gram for the control of insect vectors (Table 1). These PCAs were therefore registered by
the producer associations on the official government registry for subsequent monitoring
and control. They included 298 university Technical Agricultural Engineers (degree hold-
ers), 27 Agronomic Engineers (Master graduates), 7 technicians qualified in specialized
professional training and 3 Master graduates in Biological Science.

Table 1. IFAPA IPM courses held in the La Mojonera installations (Almería).

Year Nº Courses Qualified Participants

2007 16 389
2008 9 214
2009 3 77
2010 2 38
2011 1 30

3.3. Scope of the PCAs

The PCAs who took part in the program were contracted in different ways, depending
on the social aims of the association in question. In the producer associations (21 APC,
12 ACS and 7 PA), whose aim is the production and sale of horticultural produce, 82.58%
of the PCAs were already employed by them (Table 2). However, those associations
that were created around companies, whose aim is to sell agricultural supplies or to
sell the horticultural produce (Auctions), only employed directly 29.03% and 8.57% of
the technicians, respectively, outsourcing this service for the most part. In Almería, the
determining factor regarding the type of PCA who provides services is not the size of the
farm, but rather the aim of the producer association to which he/she belongs.

Table 2. Chart reflecting the human resources used in the provision of technical assessment between
the period 2007–2011.

Social Aim of the Enterprise (Origin) PCAs % Crop Surface Hectares/PCA

Employees 82.58% 54.68
(a) Production & sales. Horticultural produce
Outsourced 17.42% 42.65
% a/(a + b + c) a = 539 58.61%
Employees 29.03% 49.15
(b) Sales. Agricultural supplies
Outsourced 70.97% 43.53
% b/(a + b + c) b = 349 32.51%
Employees 8.57% 30.35
(c) Sales. Horticultural produce (Auctions)
Outsourced 91.43% 37.04
% c/(a + b + c) c = 118 8.88%

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Agronomy 2022, 12, 619 7 of 13

3.4. Control and Monitoring

The Department of Agriculture and Fisheries for the Regional Government of An-
dalusia set up a field-sampling plan that would involve 100% of entities benefiting from
subsidies, with samples being taken from at least 10% of the surface area for which the
subsidies were awarded. Visits to the farms were carried out by technicians from the
administration in the compulsory presence of the grower and the PCA. The farm’s technical
characteristics were checked, as were the data annotated in the compulsory logbook [17],
to ascertain that the control plan was being correctly followed. All PCAs were obliged to
register their intervention instructions (release of BCOs, phytosanitary treatments, etc.).
This procedure prevented growers with independent PCAs from receiving more
frequent visits and written status reports than growers who used supplier-affiliated PCAs.
It also prevented some growers from making use of more than one PCA in the hope of
getting better technical advice, as has happened in California in the cultivation of cotton
where 50% of farmers have 2 or more PCAs [18]. Though in California the type of PCA
appears to play an important role, this is not the case in Almería.
The in situ field monitoring was complemented with data collection via the TRIANA
software program, in which each PCA had to note the data from the field logbook over
4 consecutive winter seasons.
These two control mechanisms most likely contributed greatly to the success of the
implementation of biocontrol, suitable use of BCOs was ensured to control pests, while at
the same time, phytosanitary applications were kept to a minimum, and always in situations
which were in no way to the detriment of the BCOs. The monitoring also allowed the
authorities to determine an overall decrease in the presence and incidence of the main pests
for horticultural crops: whitefly, thrips, aphids (all of which are insect vectors of viruses)
and caterpillars. In pepper crops, this drop in incidence was particularly noteworthy. In
2007/08, thrips were found to be present in over 30% of plants, with 10% affected by TSWV
in some areas and up to 9% of fruit affected [19]. However, during just three crop seasons,
these values fell to 17.3%, 0.9% and 1.1%, respectively. The authors of [20] found that in
field and row production, the annual nature of the crops, their greater level of seasonal
disturbance, and the highly dispersive nature of many of the associated pests, are important
barriers for the establishment and impact of introduced natural enemies. Nevertheless,
here it has been shown that the same does not hold true for greenhouse crops. Despite
the brevity of the crop cycles, the BCOs not only survived but their populations increased
exponentially and held the main pests in check.
The supervision procedures also provided evidence on other crops, namely water-
melon and melon, especially in the second crop cycle, showing a decrease in the number
of releases and in the doses of BCO applications, possibly due to a fall in the amount of
aid from the 2009/10 season onwards, among other reasons. The efficiency of the system
implemented allowed rapid action to be taken, setting minimum compulsory doses for the
control of insect vectors of viruses from September 2010 [21]. Correct application of these
minimum doses was a condition sine qua non for growers to be awarded subsidies (Table 3).

Table 3. Pests to be controlled and minimum doses of BCO releases (no. BCOs/m2 ) for each crop.

Pest Pepper Tomato Eggplant Green Bean

(a) Whitefly 1 (50) 4 (0.5) 1 (50) + 4 (0.5) 1 (25)
(b) Aphids 2 (0.15) - 2 (0.1) 2 (0.25)
(c) Thrips 1 (50) + 3 (2) 4 (0.5) 1 (50) + 4 (0.5) 1 (25) + 5 (50)
Pest Zucchini Cucumber Melon Watermelon
(a) Whitefly 1 (25) 1 (50) 1 (25) 1 (25)
(b) Aphids 2 (0.2) 2 (0.25) 2 (0.2) 2 (0.2)
(c) Thrips 1 (25) 1 (50) + 5 (100) 1 (25) 1 (25)
PEST: (a) Whitefly: Bemisia tabaci and Trialeurodes vaporariorum; (b) Aphids: Aphis craccivora, Aphis gossypii, Aula-
corthum solani, Macrosiphum euphorbiae, Myzus persicae; (c) Thrips: Frankliniella occidentalis. BCOs: (1) Amblyseius
swirskii; (2) Aphidius colemani; (3) Orius laevigatus; (4) Nesidiocoris tenuis; (5) Amblyseius cucumeris.

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Agronomy 2022, 12, 619 8 of 13

However, in certain exceptional circumstances, lower doses were allowed on qualified

technical advice. It should also be pointed out that certain growers opted for placing among
their plants pruned branches from other greenhouses into which BCOs had already been
released, thus establishing high populations of these beneficial insects in the new crops.
“Interplanting” is a technique which fosters the presence of BCOs, transferring them from
autumn-cycle to spring-cycle crops.
The release of the BCOs until reaching the dose indicated in Table 3 was generally
carried out in at least two moments. For the control of whiteflies, the most used OCBs
were the predatory bug Nesidiocoris tenuis (Hemiptera: Miridae) and the predatory mite
Amblyseius swirskii (Acari: Phytoseiidae), which can be used alone or in combination
depending on the crop, as shown in Table 3. For the control of thrips, in addition to the
two OCBs indicated above, the predatory bug Orius laevigatus (Hemiptera: Anthocoridae)
and the predatory mite Amblyseius cucumeris (Acari: Phytoseiidae), were used. The most
common combinations for trips control according to crops are shown in Table 3. The
predatory bugs were released on the plant canopy or by using an application box hung on
the plant and the mites were released mainly in slow release hanging sachets. The control
of aphids by the parasitic wasp Aphidius colemani (Hymenoptera: Aphidiinae) was carried
out by using banker plant prior to the detection of aphids in the crop, based on introducing
cereal aphids into a greenhouse on cereal plants and A. colemani.
Despite these and other actions intended to minimize abundant releases of BCOs, the
demand for products was very high, and as a result, the number of enterprises involved in
the commercialization of BCOs increased rapidly, reaching a plateau in 2011/12.

3.5. Production Capacity and Price of BCOs

At present, over 70% of the companies marketing the main BCO products registered in
Spain for horticultural crops (A. swirskii, A. colemani; O. laevigatus, N. tenuis and A. cucumeris)
are in Almería (16 of 23), and the 118 products they offer represent 88% of the total available
on the market. A further indication of the importance of Almería in this market is the
fact that 9 of the 10 companies with the highest number of registered products have their
Spanish headquarters in this province (Table 4).
The rapid growth of enterprises in this market allowed a downward trend in costs to
the grower due to the greater competition for distribution to a limited crop surface area.
However, the adjustment in the doses of BCO releases constituted an additional factor in
the reduction of costs. This was made possible by the decrease and gradual elimination of
phytosanitary residues in the greenhouses, the greater know-how acquired, the perfection
of techniques applied and the fall in incidence of crop pests with regard to 2007/08. To
illustrate this final factor, in 2007/08, it was necessary to release 4 Orius laviegatus/m2 to
control Frankliniella occidentalis in pepper crops, whereas in 2010/11 many greenhouses
were able to achieve this aim with only 1.7 Orius/m2 .
According to publications of the Research Institute of the Cajamar Foundation [22]
from biological control’s arrival on the scene in 2007/08 to the 2012/13 season, pest control
cost (chemical control + biological control) fell by 32.16%.

Table 4. Companies marketing BCOs products registered in Spain in 2022. Source: MAPA, [23].

No. BCOs Products Province/Country

Enterprise
1 2 3 4 5
Agrinature Producciones Agrícolas, S.L. 1 1 1 1 Almería (Spain)
Agrobio, S.L. 1 2 2 1 1 Almería (Spain)
Agrocontrol 2007, S.L. 1 1 1 1 Almería (Spain)
Agroquímicos Los Triviños, S.L 1 Murcia (Spain)
Bgreen Biological System, S.L. 1 1 1 1 1 Almería (Spain)
BICHELOS, Control Biológico S.L. 1 1 1 Valencia (Spain)

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Agronomy 2022, 12, 619 9 of 13

Table 4. Cont.

No. BCOs Products Province/Country

Enterprise
1 2 3 4 5
Biobest Sistemas Biológicos, S.L. 5 4 3 1 4 Almería (Spain)
Biocolor Iberia, S.L. 1 1 1 1 Almería (Spain)
Biocontrol Del Mediterráneo, S.L. 1 Alicante (Spain)
Bioline Agrosciences Limited Iberia 1 3 1 1 1 Almería (Spain)
Bioplanet Ibérica, S.L. 5 4 2 2 3 Almería (Spain)
Biosur Productos Agrícolas, S.L.U. 3 2 1 1 2 Almería (Spain)
Certis Europe, B.V. 1 1 1 1 2 Alicante (Spain)
Entonova, S.L. 1 1 1 Almería (Spain)
Insectaria, S.L. 1 1 La Rioja (Spain)
Insectos Med, S.L. 1 1 1 Almería (Spain)
Koppert Biological Systems, S.L. 4 3 2 2 3 Almería (Spain)
Mip System Agro, S.L. 4 2 2 2 3 Almería (Spain)
Plant-E Productos Naturales S.L 1 1 Navarra (Spain)
Provi Agricola, S.L. 1 1 1 Almería (Spain)
Saniveg, S.L. 1 1 2 1 1 Almería (Spain)
Surinver El Grupo 1 Alicante (Spain)
Verde Ibérica, S.C.A. 1 1 1 Almería (Spain)
Total 32 29 28 24 21 Almería (Spain)
BCOs: (1) Amblyseius swirskii; (2) Aphidius colemani; (3) Orius laevigatus; (4) Nesidiocoris tenuis; (5) Amblyseius cucumeris.

Table 5 provides an overview of the annual production costs of a typical plastic

greenhouse small holding expressed in euros/ha. Applying these data to the current total
greenhouse surface area of 29,500 hectares, the growers’ savings due to the introduction of
biological pest control over the period in question would be over 43 million euros.

Table 5. Annual production costs by items in Almerian greenhouses, in euros/ha in 2006–2013.

Source: [22].

Expense Item 2006/07 2007/08 2008/09 2009/10 2010/11 2011/12 2012/13

Water 1359 1416 1420 1379 1429 1448 1463
Biological control 0 1029 1092 908 964 807 785
Pesticide control 4565 2295 2363 2349 2339 2342 2312
Energy consumption 1121 1197 1201 1208 1223 1235 1280
Fertilizers 3744 5136 5998 3911 3973 3925 3929
Labor 20,466 21,223 21,902 22,077 22,541 22,744 22,812
Seeds and seedlings 4186 4353 4497 4623 4716 4892 4991
Services 5725 6351 4476 4079 4201 4179 4185
Total 41,166 43,000 42,949 40,534 41,386 41,572 41,757

In 2006/07, expenditure on pest and pathogen control was 100% on chemical methods,
and after that date, expenditure is divided between chemical and biological techniques.
Pesticide control methods, aimed principally at pathogen control (especially fungi), fluc-
tuate slightly from 2007/08 onwards, whereas the cost of biological control methods fell
steadily over the same period, thus reducing growers’ expenditure on pest control.

3.6. Maintaining the System over a Minimum Number of Crop Seasons to Ensure Its
Stable Implementation
Public subsidies were originally planned to be maintained over 4 agricultural years
and to cover 50% of the purchase costs of BCOs. However, this plan fell through with the
advent of the international recession which hit Spain in 2008 and the subsequent banking
crisis in 2010. Public funds were no longer available to uphold the plan, and as a result,
subsidies dropped in the 2009/10 and 2010/11 crop seasons to cover less than 25% of BCO
purchases. This entailed the risk that some associations might opt out of the control plans

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Agronomy 2022, 12, 619 10 of 13

and that other might not become involved. However, the other line of subsidies aimed at
IPGs was maintained over the planned 5-year program, though in this case, the amounts
involved were considerably lower.
Table 6 outlines the public subsidies paid for the biological control of protected horticul-
tural crops in the province of Almería. A total of 31.5 million euros was destined to IPGs and
to the purchase of BCOs over 5 crop seasons. Between 2007/08 and 2011/12 campaigns,
the average annual subsidy per hectare for biological control was 450.41 €, 89.4% was
dedicated for purchase of OCBs and 10.6% for contracting PCAs.

Table 6. Public subsidies paid for the biological control of protected horticultural crops in Almería.

Public Subsidies (€)

Crop Season BCOs IPGs Total
2007/08 10,719,014 1,229,618 11,948,632
2008/09 10,891,014 831,357 11,722,371
2009/10 3,728,485 735,986 4,464,471
2010/11 2,382,899 497,228 2,880,127
2011/12 0 494,484 494,484
Total 27,721,412 3,788,673 31,510,085

There is a clear drop in demand for subsidies for the purchase of BCOs from 2009/10
onwards. It would be a mistake to attribute this to a loss of interest in biological control.
While it is true that certain growers’ associations forewent subsidies due to the fact that the
aid received did not offset expenses in administrative tasks, they did in fact continue to
employ biological control organisms for pest control.
It is quite remarkable that the first two years proved sufficient to convince those
growers who undertook biological control of the worth of this method, as Table 7 illustrates.
It shows the percentage of greenhouse crop area in Almería in which biological control
methods were implemented over 8 agricultural seasons between 2005 and 2013, detailing
the number of hectares that received subsidies for the purchase of BCOs (against insect
vectors) on the one hand, and for contracting PCAs on the other (IPGs).

Table 7. Evolution of greenhouse crop area in Almería with biological control since 2005/06
to 2012/13.

Area Receiving Area Receiving Aid

Biological Control Total Crop Area % Biological Control
Crop Season Aid for Purchase for Contracting
Area (ha) (ha) Total/Total Crop Area
of BCOs (ha) PCAs (ha)
2005/06 129 129 129 40,233 0.32%
2006/07 756 756 756 39,583 1.91%
2007/08 10,447 9239 8281 38,987 26.80%
2008/09 18,807 15,541 17,853 39,251 47.92%
2009/10 19,525 11,141 17.621 39,087 49.95%
2010/11 20,081 8135 14.383 37,224 53.95%
2011/12 20,754 0 11.432 39,599 52.41%
2012/13 25,000 0 7.251 44,114 56.67%

Table 7 clearly reflects the exponential increase in biological control methods immedi-
ately after the food safety alert, coinciding with the offer of public aid. The initial sharp
increase in crop area treated with these methods was followed by less marked increments
in subsequent seasons, but with a steady upward trend.
In 2007/08, almost 90% of the crop area that was treated with biological control
methods came under the umbrella of the aid plan for the purchase of BCOs, which acted as
a driver to change in pest control systems. Two years later, over 40% of the crop surface
under biological control received no subsidies, and this period coincided with the fall in
the subsidies offered. Unlike the subsidies for the purchase of BCOs, those destined for

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Agronomy 2022, 12, 619 11 of 13

IPGs fell less sharply. In fact, this aid remained constant due to the 5-year commitment to
the plan demanded of the growers at the outset.
BCOs can currently be considered the “conventional” pest control method in Almería.
In the last eight years (2013–14 to 2020–21), the average area dedicated to biological control
has been 25,472 ± 1262 hectares although with slight interannual modifications. Their
efficiency in keeping pests in check and their relatively low cost (considerably less than
insecticides and acaricides) have won over growers, who have embraced this method
irrespective of the final market destination of their produce and of the quality certifications
they use.
Two factors have contributed to solving the occasional problems that have arisen in
connection with biological control in greenhouses in Almería: on the one hand, the mean
size of farms in Almería means that growers are well aware of the phytosanitary conditions
of their crops, and on the other, social, technical and business factors have combined to
maintain a high level of interest and commitment to this pest control method. As a result,
the planning and management of BCOs in IPM programs of greenhouse horticultural
crops have become universal standards for the whole province. This uniformity within the
greenhouses of the province constitutes a barrier to the arrival of major populations of new
pests, and therefore provides the system with the stability which helps to maintain it.

4. Conclusions
It can be concluded from these results that, unlike many programs of public subsidies
which involve long-term expenditure, the aid in question took advantage of the socioeco-
nomic situation following the food safety alert due to the presence of isofenphos-methyl
residues in exported fresh produce. The program led to substantial economic savings and
met its objectives swiftly, achieving excellent results in terms of removing most of the
pesticides used in the “conventional” production system. Similar results using IPM were
obtained in California for over 35 years [24]. As such, they illustrate the importance of
rapid regulation and intervention if public funds are to make the most of circumstances
and benefit society as a whole, even when, as in this case, the initial scenario appears to
be unfavorable.
This can be considered a pioneering experience which has shown that at a mean cost
of 6.3 million euros a year (equivalent to 0.36% of the total value of horticultural production
in the province of Almería) over a 5-year period, it has proved possible to promote a policy
change in pest control methods. This has contributed to the stability of Almería’s produce
on national and international markets, improving its image and setting an example that has
become known on an international scale as “Almería’s green pest management revolution”.
Juntti and Downward [5] refer to Almeria’s horticultural production innovations,
such as IPM and water efficient irrigation systems, that have been advanced through
the remarkable “capillary system” formed by marketing organizations and agronomists
working closely with auxiliary enterprises and farmers.
“Almeria’s green pest management revolution” was the answer of this “capillary
system” with the Regional Administration support to a food safety alert. Although there
are other environmental challenges awaiting to be solved in Almería like in most of the
intensive production systems worldwide, but even if IPM is seen as stemming from mar-
ket demand, it is an important aspect of “greening” the industry and addressing health
concerns of both consumers and producers.

Author Contributions: M.M.A. and F.D. conceived and designed the article; M.M.A. and M.S.
performed bibliographic research and analyzed the data; M.M.A., F.D. and M.S. wrote the paper. All
authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.

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Agronomy 2022, 12, 619 12 of 13

Data Availability Statement: The data has been included in the manuscript. No other data to report.
Conflicts of Interest: The authors declare no conflict of interest.

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