**Implementation and Adoption of Integrated Pest Management Approaches in Latin America: Challenges and Potential**

Yelitza Colmenárez, Carlos Vásquez, Natália Corniani and Javier Franco

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/64098

#### **Abstract**

cause those control methods are not very effective compared to chemicals or not much re‐ search has been done to improve that method. The book focuses on some of those pest management methods that have been employed worldwide highlighting the major problem and issues and possible attempts to identify promising lines and directions for future re‐ search and implementation. Many researchers have contributed to the publication of this book. We aimed to compile information from a wide diversity of sources into a single vol‐ ume in forming this book. We begin with historical review of IPM concepts, strategies, and some experiences in applications of IPMS in Latin America. The rest of the six chapters offer information on pest management approaches alternative to chemicals. The chapters include pest control in organic agricultural system through preventive and curative measures; the use of entomopathogenic nematodes in pest management; advances in production, storage, application techniques, genetic improvement, and safety of entomopathogenic and mollus‐ coparasitic nematodes, which are important parasites of many insect and mollusks, respec‐ tively; review of performance of popular insect pheromones used in Vietnam; semiochemicals use in IPM environmentally compatible strategies to reduce pest population under economic threshold levels; and management of agriculture pests using detergents and

The inclusion of different methods for pest management globally will make this book of sig‐ nificance to researchers, scientists, graduate students, growers, policy makers, and other professionals who can make use of compiled information from this book. Environment safe‐ ty is one of the top concerns these days with growers either looking for or forced by policy makers toward more environment-friendly options than ever before. This book is not in‐ tended to provide all the alternative pest management methods but to provide many of the common ones evaluated by researchers and with feasibility over grower's farm. We hope that this book will continue to meet the expectations and needs of anyone interested in the

**Harsimran Kaur Gill, PhD,**

Cornell University, Ithaca, NY, USA

**Gaurav Goyal, PhD,** Monsanto Company, St. Louis, MO, USA

soaps as parts of IPM scheme.

VIII Preface

topic to learn more and understand different IPM options.

Latin American countries present diverse agricultural systems, ranging from the subsistence agriculture in common property lands to large highly mechanized estates that produce crops for export. Despite this diversity, the adoption of integrated pest management (IPM) is commonly based on reducing the negative effect of pesticides on consumer health and on the environment. In most of Latin American countries, the agricultural sector is characterized by poor infrastructure in research and extension systems, a public sector with limited human resources that limits the dissemination of information and provides inappropriate credit and subsidy schemes, all of these have influenced negatively on the possibility of the success of IPM programs. Thus, some innovative alternatives have emerged from concerning public and private initiatives. In this regard, the Plantwise approach, as a framework for action, is to strengthen the capacity of agricultural institutions and organizations to establish more effective and sustaina‐ ble national plant health systems. Plantwise is an innovative global program led by the Centre for Agriculture and Biosciences International (CABI), which aims to contribute to increased food security, alleviated poverty, and improved livelihoods by enabling male and female farmers around the world to lose less, produce more, and improve the quality of their crops. Strengthening plant health systems removes barriers to make accessible to farmers sustainable approaches for pest control. In this chapter, we include some historical review of IPM concepts, strategies, and some experiences in application of IPM in Latin America. Also we discuss the potential and challenges for implementation and adop‐ tion of IPM practices and the ways how Plantwise has engaged with the key partners in the different countries where the program is being implemented, promoting the implementation of IPM approaches in order to improve agriculture systems, mainly those from subsistence agriculture, in Latin America.

© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

**Keywords:** integrated pest management, Latin America, Plantwise, plant health sys‐ tems

## **1. Introduction**

One of the main challenges of the agriculture is to provide increasing supplies of food for a growing population with the increase in efficiency in the use of inputs and reduction of the environmental impacts from production [1], where both the ecological and economic dimen‐ sions are considered [2]. In this context, Yudulmen et al. [3] stated that the efficient manage‐ ment of insect pests should have a high priority given that insects still take about 15% of potential global crop yields [3]. However, the use of pesticides as one of the major control strategy adds economic and environmental costs to the food production equation [4].

The Integrated Control Concept (ICC) created by Stern [5] gave rise to the idea of the integrated pest management (IPM) and it has been a scientifically accepted "paradigm" for pest man‐ agement worldwide for more than 50 years. In the context of the ICC, a fundamental element is to understand that any control system imposed on a given pest in a given crop has conse‐ quences for the management of other pests and crops in the ecosystem [6]. Thus, the IPM is a multitactic nature approach, including aspects related to host plant (such as plant nutrition, plant physiology, and plant resistance) and the economic aspects.

Considering the pyramidal conception of an IPM program designed for whitefly management (**Figure 1**), it is possible to generalize that model to other pests. In this regard, we could state that avoidance constitutes the basis of a pest management program, although some might reside on more than one level. For example, when facing a pest outbreak, decisions could be made based upon the upper two levels of the pyramid.

Later, Kogan [8] defined IPM as a decision support system for the selection and use of pest control tactics, singly or harmoniously coordinated into a management strategy, based on cost/

**Figure 1.** Conceptual diagram of whitefly IPM, depicting three keys to whitefly management (left): sampling, effective chemical use, and avoidance. Avoidance is subdivided among three interrelated areas: area-wide impact, exploitation of pest biology and ecology, and crop management (from: [7]).

benefit analyses that take into account the interests of and impacts on producers, society, and the environment. According to Rodríguez and Niemeyer [9], this definition inherently considers the existence of ecological and economic thresholds, the need to adopt the socioe‐ cosystem as a management unit, the existence of a broad number of IPM tools including the rational use of chemical pesticides, and the requirement for interdisciplinary systems ap‐ proach, particularly since certain control measures may produce unexpected and undesirable effects. As complement to the classical definition, the United States Department of Agriculture has defined the IPM as a long-standing, science-based, decision-making process that identifies and reduces risks from pests and pest management–related strategies [10].

Additionally, Naranjo and Ellsworth [6] discussed the evolution of IPM concepts built on the original four components: thresholds for determining the need for control, sampling to determine critical densities, understanding and conserving the biological control capacity in the system, and the use of selective insecticides or selective application methods, when needed, to augment biological control.

## **2. Plant protection techniques used in IPM**

**Keywords:** integrated pest management, Latin America, Plantwise, plant health sys‐

One of the main challenges of the agriculture is to provide increasing supplies of food for a growing population with the increase in efficiency in the use of inputs and reduction of the environmental impacts from production [1], where both the ecological and economic dimen‐ sions are considered [2]. In this context, Yudulmen et al. [3] stated that the efficient manage‐ ment of insect pests should have a high priority given that insects still take about 15% of potential global crop yields [3]. However, the use of pesticides as one of the major control strategy adds

The Integrated Control Concept (ICC) created by Stern [5] gave rise to the idea of the integrated pest management (IPM) and it has been a scientifically accepted "paradigm" for pest man‐ agement worldwide for more than 50 years. In the context of the ICC, a fundamental element is to understand that any control system imposed on a given pest in a given crop has conse‐ quences for the management of other pests and crops in the ecosystem [6]. Thus, the IPM is a multitactic nature approach, including aspects related to host plant (such as plant nutrition,

Considering the pyramidal conception of an IPM program designed for whitefly management (**Figure 1**), it is possible to generalize that model to other pests. In this regard, we could state that avoidance constitutes the basis of a pest management program, although some might reside on more than one level. For example, when facing a pest outbreak, decisions could be

Later, Kogan [8] defined IPM as a decision support system for the selection and use of pest control tactics, singly or harmoniously coordinated into a management strategy, based on cost/

**Figure 1.** Conceptual diagram of whitefly IPM, depicting three keys to whitefly management (left): sampling, effective chemical use, and avoidance. Avoidance is subdivided among three interrelated areas: area-wide impact, exploitation

economic and environmental costs to the food production equation [4].

2 Integrated Pest Management (IPM): Environmentally Sound Pest Management

plant physiology, and plant resistance) and the economic aspects.

made based upon the upper two levels of the pyramid.

of pest biology and ecology, and crop management (from: [7]).

tems

**1. Introduction**

IPM relies mainly on natural mortality factors such as natural enemies and weather seeking out tactics that disrupt these factors as little as possible [11]. In a broader sense, it includes all plant protection measures that help to prevent or manage pests, whether through general crop management practices such as rotation, or of cultural, physical, biological, or chemical nature. When pesticides are applied, two crucial items to be considered are determining when pesticides actually need to be used and the choice of chemicals should be made with consid‐ eration of compatibility with nonchemical methods (e.g., natural predators), pest population level, and resistance management, products' profiles. In an IPM context, these decisions are heavily based on an important step such as the biological monitoring (also referred as 'scouting'), which consists of sampling procedures designed to estimate the stages and population densities of both pests and beneficial organisms [12]. Unfortunately, biological monitoring is a very knowledge-intensive procedure and requires highly trained individuals to obtain reliable data and consequently ensure the success of the program. On the other hand, since both pest populations and the growth and development of crop plants are governed by environmental parameters, monitoring environmental conditions should be another core component of IPM [12].

For all that, crop production is dynamic; the decisions on pest management measures should be taken at farm level based on a wide variety of instruments, such as qualified advisers' recommendations, alert services and infestation forecast, research results, experience, and threshold values. However, the actual techniques to be included in an IPM approach on-farm will vary not only between crops but also within the same crop grown in different geographical locations, or between years, depending on pest pressure, weather patterns, crop rotation, and other factors, as well as availability of tools and resources [13]. All these should consider economic aspects, trying to allocate scarce resources (capital or labour) [14].

## **3. Biological control and IPM**

Biological control has been a valuable tactic in pest management programs around the world for many years, but has undergone a resurgence in recent decades that parallels the develop‐ ment of IPM as an accepted practice for pest management [15]. Since natural enemies are often key factors in the dynamics of pests, biological control should be the cornerstone of IPM practices [16]. However, when implementing an integrated pest management programs, special care should be taken in what specific tactics could be used since they do not act independently of one another. This is especially true for biological control since the agents of insect biological control are susceptible to environmental factors, such as pesticides, cultural control, mechanical and physical control, and transgenic crops [15].

However, both biological control and IPM faced some obstacles originating from the lack of biological data and the lack of knowledge to develop economically, environmentally, and socially sound crops and animal production systems [17].


Implementation and Adoption of Integrated Pest Management Approaches in Latin America: Challenges and Potential http://dx.doi.org/10.5772/64098 5

**3. Biological control and IPM**

**Insect or mite species**

*Anisolabis maritime* (Dermaptera: Anisolabididae)

*Chelisoches morio* (Dermaptera: Chelisochidae)

*Euborellia annulipes* (Dermaptera: Anisolabididae)

*Platymeris laevicollis* (Hemiptera: Reduviidae)

*Xylocorus galactinus* (Hemiptera: Anthocoridae)

*Xanthopygus cognatus* (Coleoptera: Staphylinidae)

*Sarcophaga fuscicauda* (Diptera: Sarcophagidae)

*Billea rhynchoporae* (Diptera: Tachinidae)

*Megaselia scalaris* (Diptera: Phoridae)

**Insects**

Biological control has been a valuable tactic in pest management programs around the world for many years, but has undergone a resurgence in recent decades that parallels the develop‐ ment of IPM as an accepted practice for pest management [15]. Since natural enemies are often key factors in the dynamics of pests, biological control should be the cornerstone of IPM practices [16]. However, when implementing an integrated pest management programs, special care should be taken in what specific tactics could be used since they do not act independently of one another. This is especially true for biological control since the agents of insect biological control are susceptible to environmental factors, such as pesticides, cultural

However, both biological control and IPM faced some obstacles originating from the lack of biological data and the lack of knowledge to develop economically, environmentally, and

> *Rhynchophorus* **species**

Eggs, larvae and pupae *R. ferrugineus* Saudi Arabia

Eggs and larvae *R. ferrugineus* India

Eggs *R. ferrugineus* Italy

Unknown *R. ferrugineus* Sri Lanka

Eggs and larvae *R. palmarum* Ecuador

Adults *R. ferrugineus* India

Pupae *R. palmarum* Brazil

Pupae *R. ferrugineus* Italy

*R. ferrugineus* Saudi Arabia

**Location**

control, mechanical and physical control, and transgenic crops [15].

**Developmental stage**

Eggs, larvae and

 *B. maritima* Pupae *R. ferrugineus* Italy *B. menezesi* Pupae *R. palmarum* Brazil

*Scolia erratica* Larvae *R. ferrugineus* Malaysia

pupae

socially sound crops and animal production systems [17].

4 Integrated Pest Management (IPM): Environmentally Sound Pest Management

**attacked**


**Table 1.** List of insects and mites as natural enemies of *Rhynchophorus* spp. worldwide (from Mazza et al. [19])

The red palm weevil, *Rhynchophorus ferrugineus* (Olivier) (Coleoptera: Curculionidae), is a wellknown problem for the damage it causes to coconuts (*Cocos nucifera*) grown in plantations so that much research has been conducted with a strong emphasis on the development of IPM based on pheromone traps and biological control rather than insecticides [18]. Thus, these authors stated that the prospects for the development of a biological control component for an integrated management strategy are good; however, the establishment and effectiveness of the biological control may depend on the intensity of management practices in palm (*Phoenix dactylifera*) plantations. In addition, there is also scope for the development of biopesticides to replace directly or to reduce the use of chemical pesticides. In this regard, Mazza et al. [19] have showed a list of insects and mites as natural enemies of *R. ferrugineus* worldwide (**Table 1**). As shown, most diverse insect groups belong to Diptera (4 spp.) and Dermaptera (3 spp.), while in the group of mites, Mesostigmata are the dominant species group. Regarding geographical distribution, most of the studies have been conducted in Egypt and in some countries from Asia (India, Indonesia, Malaysia, Philippines, Saudi Arabia, Sri Lanka) and most discrete number of studies in Latin America, with reports from Brazil, Costa Rica, and Ecuador. This fact reveals the limited information about natural enemies in Latin America, thus making difficult to establish IPM programs with a predictable success opportunity. Thus, more studies concerning the biological parameters of the pests and their natural enemies are required in this geographical area.

Another successfully pest control program, known as the Moscamed Program, was developed in Mexico with participation of Mexican and Guatemalan authorities and the USDA in collaboration with the FAO and International Atomic Energy Authority (IAEA) to manage the Mediterranean fruit fly (*Ceratitis capitata*). The Moscamed program involved the application of insecticidal baits, mechanical and cultural control of hosts, restrictions on the movement of fruits and vegetables and the release of sterile males produced in the Moscamed plant at Metapa, Chiapas [20].

## **4. IPM in some Latin American countries: successful experiences**

In South America, IPM has been successfully implemented in Argentina [lucerne (*Medicago sativa*), citrus (*Citrus* sp.), soybean (*Glycine max*)], Brazil [(citrus (*Citrus* sp.), cotton (*Gossypi‐ um* sp.), soybean (*G. max*), sugarcane (*Saccharum officinarum*), tomato (*Solanum lycopersicum*), wheat (*Triticum vulgare*) and livestock)], Chile [wheat (*Triticum vulgare*)], Colombia [cotton (*Gossypium* sp.), ornamental (*Rosa* sp.), soybean (*G. max*), sugarcane (*Saccharum officinarum*), tomato (*Solanum lycopersicum*)], Paraguay [cotton (*Gossypium* sp.), soybean (*G. max*)], Peru [cotton (*Gossypium* sp.), sugarcane (*Saccharum officinarum*)], and Venezuela [cotton (*Gossypi‐ um* sp.), sugarcane (*Saccharum officinarum*)] [20].

## **4.1. Argentina**

Since the 1970s, Argentinian public institutions started to introduce farmers to IPM strategies by implementing a program of Extension and Technology Transfer focusing on the rational use of pesticides [21]. Although other IPM programs in soybeans, potatoes, and orchard crops have been developed, the cotton IPM program is being the oldest program. In this cotton IPM program, some strategies such as conservation of natural enemies, prevention of pesticide resistance, and cultural practices have been used.

At the beginning of the IPM program, farmers and technicians were trained for insect identi‐ fication and monitoring training, however, few growers put the knowledge into practice. As a consequence of the severe economic problems caused by the lack of control of *Alabama argillacea* (leafworm) in cotton (*Gossypium* sp.), a new technology transfer program was organized to teach IPM philosophy and thus the Cotton IPM Program reappeared [21]. According to these authors, after this fact, farmers understood that adequate insecticide use at the proper timing and at the correct dose reduces costs of production and provides more efficient crop management.

## **4.2. Brazil**

Ecuador. This fact reveals the limited information about natural enemies in Latin America, thus making difficult to establish IPM programs with a predictable success opportunity. Thus, more studies concerning the biological parameters of the pests and their natural enemies are

Another successfully pest control program, known as the Moscamed Program, was developed in Mexico with participation of Mexican and Guatemalan authorities and the USDA in collaboration with the FAO and International Atomic Energy Authority (IAEA) to manage the Mediterranean fruit fly (*Ceratitis capitata*). The Moscamed program involved the application of insecticidal baits, mechanical and cultural control of hosts, restrictions on the movement of fruits and vegetables and the release of sterile males produced in the Moscamed plant at

**4. IPM in some Latin American countries: successful experiences**

In South America, IPM has been successfully implemented in Argentina [lucerne (*Medicago sativa*), citrus (*Citrus* sp.), soybean (*Glycine max*)], Brazil [(citrus (*Citrus* sp.), cotton (*Gossypi‐ um* sp.), soybean (*G. max*), sugarcane (*Saccharum officinarum*), tomato (*Solanum lycopersicum*), wheat (*Triticum vulgare*) and livestock)], Chile [wheat (*Triticum vulgare*)], Colombia [cotton (*Gossypium* sp.), ornamental (*Rosa* sp.), soybean (*G. max*), sugarcane (*Saccharum officinarum*), tomato (*Solanum lycopersicum*)], Paraguay [cotton (*Gossypium* sp.), soybean (*G. max*)], Peru [cotton (*Gossypium* sp.), sugarcane (*Saccharum officinarum*)], and Venezuela [cotton (*Gossypi‐*

Since the 1970s, Argentinian public institutions started to introduce farmers to IPM strategies by implementing a program of Extension and Technology Transfer focusing on the rational use of pesticides [21]. Although other IPM programs in soybeans, potatoes, and orchard crops have been developed, the cotton IPM program is being the oldest program. In this cotton IPM program, some strategies such as conservation of natural enemies, prevention of pesticide

At the beginning of the IPM program, farmers and technicians were trained for insect identi‐ fication and monitoring training, however, few growers put the knowledge into practice. As a consequence of the severe economic problems caused by the lack of control of *Alabama argillacea* (leafworm) in cotton (*Gossypium* sp.), a new technology transfer program was organized to teach IPM philosophy and thus the Cotton IPM Program reappeared [21]. According to these authors, after this fact, farmers understood that adequate insecticide use at the proper timing and at the correct dose reduces costs of production and provides more

required in this geographical area.

6 Integrated Pest Management (IPM): Environmentally Sound Pest Management

*um* sp.), sugarcane (*Saccharum officinarum*)] [20].

resistance, and cultural practices have been used.

Metapa, Chiapas [20].

**4.1. Argentina**

efficient crop management.

Pesticide resistance, pest resurgence, worker poisoning, and ecological imbalances became apparent after indiscriminate pesticide usage in Brazil. In this regard, research was carried out on sampling methods on pests and natural enemies, use of threshold levels, and the correct timing for insecticide application [22]. Consequently, highly successful IPM programs were developed for several crops, including sugarcane, tomato, wheat, and soybean [23].

According to Hoffmann-Campo [23], most IPM programs in Brazil are characterized as follows:


IPM tactics must be made widely available to farmers through research institutions, official and private (farmer's cooperatives) extension services, and private companies. It is only by educating farmers on the importance and benefits of using IPM tactics for pest control that IPM programs can have a broader impact on agriculture in Latin America.

## **4.3. Ecuador**

Information about IPM in Ecuador is still scarce. However, some attempts have been done mostly in cocoa (*Theobroma cacao*), sugar cane (*Saccharum officinarum*), and vegetable crops. In Ecuador, about 500,000 ha are planted with cocoa cultivars 'CCN-51' and 'Nacional'. Defoli‐ ating insects belonging to Saturdinae and Megalopygidae (Order: Lepidoptera) commonly infest these cultivars. When high population levels are attained in adult plantations, control by broad-spectrum insecticides application is limited since populations of pollinators can be affected. Foliage application of biological pesticide *Bacillus thuringiensis* (New BT 2X at a rate 0.5 kg ha−1 or New BT 8L at 1 L ha−1) has showed promissory results in control of these lepidopteran pests [24].

Sugar cane: Program for the development of IPM from CINCAE (Centro de Investigación de la Caña de Azúcar del Ecuador) has proposed the following program [25]:


Finally, pilot units are settling down in fields where these compatible components are used according to the characteristics of each agroecosystem.

### **4.4. Mexico**

Mexico has a long history of proactive pest management, and more recently, IPM has become even more important as trade regulations that have begun to restrict the amounts of pesticide residue or insects that may be present on produce exported to the USA and Canada [26]. In order to maintain the extensive trade in fresh fruits and vegetables, these commodities must comply with strict regulations that are difficult to meet with conventional pest control methods, being IPM, in most of the cases, the only viable option for growers intending to export their products [26]. Several IPM programs have been successfully developed in Mexico.

IPM to control the tomato pinworm, *Keiferia lycopersicella* and other lepidopteran species in tomato has included careful scouting (primarily with pheromone traps from planting to harvesting), cultural control (including plowing under crop residues promptly after harvest‐ ing, cleaning drainage ditches and irrigation canals where alternate hosts grow, and estab‐ lishing a tomato-free period during summer or winter to break the cycle of tomato pinworm reproduction), mating disruption, use of selective insecticides, and biological control [23].

The parasitoid wasp, *Trichogramma pretiosum* is an egg parasitoid of tomato pinworm and it has been found occurring in several Mexican states (Chihuahua, Coahuila, Durango, Nuevo León, Sinaloa, Sonora, Tamaulipas, and Zacatecas) [27]. This parasitoid species has been released in combination with mating disruption [28]. Due to the overuse of insecticide applications, the tomato pinworm has developed resistance to conventional insecticides so that combined use of pheromones, biological control, and selective insecticides has reduced damage and number of insecticide applications [23].

IPM in cruciferous [the diamondback moth, *Plutella xylostella*]: effective cultural control methods included plowing to eliminate crop residue, and rotation with nonhost crops, careful inspection of nursery plants for diamondback moth eggs and larvae helped to prevent accidental introduction of diamondback moth into the field [29]. In addition, biological control has showed to have an important impact on the control of the diamondback moth, including use of native parasitoid species and the introduction of effective exotic species. In Puebla, a last-instar-parasitoid of diamondback moth, *Diadegma insulare*, has been found parasitizing 46.7% of *Plutella xylostella* larvae in cauliflower [30].

IPM of fruit flies [*Ceratitis capitata*]: according to Mota-Sánchez et al. [26], success of IPM of fruit flies relies on the following crucial steps:

**a.** Early detection and identification.

infest these cultivars. When high population levels are attained in adult plantations, control by broad-spectrum insecticides application is limited since populations of pollinators can be affected. Foliage application of biological pesticide *Bacillus thuringiensis* (New BT 2X at a rate 0.5 kg ha−1 or New BT 8L at 1 L ha−1) has showed promissory results in control of these

Sugar cane: Program for the development of IPM from CINCAE (Centro de Investigación de

**a.** During the first phase, an evaluation and characterization of pests to determine the impact (population, damage, and grower's perception), followed by bioecological studies (life

**b.** After that, some management components should be developed, focusing in methods of control that provoke more permanent natural mortality, being pesticides the last strategy to be considered. When pesticides are used, the minimum number of applications of selective molecules should be considered. After that, key components are integrated in a

Finally, pilot units are settling down in fields where these compatible components are used

Mexico has a long history of proactive pest management, and more recently, IPM has become even more important as trade regulations that have begun to restrict the amounts of pesticide residue or insects that may be present on produce exported to the USA and Canada [26]. In order to maintain the extensive trade in fresh fruits and vegetables, these commodities must comply with strict regulations that are difficult to meet with conventional pest control methods, being IPM, in most of the cases, the only viable option for growers intending to export their products [26]. Several IPM programs have been successfully developed in Mexico.

IPM to control the tomato pinworm, *Keiferia lycopersicella* and other lepidopteran species in tomato has included careful scouting (primarily with pheromone traps from planting to harvesting), cultural control (including plowing under crop residues promptly after harvest‐ ing, cleaning drainage ditches and irrigation canals where alternate hosts grow, and estab‐ lishing a tomato-free period during summer or winter to break the cycle of tomato pinworm reproduction), mating disruption, use of selective insecticides, and biological control [23].

The parasitoid wasp, *Trichogramma pretiosum* is an egg parasitoid of tomato pinworm and it has been found occurring in several Mexican states (Chihuahua, Coahuila, Durango, Nuevo León, Sinaloa, Sonora, Tamaulipas, and Zacatecas) [27]. This parasitoid species has been released in combination with mating disruption [28]. Due to the overuse of insecticide applications, the tomato pinworm has developed resistance to conventional insecticides so that combined use of pheromones, biological control, and selective insecticides has reduced

la Caña de Azúcar del Ecuador) has proposed the following program [25]:

basis ecological, agronomical, and socioeconomically compatible.

cycle, behavior, and population dynamic).

8 Integrated Pest Management (IPM): Environmentally Sound Pest Management

according to the characteristics of each agroecosystem.

damage and number of insecticide applications [23].

lepidopteran pests [24].

**4.4. Mexico**


Apart from the strategies for pest control, some other aspects have contributed to the success of IPM programs in Mexico (**Figure 2**).

**Figure 2.** Factors contributing to the success of IPM in Mexico.

However, Mexico still face challenges as some poor farmers cannot afford to implement IPM. Mexico is a country of contrasts where 50 million people live in poverty including poor farmers. Some government programs have been dedicated to improve the conditions of poor people in the country, however, is not an easy problem to solve.

## **4.5. Colombia**

In Colombia, the production of passion fruit (*Passiflora* spp.) is mainly in hands of small farmers. Being cultivated over 8000 hectares, *Dasiops inedulis* (Díptera: Lonchaeidae) is a key pest of passion fruit crop, but there is little information regarding their biology, ecology, and management. Local producers have large production losses due to pests, due to limited knowledge to manage them properly, facing difficulty in positioning their products in the market.

In 2008, Centro Internacional de Agricultura Tropical (CIAT) researchers worked together with local universities and farmer associations to develop a sustainable pest management package for *Dasiops inedulis*. This work allowed farmers to increase their IPM package at the field level. Field surveys conducted from 2008 to 2010 in the main fruit producing regions provided information about the pest population dynamics and geographic patterns of infestation [32]. Then, a national survey of farmers was conducted to get an idea of agroecological behavior management and local knowledge of the farmers. Apart from the common use of insecticide applications based on the calendar of application, they experimented extensively with the farmers the use of inexpensive bait traps. By using participatory practices in five agricultural communities, the farmers realized that some of the new management practices were much more effective and less expensive than current practices of pesticide application [33].

## **4.6. Peru**

IPM in Peru began in the mid-1950s in response to problems caused by the use of organo‐ chlorines on crops such as cotton, citrus, olives, and sugarcane [34]. In 1971, graduate programs (MSc level) in entomology and plant pathology were initiated at the National Agrarian University 'La Molina'. In recent years, the Government of Peru has reinitiated technical assistance to farmers through special programs that included the extension of IPM. These programs include Modules of Technical Assistance, coordinated by INIA (Instituto Nacional de Innovación Agraria) at the national level, which have the plant clinics as the diagnostic component, PRONAMACHCS (Programa Nacional de Manejo de Cuencas Hidrográficas y Conservación de Suelos; it is a national program for the management of soils and watersheds), and SENASA (Servicio Nacional de Sanidad Agraria; it is the national service for plant and animal health) [34].

In Peru, most of the vegetable species are usually cultivated in smallholder farms; hence, agricultural production is characterized by lower productivity due to limited availability of good quality seeds and pest problems, besides lack of selected varieties adapted to the agroecosystem [35]. Moreover, most of the farmers do not recognize neither pest species nor beneficial organisms, making insecticide/fungicide applications when is not necessary [35].

All these factors highlight the need to establish an education program for farmers to be trained in sustainable pest management. Saldaña et al. [36] proposed an IPM program for industrial‐ ized tomato to manage populations of the two most important pests (*Tuta absoluta* and *Bemisia* spp.) in Barranca, Lima (**Figure 3**). This proposal was based on the pest evaluation strategy, action thresholds, and the application of different control methods, including the establish‐ ment of planting dates (legal control), optimization of farming practices (cultural control), installation of light and pheromone traps (ethological control), and removal of virosic plants (mechanical control), maintenance of natural enemies populations (biological control), and selective application of pesticides (chemical control).

**4.5. Colombia**

market.

**4.6. Peru**

animal health) [34].

In Colombia, the production of passion fruit (*Passiflora* spp.) is mainly in hands of small farmers. Being cultivated over 8000 hectares, *Dasiops inedulis* (Díptera: Lonchaeidae) is a key pest of passion fruit crop, but there is little information regarding their biology, ecology, and management. Local producers have large production losses due to pests, due to limited knowledge to manage them properly, facing difficulty in positioning their products in the

10 Integrated Pest Management (IPM): Environmentally Sound Pest Management

In 2008, Centro Internacional de Agricultura Tropical (CIAT) researchers worked together with local universities and farmer associations to develop a sustainable pest management package for *Dasiops inedulis*. This work allowed farmers to increase their IPM package at the field level. Field surveys conducted from 2008 to 2010 in the main fruit producing regions provided information about the pest population dynamics and geographic patterns of infestation [32]. Then, a national survey of farmers was conducted to get an idea of agroecological behavior management and local knowledge of the farmers. Apart from the common use of insecticide applications based on the calendar of application, they experimented extensively with the farmers the use of inexpensive bait traps. By using participatory practices in five agricultural communities, the farmers realized that some of the new management practices were much

more effective and less expensive than current practices of pesticide application [33].

IPM in Peru began in the mid-1950s in response to problems caused by the use of organo‐ chlorines on crops such as cotton, citrus, olives, and sugarcane [34]. In 1971, graduate programs (MSc level) in entomology and plant pathology were initiated at the National Agrarian University 'La Molina'. In recent years, the Government of Peru has reinitiated technical assistance to farmers through special programs that included the extension of IPM. These programs include Modules of Technical Assistance, coordinated by INIA (Instituto Nacional de Innovación Agraria) at the national level, which have the plant clinics as the diagnostic component, PRONAMACHCS (Programa Nacional de Manejo de Cuencas Hidrográficas y Conservación de Suelos; it is a national program for the management of soils and watersheds), and SENASA (Servicio Nacional de Sanidad Agraria; it is the national service for plant and

In Peru, most of the vegetable species are usually cultivated in smallholder farms; hence, agricultural production is characterized by lower productivity due to limited availability of good quality seeds and pest problems, besides lack of selected varieties adapted to the agroecosystem [35]. Moreover, most of the farmers do not recognize neither pest species nor beneficial organisms, making insecticide/fungicide applications when is not necessary [35].

All these factors highlight the need to establish an education program for farmers to be trained in sustainable pest management. Saldaña et al. [36] proposed an IPM program for industrial‐ ized tomato to manage populations of the two most important pests (*Tuta absoluta* and *Bemisia* spp.) in Barranca, Lima (**Figure 3**). This proposal was based on the pest evaluation strategy, action thresholds, and the application of different control methods, including the establish‐

**Figure 3.** IPM program proposed for pest control in industrialized tomato in Peru (from: [36]).

As a first step, authors developed a methodology to evaluate the specific characteristics of the agricultural ecosystem to determine pest incidence on different phenological stages and establish thresholds to take more efficient control measures. The pest evaluation methodology developed by Sarmiento and Sánchez [37], consists in considering 5 ha as a unit of evaluation which is divided into five subunits. In each subunit, five plants are sampled (four shoots, one leaflet from basal and middle strata, four inflorescences, one twig, and four fruits along 2 m in a furrow).

## **5. IPM in Latin America: status and challenges**

As stated by Rodríguez and Niemeyer [9], IPM research and promotion have responded, in one hand, to food security, which is devoted to the protection of a subsistence crop mainly focused on smallholder peasants, and on the other hand, exports which try to fulfil the requirements of foreign markets and are concentrated in larger producers.

Although research and field-level implementation of IPM has been most successful in the United States and Europe, IPM has made significant progress in developing countries, but focused generally on large-scale rather than small, subsistence farms [38]. According to Rodríguez and Niemeyer [9], government programs and subsidies in developing countries have been concentrated on medium and large farmers since they are able to hire personnel to develop research or to create links with external institutions. Thus, in some countries, such as Chile, there are grant funds available for agricultural research and innovation projects incorporating IPM practices involving partnerships with private firms under a commitment to transfer the results to potential users. Given the requirements for partnerships, the program is not easily available for small farmers, and most research is guided by the specific needs of larger export companies. However, increasingly, scientists, policy makers, and donor agencies in developing countries are turning their attention to small farmers.

Some farmers have benefited greatly from introduced technologies in major production areas in Latin America as many of the new crop technologies have increased crop yield and also their commodity crops can be sent to market [39]. Conversely, those farmers poorly served by markets or have not been reached by modernization packages, the technologies, and practices have failed to generate significant benefits in crop protection systems [40].

The media and public agricultural extension have played a crucial role in introducing the new technologies and good agricultural practices to farmers, however; there has been little investment in farmer education so that they are able to expand their capabilities to understand, innovate, and adapt to the changing context [39]. Although more effort to expand farmers' capabilities to improve production and productivity have been made, agricultural develop‐ ment programs have been unsuccessful because they failed to educate farmers on the sustain‐ able management of variable agroecosystems and to cope with the changes in marketing demands arising from globalizing food and commodity trade [39, 41].

As stated by van den Berg and Jiggins [39], the role of the new generations of farmers has reduced to be simple technology clients, leading them to lose much of the indigenous agri‐ cultural knowledge and skills, and in the integrity of the social organization in which indige‐ nous innovation capacity is embedded.

Thereby, the challenge then would be focused to capacitate the millions of small farmers to deal with pest and become experts in decentralized pest management through practical, fieldbased learning methods.

## **6. Plantwise helping small farmers to produce in a sustainable way**

In some areas, up to 70% of food is lost before it can be consumed. This problem is exacerbated by international trade, intensified production, and climate change altering and accelerating the spread of plant pests. Clearly there is an opportunity to lose less and feed more by improving control of such pest problems, particularly in the developing world [42, 43].

Plantwise (www.plantwise.org), an innovative global program, led by CABI, aims to contrib‐ ute to increased food security, alleviated poverty, and improved livelihoods by enabling male and female farmers around the world to lose less, produce more, and improve the quality of their crops. Working in close partnership with relevant actors, Plantwise strengthens national plant health systems from within, enabling countries to provide farmers with the knowledge they need to lose less and feed more [44].

The Plantwise approach is based on three interlinked components:

Although research and field-level implementation of IPM has been most successful in the United States and Europe, IPM has made significant progress in developing countries, but focused generally on large-scale rather than small, subsistence farms [38]. According to Rodríguez and Niemeyer [9], government programs and subsidies in developing countries have been concentrated on medium and large farmers since they are able to hire personnel to develop research or to create links with external institutions. Thus, in some countries, such as Chile, there are grant funds available for agricultural research and innovation projects incorporating IPM practices involving partnerships with private firms under a commitment to transfer the results to potential users. Given the requirements for partnerships, the program is not easily available for small farmers, and most research is guided by the specific needs of larger export companies. However, increasingly, scientists, policy makers, and donor agencies

Some farmers have benefited greatly from introduced technologies in major production areas in Latin America as many of the new crop technologies have increased crop yield and also their commodity crops can be sent to market [39]. Conversely, those farmers poorly served by markets or have not been reached by modernization packages, the technologies, and practices

The media and public agricultural extension have played a crucial role in introducing the new technologies and good agricultural practices to farmers, however; there has been little investment in farmer education so that they are able to expand their capabilities to understand, innovate, and adapt to the changing context [39]. Although more effort to expand farmers' capabilities to improve production and productivity have been made, agricultural develop‐ ment programs have been unsuccessful because they failed to educate farmers on the sustain‐ able management of variable agroecosystems and to cope with the changes in marketing

As stated by van den Berg and Jiggins [39], the role of the new generations of farmers has reduced to be simple technology clients, leading them to lose much of the indigenous agri‐ cultural knowledge and skills, and in the integrity of the social organization in which indige‐

Thereby, the challenge then would be focused to capacitate the millions of small farmers to deal with pest and become experts in decentralized pest management through practical, field-

In some areas, up to 70% of food is lost before it can be consumed. This problem is exacerbated by international trade, intensified production, and climate change altering and accelerating the spread of plant pests. Clearly there is an opportunity to lose less and feed more by improving control of such pest problems, particularly in the developing world [42, 43].

Plantwise (www.plantwise.org), an innovative global program, led by CABI, aims to contrib‐ ute to increased food security, alleviated poverty, and improved livelihoods by enabling male

**6. Plantwise helping small farmers to produce in a sustainable way**

in developing countries are turning their attention to small farmers.

12 Integrated Pest Management (IPM): Environmentally Sound Pest Management

have failed to generate significant benefits in crop protection systems [40].

demands arising from globalizing food and commodity trade [39, 41].

nous innovation capacity is embedded.

based learning methods.


**Figure 4.** Plantwise theory of change (from: [46]).

In the Plantwise knowledge bank, plant clinic records are collated and analysed to support the quality of advice given to farmers and inform decision-making. By putting knowledge into the hands of smallholder farmers, Plantwise is able not only to help them lose less and feed more but also to gather data which can assist all stakeholders in the plant health system-from research, agro-input supply, extension and policy-making. Most importantly, Plantwise is a development program which cooperates with a number of international and national organ‐ izations working to remove constraints to agricultural productivity. Countries are now using plant clinics and Knowledge bank resources to improve national vigilance against pest outbreaks [45].

The key premise of the Plantwise Theory of Change is that plant health systems function to reduce crop losses and promote plant health (**Figure 4**). Plantwise defines a plant health system by four key components: (1) extension, which delivers available knowledge intended to improve plant health; (2) research, which develops new knowledge about plant health and is often linked to higher level education; (3) input suppliers, who deliver knowledge and physical inputs such as seeds, biological and other crop protection products, and fertilizers; and (4) regulation, which regulates sale and use of agricultural inputs, protects countries from new and emerging pests (invasive species included), and regulates produce export requirements.

The Plantwise approach develops sustainable mechanisms to deliver better plant health services that address farmer needs and improve output, including (1) improving advisory services based on plant clinics and complementary extension approaches and delivering effective responses to any plant health problem affecting any crop; (2) improving regulatory systems so that plant health problems are detected early and advisory staff on the ground are able to communicate appropriate mitigation measures to farmers before the problems become devastating; (3) stimulating research that supports farmers' needs; and (4) improving input supply ensuring provision of appropriate, legitimate, and effective goods [46].

The Plantwise programme encourages extension officers to offer plant health management advice to farmers guided by the principles of integrated pest management (IPM), looking forward to increase the sustainability of the production system [46].

## **Author details**

Yelitza Colmenárez1\*, Carlos Vásquez2 , Natália Corniani3 and Javier Franco4

\*Address all correspondence to: y.colmenarez@cabi.org

1 UNESP-FEPAF-Fazenda Experimental Lageado, Botucatu - SP, Brazil

2 Universidad Técnica de Ambato, Facultad de Ciencias Agropecuarias, Campus Querochaca, Cevallos, Ecuador

3 CABI South America, Botucatu, Brazil

4 Proinpa Foundation, Cochabamba, Bolívia

## **References**

hands of smallholder farmers, Plantwise is able not only to help them lose less and feed more but also to gather data which can assist all stakeholders in the plant health system-from research, agro-input supply, extension and policy-making. Most importantly, Plantwise is a development program which cooperates with a number of international and national organ‐ izations working to remove constraints to agricultural productivity. Countries are now using plant clinics and Knowledge bank resources to improve national vigilance against pest

14 Integrated Pest Management (IPM): Environmentally Sound Pest Management

The key premise of the Plantwise Theory of Change is that plant health systems function to reduce crop losses and promote plant health (**Figure 4**). Plantwise defines a plant health system by four key components: (1) extension, which delivers available knowledge intended to improve plant health; (2) research, which develops new knowledge about plant health and is often linked to higher level education; (3) input suppliers, who deliver knowledge and physical inputs such as seeds, biological and other crop protection products, and fertilizers; and (4) regulation, which regulates sale and use of agricultural inputs, protects countries from new and emerging pests (invasive species included), and regulates produce export requirements.

The Plantwise approach develops sustainable mechanisms to deliver better plant health services that address farmer needs and improve output, including (1) improving advisory services based on plant clinics and complementary extension approaches and delivering effective responses to any plant health problem affecting any crop; (2) improving regulatory systems so that plant health problems are detected early and advisory staff on the ground are able to communicate appropriate mitigation measures to farmers before the problems become devastating; (3) stimulating research that supports farmers' needs; and (4) improving input

The Plantwise programme encourages extension officers to offer plant health management advice to farmers guided by the principles of integrated pest management (IPM), looking

, Natália Corniani3

and Javier Franco4

supply ensuring provision of appropriate, legitimate, and effective goods [46].

forward to increase the sustainability of the production system [46].

1 UNESP-FEPAF-Fazenda Experimental Lageado, Botucatu - SP, Brazil

2 Universidad Técnica de Ambato, Facultad de Ciencias Agropecuarias, Campus

outbreaks [45].

**Author details**

Yelitza Colmenárez1\*, Carlos Vásquez2

Querochaca, Cevallos, Ecuador

3 CABI South America, Botucatu, Brazil

4 Proinpa Foundation, Cochabamba, Bolívia

\*Address all correspondence to: y.colmenarez@cabi.org


[25] Mendoza J, Gualle D, Gómez P, Ayora A, Martínez I, Cabezas C. Progresos en el manejo de plagas en caña de azúcar en Ecuador [Internet]. Available from: http:// www.aeta.org.ec/2do congreso cana/art\_campo/MENDOZA cana.pdf [accessed: 30/03/2016].

[14] Mumford JD, Norton GA. Economics of decision making in pest management. Annual

[15] Orr D. Biological control and integrated pest management. In: Peshin R, Dhawan AK, editors. Integrated Pest Management: Innovation-Development Process. Netherlands:

[16] O'neil RJ, Yaninek JS, Landis DA, Orr DB. Biological control and integrated pest management. In: Maredia KM, Dakouo D, Mota-Sanchez D, editors. Integrated Pest Management in the Global Arena. Wallingford, Oxfordshire, England: CABI Publish‐

[17] Tauber MJ, Hoy MA, Herzog DC. Biological control in agricultural IPM systems: a brief overview of the current status and future prospects. In: Hoy MA, Herzog DC, editors. Biological control in Agricultural IPM Systems. Orlando, FL, USA: Academic Press

[18] Murphy ST, Briscoe BR. The red palm weevil as an alien invasive: biology and the prospects for biological control as a component of IPM. Biocontrol News and Informa‐

[19] Mazza G, Francardi V, Simoni S, Benvenuti C, Cervo R, Faleiro JR, Llácer E, Longo S, Nannelli R, Tarasco E, Roversi PF. An overview on the natural enemies of *Rhynchopho‐*

[20] Bajwa WI, Kogan M. Integrated pest management adoptions by global community. In: Maredia KM, Dakouo D, Mota-Sanchez D, editors. Integrated Pest Management in the Global Arena. Wallingford, Oxfordshire, England: CABI Publishing; 2003. p. 97–107.

[21] Carmona D, Huarte M, Arias G, López A, Vincini AM, Álvarez HA, Manetti P, Capezio S, Chávez E, Torres M, Eyherabide J, Mantecón J, Cichón L, Fernández D. Integrated pest management in Argentina. In: Maredia KM, Dakouo D, Mota-Sanchez D, editors. Integrated Pest Management in the Global Arena. Wallingford, Oxfordshire, England:

[22] Parra JR. Manejo integrado de pragas. In: Paterniani E, editor. Agricultura Brasileira e a Pesquisa Agropecuária. Brasília: Embrapa Comunicação para Transferência de

[23] Hoffmann-Campo CB, Oliveira LJ, Moscardi F, Gazzoni DL, Corrêa-Ferreira BS, Lorini IA, Borges M, Panizzi AR, Sosa-Gomez DR, Corso IC. Integrated Pest Management in Brazil. In: Maredia KM, Dakouo D, Mota-Sanchez D, editors. Integrated Pest Manage‐ ment in the Global Arena. Wallingford, Oxfordshire, England: CABI Publishing; 2003.

[24] Emilio Farias Falcones. Manejo Integrado de Plagas en Cacao en el Ecuador. Available from: http://elproductor.com/2012/07/09/manejo-integrado-de-plagas-en-cacao-

*rus* palm weevils, with focus on *R. ferrugineus*. 2014;77:83–92.

Review of Entomology 1984;29:157-174.

16 Integrated Pest Management (IPM): Environmentally Sound Pest Management

ing; 2003. p. 19–30.

INC.; 1985. p. 9-12.

tion. 1999;20(1):35-46.

CABI Publishing; 2003. p. 313–326.

utilizando-new-bt-2x [accessed: 30/03/2016].

Tecnologia; 2000. p. 92-105.

p. 285–300.

Springer Science + Business Media; 2009. p. 207–240.


## **Chapter 2**

## **Pest Control in Organic Systems**

Vasile Stoleru and Vicenzo Michele Sellitto

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/64457

#### **Abstract**

[36] Saldaña C, Sarmiento J, Sánchez G. Manejo Integrado de plagas en el cultivo industrial de tomate (*Lycopersicum esculentum* Mill.) en el Valle de Barranca, Lima, Perú. Revista

[37] Sarmiento J, Sánchez G, editors. Evaluación de Insectos. Lima: Universidad Nacional

[38] Goodell G. Challenges to international pest management research and extension in the third world: Do we really want IPM to work? Bulletin of the Entomological Society of

[39] van den Berg H, Jiggins J. Investing in farmers – the impacts of farmer field schools in relation to integrated pest management. World Development. 2007;35(4):663–686. [40] Inter-Academy Council. Realizing the promise and potential of African Agriculture: science and technology strategies for improving agricultural productivity and food

[41] Reardon T, Berdegué JA. The rapid rise of supermarkets in Latin America: challenges and opportunities for development. Development Policy Review. 2002;20:371–388.

[43] Finegold C, Oronje M, Leach MC, Karanja T, Chege F, Hobbs SLA. Plantwise knowl‐ edge bank: building sustainable data and information processes to support plant clinics

[44] Romney DR. Plantwise: putting innovation systems principles into practice. Agricul‐

[45] Kuhlmann U. Plantwise: a global alliance for plant health support. International Agriculture in a changing world: good news from the field; Bern. 2014. p. 23.

[46] Plantwise. Plantwise Strategy 2015–2020 [Internet]. Available from: https://www.plant‐ wise.org/Uploads/Plantwise/Plantwise%20Strategy%202015%202020.pdf [accessed:

[42] Oerke EC. Crop losses to pests. Journal of Agricultural Science 2006;144:31–43.

security in Africa. Amsterdam: Inter-Academy Council; 2004.

in Kenya. Agricultural Information Worldwide. 2014;6:96–101.

ture for Development. 2013;18:27–31.

2/02/2016].

Peruana de Entomología. 2033;43:153–157.

18 Integrated Pest Management (IPM): Environmentally Sound Pest Management

Agraria; 2000. 117 p.

America. 1984;30(3):18–26.

Conventional agriculture techniques applied in the latest decades have had undesired consequences on the environmental sustainability, carried out to the soil erosion, the degradation of the ecological system, changing the balance between beneficial and harmful pests, and contamination of soil, water, and agricultural products by heavy metals and pesticides. Thus, in organic agriculture, using synthetic chemicals for pest control is prohibited, assigning to the diversity a major role. The study provides to the reader many important practical data, judiciously documented, which are useful for the researchers and farmers from the world. Pest control in organic agriculture can be obtained through prevention and curative measure, but modern agriculture must be focused on the prevention.

**Keywords:** organic agriculture, pest control, preventive and curative methods

## **1. Introduction**

Organic agriculture (OA) farming aims to achieve sustainable, diversified, and balanced systems, with the purpose of protecting the environment for present and future generations. In the same way, OA provides on the food market, products of a certain nutritional quality, suitable in terms of lower contaminants.

The organic product is governed by some well defined principles, aimed at ensuring environ‐ mental and crop sustainability.

© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

## **1.1. Circumstances of pest control in organic systems**

Being a type of sustainable agriculture the purpose of OA can be expressed by a mini–max function, maximizing production and minimizing the negative agricultural activities on the environment [1].

OA stimulates the activity of useful microorganisms, flora and fauna. Soils under crops are increasingly lifeless and infested with weeds, diseases, as well as pests. This situation is determined by current agricultural practices that excel in monoculture and short crop rota‐ tions, of 2–3 years, much delayed and bad quality soil tillage and plant care, burning plant debris, etc.

Biodiversity management. The soil's biological resources are vital to the economic and social development of all humanity. That is why, it is more and more frequently recognized that biological diversity is universal asset, of inestimable value for future generations. Biological (ecologic, organic) agriculture generally uses a greater number of cultivated species, to explore their suitability and ecological plasticity. Non-using synthetic herbicides, and instead using milder solutions for weed destruction, ensures the coexistence of weeds together with the crop.

Protecting the natural landscape. Elevation diversity, as well as flora and fauna variability, is inseparable to the applied vegetable growing systems, the most aggressive ones being of the intensive type, often causing deterioration.

Many cultivation techniques applied in the past decades have had undesired consequences on the environment, contributing to soil erosion, the degradation of the ecological system, contamination of ground water and crops with pesticides and nitrates.

Organic agriculture aims to preserve the environment unaltered, using organic fertilizers and also less soluble mineral fertilizers, organic fertilizers, such as composts and green fertilizers, avoiding to use products that can have harmful effects [2].

The use of synthetic herbicides and pesticides are prohibited, and only products that are harmless for the plant are allowed, products based on simple minerals (Cu, S, Na, silicate, etc.) or plant extracts (pyrethrum), including the application of physical (thermal) methods.

In organic agriculture, the emphasis is laid on the quality of human intervention over nature, which is non-aggressive, compared to conventional agriculture.

## **1.2. Standards and regulations regarding organic farming**

After 2010, OA can be considered a period of consolidation for standards and the regulations, which aimed and still aims to facilitate international trade with organic products in order to reduce legislative gaps which exist among the various certification types, such as the EC Regulations [3, 4], the USA (NOP), Australia (AS 6000-2009), Japan (JAS), and Switzerland (Bio Swiss). Thus, the EC Regulation of organic agriculture [3] has been improved in the least years with new regulations, targeting aquaculture and organic wine production.

The number of the certification bodies, in 2013, was at 569, increasing from 2010 when there were 532. Most certification bodies are found in the European Union, Japan, the United States of America, South Korea, China, Canada, India, and Brazil [5].

Organic farming (biological, ecological) is currently one of the most dynamic forms of agriculture. This affirmation is mainly supported by the expansion of agricultural areas, currently occupying 40.2 of the surface in Oceania, 26.6 in Europe, and 15.3% in Latin America. There are also cases of countries, such as Argentina, Spain, and USA, in which the area increased in 2013 compared to 2011 with over 185,000 ha.

Around the world, at the end of 2013, the organically certified area covered more than 78 million ha. Organically certified agricultural areas covered over 43 million ha (1% from total arable land), including the same land under its conversion period, but excluded wild collection and aquaculture. From these data, it appears that the organically administered surface has had a growth rate of over 14.94% compared with 2012 (approx. 37.4 million ha). Europe and Oceania recorded the fastest land expansion rhythm in 2013, compared to 2011, which shows that the expansion of the areas is supported by an intensive marketing of organic products [5].

Compared to 2012, the organically certified area in the world increased by over 5.6 million ha, which means a growth rate of the arable production from the total agricultural area of 0.1%.

At the end of 2013, the situation of the organic agricultural area distributed on categories of land use highlighted that 63% was permanent grassland, 18% was arable land (cereals, green fodder, oilseed, vegetable, and protein crops), and 7% was permanent crop (coffee, olives, nuts, grapes, and cocoa) and the rest with other crops [5].

Of course, in some countries, the conversion areas or the cultivated ones are decreasing, especially due to legislation and government support, which differ from country to country (UK).

Global sales of organic food and drinks reached more 72 billion dollars at the end of 2013. Compared to 2009, this sector revenue increased almost five times. Europe and North America made a big contribution to cover these specific sectors. Asia, Latin America, and Africa have become really important producers of organic crops for this market. About 43% from this market is covered by the United States followed by Europe at percent 40% [5].

In 2013, the countries with the largest organic markets were the USA (24.3 billion €), Germany (7.6 billion €), and France (4.4 billion €) [5].

## **2. Pest control measures**

**1.1. Circumstances of pest control in organic systems**

20 Integrated Pest Management (IPM): Environmentally Sound Pest Management

intensive type, often causing deterioration.

environment [1].

debris, etc.

Being a type of sustainable agriculture the purpose of OA can be expressed by a mini–max function, maximizing production and minimizing the negative agricultural activities on the

OA stimulates the activity of useful microorganisms, flora and fauna. Soils under crops are increasingly lifeless and infested with weeds, diseases, as well as pests. This situation is determined by current agricultural practices that excel in monoculture and short crop rota‐ tions, of 2–3 years, much delayed and bad quality soil tillage and plant care, burning plant

Biodiversity management. The soil's biological resources are vital to the economic and social development of all humanity. That is why, it is more and more frequently recognized that biological diversity is universal asset, of inestimable value for future generations. Biological (ecologic, organic) agriculture generally uses a greater number of cultivated species, to explore their suitability and ecological plasticity. Non-using synthetic herbicides, and instead using milder solutions for weed destruction, ensures the coexistence of weeds together with the crop.

Protecting the natural landscape. Elevation diversity, as well as flora and fauna variability, is inseparable to the applied vegetable growing systems, the most aggressive ones being of the

Many cultivation techniques applied in the past decades have had undesired consequences on the environment, contributing to soil erosion, the degradation of the ecological system,

Organic agriculture aims to preserve the environment unaltered, using organic fertilizers and also less soluble mineral fertilizers, organic fertilizers, such as composts and green fertilizers,

The use of synthetic herbicides and pesticides are prohibited, and only products that are harmless for the plant are allowed, products based on simple minerals (Cu, S, Na, silicate, etc.) or plant extracts (pyrethrum), including the application of physical (thermal) methods.

In organic agriculture, the emphasis is laid on the quality of human intervention over nature,

After 2010, OA can be considered a period of consolidation for standards and the regulations, which aimed and still aims to facilitate international trade with organic products in order to reduce legislative gaps which exist among the various certification types, such as the EC Regulations [3, 4], the USA (NOP), Australia (AS 6000-2009), Japan (JAS), and Switzerland (Bio Swiss). Thus, the EC Regulation of organic agriculture [3] has been improved in the least years

contamination of ground water and crops with pesticides and nitrates.

avoiding to use products that can have harmful effects [2].

which is non-aggressive, compared to conventional agriculture.

with new regulations, targeting aquaculture and organic wine production.

**1.2. Standards and regulations regarding organic farming**

Organic farming (OF) is a system-based agricultural production system working with rather than against natural systems [2].

The major differences that have been made in terms of technology between organic and conventional cultivation of plants are as follows: soil fertility, weeds, pathogens, and pest control.

Pest control in organic agriculture can be obtained through prevention and curative measure but must be focused on the preventive infestation of pests [2]. Measures to prevent infestation by pests refers to: phytosanitary quarantine (special for seed and planting materials used for establishing crops); monitoring pest infestation (used in general agro-expert stations or traps); choice of cultivars according to the criterion of resistance and ecological plasticity; seed conditioning; destruction of problematic weeds; solarization; and hygienic conditions.

## **2.1. Prevention pests in an organic system**

The fundamental principle of controlling pests in organic systems (OS) should consider the mechanism of adjusting its biocenosis (total community of organisms from o biotope), through the correlation and interdependence between the cultivated species, pathogens, weeds, pests, technology, and the environment. Protecting plants from pests and diseases probably has the greatest impact on achieving an organic vegetable crop, due to the very large spectrum of pathogens and pests from these crops. The first major attempt to reduce chemical treatments took place even before 1970, when the concept of integrated control was promoted [6, 7]. According to this concept, all technical methods are allowed to maintain the populations of pests and pathogens under a certain degree of impairment, which does not affect the yields from an economic point of view.

This concept is approved by the International Organization for Biological Control (IOBC), but first of all natural factors must be used, together with other methods appropriate for the economic, ecological, and toxicological requirements [8].

In organic farming, the principles of the integrated pest control are perfectly applicable in substantializing the mechanisms for fighting pests, diseases, but most chemical means are forbidden; instead, new unconventional methods have been used, like some biodynamic preparations.

The strong attack of some pests may be favored by some technical mistakes, in general, or mistakes in the environmental context such as the following: improper choice of the place of culture; using seeds or plants that are weakly developed; mistakes in crop association; practicing monocultures without using proper crop rotation; incorrectly executed soil tillage; unilateral or excessive fertilization, without organic fertilizers; insufficient fertilization; extreme weather conditions; and improper choice of the sowing period [1, 9].

#### *2.1.1. Phytosanitary quarantine*

The quarantine is a complex of preventive measures taken to stop the penetration of diseases, pests, or weeds from other countries and to limit their spread. Overall, export products between countries shall be binding accompanied by a phytosanitary document certifying that the seeds or agricultural materials for setting up the crop (seeds, cuttings, tubers, bulbs, seedlings, shrubs, or trees) are free from pest quarantine.

There are numerous species (mites, insects), generally in polyphagus that are considered extremely dangerous and huge efforts have been made to limit their expansion, for example: *Leptinotarsa decemlineata* (Colorado beetle), *Tetranychus urticae (*red spider mite*)*, *Myzus persicae (*green peach aphid*)*, *Bemisia tabaci (*silverleaf whitefly*)*, *Trialeurodes vaporariorum* (greenhouse whitefly), *Liriomyza trifolii (*leaf miner flies*)*, *Tuta absoluta* (tomato leaf miner), *Spodoptera litura (*Oriental leaf worm moth*)*, *Frankliniella intonsa red (*red thrips*), Diabrotica virgifera virgifera* (western corn rootworm), or others [10–12].

## *2.1.2. Maintenance of biodiversity*

Pest control in organic agriculture can be obtained through prevention and curative measure but must be focused on the preventive infestation of pests [2]. Measures to prevent infestation by pests refers to: phytosanitary quarantine (special for seed and planting materials used for establishing crops); monitoring pest infestation (used in general agro-expert stations or traps); choice of cultivars according to the criterion of resistance and ecological plasticity; seed conditioning; destruction of problematic weeds; solarization; and hygienic conditions.

The fundamental principle of controlling pests in organic systems (OS) should consider the mechanism of adjusting its biocenosis (total community of organisms from o biotope), through the correlation and interdependence between the cultivated species, pathogens, weeds, pests, technology, and the environment. Protecting plants from pests and diseases probably has the greatest impact on achieving an organic vegetable crop, due to the very large spectrum of pathogens and pests from these crops. The first major attempt to reduce chemical treatments took place even before 1970, when the concept of integrated control was promoted [6, 7]. According to this concept, all technical methods are allowed to maintain the populations of pests and pathogens under a certain degree of impairment, which does not affect the yields

This concept is approved by the International Organization for Biological Control (IOBC), but first of all natural factors must be used, together with other methods appropriate for the

In organic farming, the principles of the integrated pest control are perfectly applicable in substantializing the mechanisms for fighting pests, diseases, but most chemical means are forbidden; instead, new unconventional methods have been used, like some biodynamic

The strong attack of some pests may be favored by some technical mistakes, in general, or mistakes in the environmental context such as the following: improper choice of the place of culture; using seeds or plants that are weakly developed; mistakes in crop association; practicing monocultures without using proper crop rotation; incorrectly executed soil tillage; unilateral or excessive fertilization, without organic fertilizers; insufficient fertilization;

The quarantine is a complex of preventive measures taken to stop the penetration of diseases, pests, or weeds from other countries and to limit their spread. Overall, export products between countries shall be binding accompanied by a phytosanitary document certifying that the seeds or agricultural materials for setting up the crop (seeds, cuttings, tubers, bulbs,

There are numerous species (mites, insects), generally in polyphagus that are considered extremely dangerous and huge efforts have been made to limit their expansion, for example:

extreme weather conditions; and improper choice of the sowing period [1, 9].

**2.1. Prevention pests in an organic system**

22 Integrated Pest Management (IPM): Environmentally Sound Pest Management

from an economic point of view.

*2.1.1. Phytosanitary quarantine*

preparations.

economic, ecological, and toxicological requirements [8].

seedlings, shrubs, or trees) are free from pest quarantine.

Synthetic pesticides are not permitted in organic farming which serves to preserve and enhance biodiversity within the system. Natural enemies of pest species are therefore able to thrive, exerting control on pest populations. Conservation and improvement of natural features of the landscape, such as hedgerows and ponds and the construction of beetle banks and sown flower strips, have also enabled communities of predators to flourish.

In agriculture, in general, farmers work with biological organisms, which behave differently under the action of nature's biotic or abiotic factors [13].

The pests are very adaptive to the changes of production systems, especially from the transfer from conventional to organic farms (in conversion).

In OA, pest problems are influenced by three major components of farming systems, such as: crop species and cultivar, agro-ecosystem structure, and technology production (**Figures 1** and **2**).

**Figure 1.** Management of land for organic agriculture (photograph by Stoleru Vasile).

Researchers developed flowering strips that are tailored to requirements of the specific complex of natural enemies within a cropping system. So, any experiments identified selective plant species that would improve the longevity and parasitization rate of the parasitoid wasps (*Microplitis mediator*, *Diadegma fenestrale,* and *D. semiclausum*) on the *Mamestra brassicae*.

**Figure 2.** Sea buckthorn hedge on an organic farm (photograph by Stoleru Vasile).

Comparing the effects of floral and extrafloral nectar of different plants, beneficial effects of *Fagopyrum esculentum* (floral nectar), *Centaurea cyanus* (floral and extrafloral nectar), and nonflowering *Vicia sativa* (extrafloral nectar) on parasitoids were found. Extensive plant screening is essential to achieve plant selectivity and to maximize biological control. *F. esculentum*, *C. cyanus* and *V. sativa* are recommended as selective plant species to enhance parasitoids of *M. brassicae* [14].

## *2.1.3. Selection of cultivars according to the resistance and ecological plasticity criteria*

The cultivar is perhaps the most important factor that productivity and quality depend on. Because of its biological and technological potential, it will be expressed in terms of appropriate measures [15].

In order to choose the most suitable cultivar for OA, the farmer should take into account main criteria: consumer preferences regarding appearance, taste [2], etc.; climate and soil conditions, adaptation to extreme environmental conditions; extreme temperatures, the length of the photoperiod, tolerance to high concentrations of salts, and economic use of fertilizers; resist‐ ance or tolerance to diseases and pests; cultivation technology (field, greenhouse, tunnels, time of sowing, planting and the harvesting period, irrigated regime or less, mechanization) [16]; and product destination: fresh consumption and industrialization (canning, freezing, dehy‐ dration, etc.);

A cultivar cannot meet all these requirements, but, depending on the destination of the products and both the consumers' requirement and farmers' preferences, the most suitable biological material will be chosen under the given conditions [17].

There are very different requirements from the growers regarding variety characteristics, depending on the size of the surfaces and the destination of the products. Thus, for small gardens, created by amateurs for their own consumption, large fruit species can be cultivated, as they are more sensitive to transport and storage. OA can be used as varieties, hybrids, local populations, and clones [3, 4], but not accepted genetically modified organisms.

Choosing varieties and hybrids with resistance to pathogens and pests is necessary both for protected crops and for early field crops, because the investment is often large, so risks and loss must be eliminated [18–20].

For many crops (tomatoes, cucumbers, eggplants, bushes, or trees) grafted method may be used that causes plant vigor and thus resistance to nematode (**Figure 3**).

**Figure 2.** Sea buckthorn hedge on an organic farm (photograph by Stoleru Vasile).

24 Integrated Pest Management (IPM): Environmentally Sound Pest Management

*brassicae* [14].

measures [15].

dration, etc.);

Comparing the effects of floral and extrafloral nectar of different plants, beneficial effects of *Fagopyrum esculentum* (floral nectar), *Centaurea cyanus* (floral and extrafloral nectar), and nonflowering *Vicia sativa* (extrafloral nectar) on parasitoids were found. Extensive plant screening is essential to achieve plant selectivity and to maximize biological control. *F. esculentum*, *C. cyanus* and *V. sativa* are recommended as selective plant species to enhance parasitoids of *M.*

The cultivar is perhaps the most important factor that productivity and quality depend on. Because of its biological and technological potential, it will be expressed in terms of appropriate

In order to choose the most suitable cultivar for OA, the farmer should take into account main criteria: consumer preferences regarding appearance, taste [2], etc.; climate and soil conditions, adaptation to extreme environmental conditions; extreme temperatures, the length of the photoperiod, tolerance to high concentrations of salts, and economic use of fertilizers; resist‐ ance or tolerance to diseases and pests; cultivation technology (field, greenhouse, tunnels, time of sowing, planting and the harvesting period, irrigated regime or less, mechanization) [16]; and product destination: fresh consumption and industrialization (canning, freezing, dehy‐

A cultivar cannot meet all these requirements, but, depending on the destination of the products and both the consumers' requirement and farmers' preferences, the most suitable

biological material will be chosen under the given conditions [17].

*2.1.3. Selection of cultivars according to the resistance and ecological plasticity criteria*

**Figure 3.** Fado hybrid grafted on the Rezistar rootstock for an attack on nematodes (photograph by Stoleru Vasile).

In **Table 1** are presented any cultivars with resistance or tolerance to the attack of different pests, especially for nematode control, in temperate climate conditions.

Recent research on the outside cabbage crop in the temperate climate highlighted, Timpurie de Vidra cultivar (cv) of early cabbage is most resistant to the cabbage fly (8.5% degree of attack) in comparison with the Golden acre cv., where the degree of attack was 14.2%, during two study years [21].

The reaction of cultivars resistant to pests and the nematode default may be determined by its presence in the plant silica [22], iron [23] genes that provide resistance [18, 24, 25], or protein presence in bean or cowpea [23, 26, 27].


**Table 1.** Varieties created with resistance or tolerance to various pests.

#### *2.1.4. Seed conditioning*

Numerous pests, especially from the coleopteran order, can be found between the seeds or inside them during sowing, as they feed within their endosperm, endangering seed germina‐ tion or weakening the newly sprouted plant [8]. The larvae and adults of nematodes (*Ditylen‐ chus dipsaci*, *Tylenchorhynchus cylindricus*) attack both the garlic and onion bulbs but also the roots of the vegetables, making the plant die dry [28, 29].

#### *2.1.5. Crop rotation*

Effective crop rotations are fundamental to pest control in OS. Correct rotations provide an obstacle to the pest life cycles by removing host crops for prolonged periods of time. They also help in supporting a more diverse and stable agro-ecosystem to assist with natural pest suppression.

In areas where the climate permits, two or three crops can be grown during on the year on the same area, both in greenhouses or tunnels. From this point of view, it must be considered as species that succeed have no common pests (**Table 2**).


**Table 2.** Plot design for successive crops in greenhouse/tunnel.

For the outdoor crops, in **Table 3**, some design rotation successive crops are presented. For these designs bear in mind that the crops that are grown on the same land area must belong to the same botanical family, have no common diseases and pests, and have different growing seasons.


**Table 3.** Plot design for successive crops in the field.

#### *2.1.6. Crop monitoring*

**Species Cultivar Pest resistant or tolerance**

Dianthus Sooty *Meloidogyne arenaria Neal.,* Pineapple Turiacu *Meloidogyne arenaria Neal.,*

Numerous pests, especially from the coleopteran order, can be found between the seeds or inside them during sowing, as they feed within their endosperm, endangering seed germina‐ tion or weakening the newly sprouted plant [8]. The larvae and adults of nematodes (*Ditylen‐ chus dipsaci*, *Tylenchorhynchus cylindricus*) attack both the garlic and onion bulbs but also the

Effective crop rotations are fundamental to pest control in OS. Correct rotations provide an obstacle to the pest life cycles by removing host crops for prolonged periods of time. They also help in supporting a more diverse and stable agro-ecosystem to assist with natural pest

In areas where the climate permits, two or three crops can be grown during on the year on the same area, both in greenhouses or tunnels. From this point of view, it must be considered as

For the outdoor crops, in **Table 3**, some design rotation successive crops are presented. For these designs bear in mind that the crops that are grown on the same land area must belong to the same botanical family, have no common diseases and pests, and have different growing

**No. Crop Sowing period Planting End of the crop** Lettuce, anticipated 20 VIII–10 IX 20 IX–10 X 15–30 III Sweet pepper 10–15 I 1–15 IV 20–30 IX Green onion 25–30 IV 1–15 X 25 III–5 IV

Zucchini Amalthee *Meloidogyne* spp. Cucumber Dasher II *Meloidogyne* spp. Soybean Huasteca 300 *Tamaulipas state*

*Meloidogyne incognita Chitw., Meloidogyne hapla Chitw.*

Tomato Getina F1 Gloria F1, Splendid

*2.1.4. Seed conditioning*

*2.1.5. Crop rotation*

suppression.

seasons.

F1, Solara F1, Nemarom F1

26 Integrated Pest Management (IPM): Environmentally Sound Pest Management

**Table 1.** Varieties created with resistance or tolerance to various pests.

roots of the vegetables, making the plant die dry [28, 29].

species that succeed have no common pests (**Table 2**).

**Table 2.** Plot design for successive crops in greenhouse/tunnel.

Monitoring insects is fundamental in organic farming systems (OFS). Correct identification of insects and insect biology knowledge when they colonize crops is one of the main activities of management decisions that lead to optimal moment. This can be done by simply checking the crop (aphids, spider mites) or by using pheromone traps (thrips, cydia, white fly, rose fly, carrot fly and cabbage moth).

**Figure 4.** (a) Eggplant leaf affected by *Thrips tabaci* (photograph by Stoleru Vasile). (b) Tomato root affected by *Thrips tabaci* (photograph by Stoleru Vasile).

Pests of agricultural crops can cause damage directly (lower leaf surface, destroying fruit), (**Figure 4a**) or indirectly (gale or gates run for various soil diseases, such as *Rhizoctonia* sp. or *Fusarium* sp.), because many pests performing the biological cycle in soil (**Figure 4b**).

Prognosis and warning are performed by the centers dealing with plant protection, and they establish, at the right moment, the imminent danger of setting off massive pest attacks.

## *2.1.7. Management practices when it comes to pest control*

Cultural activities in organic farming may be considered as specific as crop production practices that implemented in the initial stages of the organic farm plan to reduce the likelihood of insect pest infestation. These measures are based on disrupting the biological cycle of the pest as follows: an unavailable crop to pests in space and time; unacceptable crop to pests by interfering with location; reducing the pest on the crop by natural enemies, etc.

Cultural practices are among the oldest techniques used for pest suppression, and many of the practices used in conventional and organic farming today have their roots in traditional agriculture. Effective deployment of cultural tactics is information intensive; it requires knowledge of pest–crop interactions and about the natural enemies of the pests.

## *2.1.8. Intercropping system*

Intercropping is the practice of growing two or more crops (usually different families) in the same area. Strip cropping is a derivation of intercropping and is the practice of growing two or more crops in alternating strips across a field. Both practices serve to increase biodiversity and make the habitat less suitable for pest development (**Figure 5a, b**).

**Figure 5.** (a) Intercropping management of the runner bean with maize (photograph by Hamburda Silvia). (b) Inter‐ cropping management of the runner bean with sunflower (photograph by Hamburda Silvia).

## *2.1.9. Tillage management*

Prognosis and warning are performed by the centers dealing with plant protection, and they establish, at the right moment, the imminent danger of setting off massive pest attacks.

Cultural activities in organic farming may be considered as specific as crop production practices that implemented in the initial stages of the organic farm plan to reduce the likelihood of insect pest infestation. These measures are based on disrupting the biological cycle of the pest as follows: an unavailable crop to pests in space and time; unacceptable crop to pests by

Cultural practices are among the oldest techniques used for pest suppression, and many of the practices used in conventional and organic farming today have their roots in traditional agriculture. Effective deployment of cultural tactics is information intensive; it requires

Intercropping is the practice of growing two or more crops (usually different families) in the same area. Strip cropping is a derivation of intercropping and is the practice of growing two or more crops in alternating strips across a field. Both practices serve to increase biodiversity

**Figure 5.** (a) Intercropping management of the runner bean with maize (photograph by Hamburda Silvia). (b) Inter‐

cropping management of the runner bean with sunflower (photograph by Hamburda Silvia).

interfering with location; reducing the pest on the crop by natural enemies, etc.

knowledge of pest–crop interactions and about the natural enemies of the pests.

and make the habitat less suitable for pest development (**Figure 5a, b**).

*2.1.7. Management practices when it comes to pest control*

28 Integrated Pest Management (IPM): Environmentally Sound Pest Management

*2.1.8. Intercropping system*

Much of the pest population from both soil and foliar can be influenced through tillage practices. Tillage systems reduce insect pressure in succeeding crops. Fields are usually tilled in the fall or early spring when many kinds of insects are in the overwintering stage within the soil or in crop residues. Direct destruction of the insect or its overwintering chamber, removal of the protective cover, elimination of food plants, and disruption of the insect life cycle generally kills many of the insects through direct contact, starvation or exposure to predators, and weather.

Crop irrigation by sprinkler reduces the number of pests in crops [30]. Irrigation by culverts reduces the number of galas in the soil and thus causes interruption of the biological cycle of soil insects.

### *2.1.10. Mulches*

Mulch is a layer film of material applied to the soil surface for the following reasons: to conserve moisture, to improve the fertility and health of the soil, to reduce weed growth, and to pressure soil land crop infestation with different pests [31].

Mulch is usually but not exclusively organic in nature (**Figure 6a**). It may be non-biodegradable (e.g., plastic sheeting) or biodegradable (e.g., bark chips). It may be applied to bare soil or around existing plants. Mulch consisting of manure or compost is incorporated naturally into the soil through the activity of worms and other organisms [32].

**Figure 6.** (a) Organic cabbage mulched with phacelia (photograph by Stoleru Vasile). (b) Organic cabbage mulched with biodegradable plastic (photograph by Stoleru Vasile).

All mulch types suppress insects in comparison with bare soil. Different colors of plastic have been tested; clear, white, yellow, or aluminum (reflective) colors may provide some additional suppression of aphids and whiteflies [33]. Blue and yellow may bring in more pests. Plastic can be painted the desired color (**Figure 6b**). Before choosing a mulch type, farmers should check with their certifier bodies to see whether the practice is allowable by organic regulations [34].

## *2.1.11. Optimum crop health*

The driving force behind the sustainability and environmental preservation derived through organic farming comes through healthy living soil. Microbes in the soil process organic matter to provide a balance of minerals and nutrients which are utilized by plants to achieve healthy, vigor crop growth. When this balance is achieved, the associated health of the crop gives it a heightened ability to withstand pest and disease attack. Good crop husbandry and hygiene also make a significant contribution to the health of the crop and the prevention of pest problems.

## *2.1.12. "Host weed" removal*

Numerous dangerous species find favorable conditions for the summer or winter diapause on the spontaneous vegetation from the forest skirt, the borderline of strip ground, roads, or railways or the less cared for agricultural crops. So, the cabbage aphid has as host plant the cole, and the Colorado beetle has as host plant the black nightshade—*Solanum nigrum* [8].

Storing crops in hygienic conditions generally represents an additional source of pest infesta‐ tion. (e.g., the bean weevil (*Acanthoscelides obsoletus*), pea weevil—*Bruchus pisorum*). They can be fought against either by storing the products in refrigerated storerooms for a certain period of time or by vacuuming the products in a special room [35].

## **2.2. Curative measures**

Curative care or curative measure is the health care given for environmental conditions where a measure is considered achievable, or even possibly so, and directed to this end. Curative care differs from the preventive method, which aims at preventing the appearance of pests, which concentrates on reducing the degree of the attack.

## *2.2.1. Physical–mechanical methods*

According to specific regulation (EU 834/2007), in OA, it can be used following measures: thermotherapy, heliotherapy, radiotherapy, ultrasounds, nets, fences, or traps.

Thermotherapy is recommended only if the vegetal remains are highly infested with pests and, as much as possible, after collecting and removing the remains from the cultivated area. In OA according to EU Regulation 834/2007, this method is restrictive and can be applied only in problematic crops. If this is not possible, in situ burning may be used, but only after a thorough investigation of the opportunity of such a measure and registering it in the farm register and announcing the local organization of environmental protection (EU 889/2008).

Heliotherapy. The method is very simple and has been the subject of thorough research studies carried out at the Central Food Technological Research Institute in India [1]. This method consists of exposing the infested seeds to a temperature of 60°C for 10 min [17]. In order to do so, seeds are put in a dark color polyethylene bag with high molecular and density weight, which, at its turn, is tightly covered by another transparent low density polyethylene bag. The entire operation is carried out on a plane surface exposed to sun. The two foils act as a condenser making the temperature inside the seed bag quickly increase leading to the pests' death.

Radiotherapy is used for sterilizing males with the aid of X-rays and gamma radiations. Achieving the dominant lethal mutations has led to obtaining a biological method called autocide.

**Figure 7.** Ultrasound for pest control (photograph by Stoleru Vasile).

check with their certifier bodies to see whether the practice is allowable by organic regulations

The driving force behind the sustainability and environmental preservation derived through organic farming comes through healthy living soil. Microbes in the soil process organic matter to provide a balance of minerals and nutrients which are utilized by plants to achieve healthy, vigor crop growth. When this balance is achieved, the associated health of the crop gives it a heightened ability to withstand pest and disease attack. Good crop husbandry and hygiene also make a significant contribution to the health of the crop and the prevention of pest

Numerous dangerous species find favorable conditions for the summer or winter diapause on the spontaneous vegetation from the forest skirt, the borderline of strip ground, roads, or railways or the less cared for agricultural crops. So, the cabbage aphid has as host plant the cole, and the Colorado beetle has as host plant the black nightshade—*Solanum nigrum* [8].

Storing crops in hygienic conditions generally represents an additional source of pest infesta‐ tion. (e.g., the bean weevil (*Acanthoscelides obsoletus*), pea weevil—*Bruchus pisorum*). They can be fought against either by storing the products in refrigerated storerooms for a certain period

Curative care or curative measure is the health care given for environmental conditions where a measure is considered achievable, or even possibly so, and directed to this end. Curative care differs from the preventive method, which aims at preventing the appearance of pests, which

According to specific regulation (EU 834/2007), in OA, it can be used following measures:

Thermotherapy is recommended only if the vegetal remains are highly infested with pests and, as much as possible, after collecting and removing the remains from the cultivated area. In OA according to EU Regulation 834/2007, this method is restrictive and can be applied only in problematic crops. If this is not possible, in situ burning may be used, but only after a thorough investigation of the opportunity of such a measure and registering it in the farm register and

Heliotherapy. The method is very simple and has been the subject of thorough research studies carried out at the Central Food Technological Research Institute in India [1]. This method consists of exposing the infested seeds to a temperature of 60°C for 10 min [17]. In order to do

thermotherapy, heliotherapy, radiotherapy, ultrasounds, nets, fences, or traps.

announcing the local organization of environmental protection (EU 889/2008).

of time or by vacuuming the products in a special room [35].

30 Integrated Pest Management (IPM): Environmentally Sound Pest Management

concentrates on reducing the degree of the attack.

[34].

problems.

*2.1.11. Optimum crop health*

*2.1.12. "Host weed" removal*

**2.2. Curative measures**

*2.2.1. Physical–mechanical methods*

Scientifically, literature mentioned the effects of X-ray irradiation applied on six floriculture insect pests (*Tetranychus urticae*, *Myzus persicae*, *Bemisia tabaci*, *Liriomyza trifolii*, *Spodoptera litura*, and *Frankliniella intonsa*) placed in the bottom sections of rose and chrysanthemum pots. After irradiation with an X-ray dose of 150 Gy, the development of nymphs and adults of *M. persicae* and eggs, nymphs, and adults of *B. tabaci* was prevented at every position in the pots. *T. urticae* nymphs irradiated at 200 Gy newly emerged adults laid eggs in the bottom section of rose boxes only. *L. trifolii* adults irradiated at 200 Gy were completely inhibited. Radiother‐ apy method depends on dose of X-ray irradiation, insects, and crops [10].

Other physical or mechanical methods refer to installing various barriers, such as: nets for carrot fly, ultrasounds for soil insects (**Figure 7**), metallic fences for snails (**Figure 8**), layers for aphids and Lepidoptera's insects (**Figure 9**), traps or rollers (carrot fly, thrips) (**Figure 10**), flooding, and crushing the eggs of caterpillars or even the adults.

**Figure 8.** Metallic fence for protection against the snail (photograph by Stoleru Vasile).

**Figure 9.** Early crops protected with Agryl P17 (photograph by Stoleru Vasile).

**Figure 10.** Thrips and whitefly plaque applied in tomato crops (photograph by Stoleru Vasile).

Flooding provides better results in fighting against underground pests (mice, moles, crickets, etc.) by flooding their galleries. The impossibility of knowing the exact side of their galleries reduces the method's practical value and limits its use [36].

## *2.2.2. Biotechnical methods*

**Figure 8.** Metallic fence for protection against the snail (photograph by Stoleru Vasile).

32 Integrated Pest Management (IPM): Environmentally Sound Pest Management

**Figure 9.** Early crops protected with Agryl P17 (photograph by Stoleru Vasile).

**Figure 10.** Thrips and whitefly plaque applied in tomato crops (photograph by Stoleru Vasile).

Installing food bait traps. They can consist of parts of plants, fruits, tubercles, or feed and are placed on the ground or in storehouses. After collecting the pests, traps are removed, soaked in boiling water or burnt [31, 37].

Installing pheromone traps. Pheromones are chemical substances secreted and spread outside the body and determine a response only from the individuals of the same species (**Figure 11**). There are multiple types of pheromones, according to the role they fulfill: sexual, alarm, aggregation, path marking, recognition, and social regulation (e.g., ATRAGAM and ATRA‐ POM are a sexual pheromone used for *Autographa gamma* and *Cydia pomonella*) [8, 38].

**Table 4** presents other products that can be applied in organic farming, based on the phero‐ mones.

**Figure 11.** Attractive traps for pests control in tomato crops (photograph by Stoleru Vasile).

Natural enemies (predators and parasites). This category includes methods in order to attract animals that eat insects and other harmful living animals.


**Table 4.** Pheromones and attractants for organic farming.

The effect of control pest in OA is to increase functional biodiversity, that is, to use wild flowers to attract parasitoids into the cabbage field—or to retain them if we release them—to increase natural pest control, directly through the added plants and the organisms that use them as resources and indirectly through the reduction of pesticides.

Creating proper shelters and feed for the useful fauna (frogs, green lizards, snakes, insectivore insects, and mammals), including their artificial breeding, have positive effects for farmers. Snakes can be used against rodents; hedgehogs counteract the attack of shell-less snails, mice, mole crickets, and also the Colorado beetles [39].

Predators catch and eat their prey. Some common predatory arthropods include ladybird beetles, carabid (ground) beetles, staphylinid (rove) beetles, syrphid (hover) flies, lacewings, minute pirate bugs, nabid bugs, big-eyed bugs, and spiders.

Entomophagy predators are species of animals which consume other animals, pests in particular.

The main species of insects and nematodes used for fighting against harmful insects are pre‐ sented in **Table 5**. This method of biological control is widely used in horticulture, especially in protected areas, such as flower, orchard, and vegetables crops (**Figures 12**–**17**).



**Name of product Pest Crop Pheromone/attractant Application**

Codling moth Apples Pheromone attracts male

Rollertrap® Range of insects Various Two sided sticky trap Yellow and blue

The effect of control pest in OA is to increase functional biodiversity, that is, to use wild flowers to attract parasitoids into the cabbage field—or to retain them if we release them—to increase natural pest control, directly through the added plants and the organisms that use them as

Creating proper shelters and feed for the useful fauna (frogs, green lizards, snakes, insectivore insects, and mammals), including their artificial breeding, have positive effects for farmers. Snakes can be used against rodents; hedgehogs counteract the attack of shell-less snails, mice,

Predators catch and eat their prey. Some common predatory arthropods include ladybird beetles, carabid (ground) beetles, staphylinid (rove) beetles, syrphid (hover) flies, lacewings,

Entomophagy predators are species of animals which consume other animals, pests in

The main species of insects and nematodes used for fighting against harmful insects are pre‐ sented in **Table 5**. This method of biological control is widely used in horticulture, especially

> *Aphidius colemani* parasitic wasp

> *Aphidius colemani* parasitic wasp

*Aphidoletes aphidimyza* (gall midge)

Preventive = 0.25 ex./m2

Preventive = 0.25 ex./m2

Curative light = 1 ex./m2

interval, 3–6 application/year)

, curative heavy = 2 ex./m2

, curative heavy =2 ex./m2

(continuously application)

days interval, continuously application)

ex./m2

0.5 ex./m2

10 ex./m2

, curative light = 1

, curative light =

, curative heavy =

(7 days

(7

in protected areas, such as flower, orchard, and vegetables crops (**Figures 12**–**17**).

**Name of products Pests controlled Crops Parasites/predators Application/dose**

Protected crops

Protected crops

crops

crops

crops

Pheromone trap® Butterflies and moths Protected and field

34 Integrated Pest Management (IPM): Environmentally Sound Pest Management

Agralan Envirofleece® Various pests Protected and field

resources and indirectly through the reduction of pesticides.

minute pirate bugs, nabid bugs, big-eyed bugs, and spiders.

**Table 4.** Pheromones and attractants for organic farming.

mole crickets, and also the Colorado beetles [39].

moths, for monitoring only

Monitors butterfly and moth population

Polypropylene fleece, physical barrier to pests 8 traps/ha

5–8 traps/ha

17–30 g/m2

Codling Moth Pagoda Trap with lure®

particular.

Aphipar® Aphids (cotton

Ervipar® Aphids (potato

aphid,

aphid,

aphid)

Aphidend® Aphids Protected

peach and potato aphid, tobacco aphid

glasshouse potato


**Table 5.** Parasites and predators permitted for organic pest control.

**Figure 12.** *Encarsia formosa* for greenhouse crops (photograph by Stoleru Vasile).

**Figure 13.** Applying the parasite wasp to a cucumber crop (photograph by Stoleru Vasile).

**Name of products Pests controlled Crops Parasites/predators Application/dose**

Slugs Various *Phasmarhabditis*

Protected crops

crops

Vine weevil Various *Heterorhabditis*

crops

Protected crops

Various *Hypoaspis aculeifer* or *Hypoaspis miles* predatory mites

> *hermaphrodita* nematode

*Amblyseius cucumeris* predatory mite

*Orius laevigatus*, *Orius insidiosus* or *Orius majusculus* predatory bug

*megidis* nematode

*Encarsia formosa* parasitic wasp

*Macrolophus caliginosus* predatory bug Preventive = 100 ex./m2

200 ex./m2 , curative heavy = 500 ex./m2

application)

100 ex./m2

1 ex./m2

heavy = 1,000,000/m2

= 9 ex./m2

= 50 ex./m2

curative heavy = 100 ex./m2

500–1000 ex./m2

Preventive = 50 ex./m2

Preventive = 0.5 ex./m2

(one application/14 days)

Curative light = 500,000/m2

Preventive = 1.5–3 ex./m2

curative light = 3–6 ex./m2

Curative light = 10 ex./m2

(one applic./week)

(one applic./14 days)

, curative light =

(one

, curative light =

, curative light =

, curative

, curative heavy

, curative heavy

(application at 14 days),

(one application/week)

, curative heavy = 10 ex./m2

(one application)

,

Entomite® Soil-living insects,

Nemaslug® Slugsure®

Thripex® Fightathrip®

Thripor® Fightabug®

Larvanem® Nemasys H® files

thrips, collembola, nematodes, sciarid

36 Integrated Pest Management (IPM): Environmentally Sound Pest Management

Thrips (various), spider mites

En-strip® Whitefly Protected

leafhopper, leaf miner, spider mite

**Table 5.** Parasites and predators permitted for organic pest control.

**Figure 12.** *Encarsia formosa* for greenhouse crops (photograph by Stoleru Vasile).

Fightafly B® Whitefly,

Thrips (various) Protected

**Figure 14.** *Trichogramma* eggs plaques made in a laboratory (photograph by Stoleru Carmen).

**Figure 15.** Application of *Trichogramma* plaques for white butterfly eggs (photograph by Stoleru Carmen).

**Figure 16.** Tomato fruit damage by *Helicoverpa armigera* (photo by Deleanu Florina).

**Figure 17.** Whitefly in on the flower crop (photograph by Stoleru Vasile).

Biological methods. Biological control consists of using organisms and products against other living beings. The methods correspond to the future approaches; they are characterized by high selectivity and improbability levels regarding the fact of inducing the pest resistance phenomena, as well as a good capacity of self-perpetuation.

Economically speaking, these methods are more expensive, at least initially, when they have to be projected and produced, or when special installations are necessary and they require a lot of manual work for operation or for the uphill works. But in the end, does not the envi‐ ronment's health and ours implicitly deserve a bonus from the beneficiary?

**Figure 18.** Multitrophic lifestyle of fungal parasites [38].

**Figure 16.** Tomato fruit damage by *Helicoverpa armigera* (photo by Deleanu Florina).

38 Integrated Pest Management (IPM): Environmentally Sound Pest Management

**Figure 17.** Whitefly in on the flower crop (photograph by Stoleru Vasile).

phenomena, as well as a good capacity of self-perpetuation.

Biological methods. Biological control consists of using organisms and products against other living beings. The methods correspond to the future approaches; they are characterized by high selectivity and improbability levels regarding the fact of inducing the pest resistance

**Figure 19.** *B. bassiana* parasitism for *Bemisia tabaci* control (photograph by Sellitto Michele).

Microbiological control is a modern, efficient method but still quite expensive; it consists of using certain preparations based on living organisms (viruses, bacteria, fungi) that parasites and kill some of the pests.

Nowadays, more than 500 species of insect parasite fungi are known. Their advantage is that they spread out easily through spores and they are resistant to unfriendly conditions for long periods of time (**Figure 18**). In general, the relation between pests and their parasites are affected by global change, abiotic and biotic stresses to crops [40].

*Beauveria* sp. and *Metarhizium* sp. are two pathogenic fungi for insects which can penetrate the host insect through its exoskeleton due to its production of chitinolytic enzymes (**Figures 19** and **20**). Once inside the host, the fungus develops and feeds, causing its host's death.

The infested insects, still living, experience limited motion ability and the incapacity to feed themselves; moreover, they represent a source of infection for other insects [37].

**Figure 20.** *B. bassiana* on palm carbide (*Rhynchophorus ferrugineus*) (photograph by Sellitto Michele).

**Figure 21.** Conidi of *Pochonia chlamydospores* (photograph by Sellitto Michele).

Different studies have shown that *Beauveria* sp. and *Metarhizium* sp. actively control species from the following genera Coleoptera (*Melolontha* sp., *Diabrotica* sp.), Lepidoptera (*Tuta absoluta*), or Orthoptera [aphids, greenhouse whitefly, thrips, [41, 42] etc].

*Pochonia* sp. is a hyphomycete that acts as a parasite of nematode eggs. Its antagonistic activity is related to the production of proteolytic and chitinolytic enzymes that degrade the cellular structure of nematodes, especially that of eggs and females in the early stage (**Figures 21** and **22**).

**Figure 22.** Tubers of a potato attacked by nematodes (photograph by Aurelio Ciancio).

Nowadays, more than 500 species of insect parasite fungi are known. Their advantage is that they spread out easily through spores and they are resistant to unfriendly conditions for long periods of time (**Figure 18**). In general, the relation between pests and their parasites are

*Beauveria* sp. and *Metarhizium* sp. are two pathogenic fungi for insects which can penetrate the host insect through its exoskeleton due to its production of chitinolytic enzymes (**Figures 19** and **20**). Once inside the host, the fungus develops and feeds, causing its host's death.

The infested insects, still living, experience limited motion ability and the incapacity to feed

themselves; moreover, they represent a source of infection for other insects [37].

**Figure 20.** *B. bassiana* on palm carbide (*Rhynchophorus ferrugineus*) (photograph by Sellitto Michele).

**Figure 21.** Conidi of *Pochonia chlamydospores* (photograph by Sellitto Michele).

affected by global change, abiotic and biotic stresses to crops [40].

40 Integrated Pest Management (IPM): Environmentally Sound Pest Management

*Arthrobotrys* sp. is a fungus that parasitizes nematodes. The nematodes' biocontrol activity is related to the production of ring-like structures which swallow when a nematode pass by and catches it. Afterwards, the nematode is degraded by enzymes and used by the fungus as feed.

The combination between *Pochonia* sp. and *Arthrobotrys* sp. represents the most effective biological control method for the nematodes from a genera *Meloidogyne* sp., *Globodera* sp., and *Heterodera* sp*.* (**Figures 23** and **24**).

**Figure 23.** Adult of a nematode parasited by *Pochonia chlamydospores* (photograph by V.M. Sellitto, 2014).

**Figure 24.** Egg of a nematode parasited by *Pochonia chlamydospores* (photograph by L. Lopez-Llorca, 2015).

The literature dealing with this subject mentions tests that proved that the use of these fungi, on soils sterilized using chemical products and solarization and steam, has maintained the soil and the level of nematodes below the damaging threshold for many years, compared to the soils where these fungi were not present [43].

*Lecanicillium lecanii* is a pathogenic fungus for numerous species of insects. This fungus acts as follows: the fungus spores lie and remain on the insects' exoskeleton, and then, they germinate and mechanically penetrate the insects' exoskeleton, due to their production of chitinolytic enzymes. From the industrial products containing entomopathogenic fungi, we mention the following: Muscardin M 45® and *Beauveria* spores (from *B. bassiana*), Boverin® (from *B. densa*), and Mitecidin® (from *Streptomyces aureus*), which act against the Colorado beetle and other coleopters (**Table 6**). Applying myco-insecticides, Naturalis-L® (*Beauveria bassiana*) and PreFeRal®WG (*Paecilomyces fumosoroseus*), were applied against adult *Rhagoletis cerasi* (Diptera: Tephritidae). In the first case, *B. bassiana* significantly reduced the number of damaged fruit (efficacy: 69–74%), whereas damage was not significantly reduced with PreFeRal®WG (efficacy: 27%) [44].


**Table 6.** Biological control agents used in organic farming.

Once the fungus is in, it develops and digests the insect from the inside until it kills it. Infested insects die in 4–6 days and are then covered with a whitish efflorescence, depending on the fungus sporulation. Thus, these insects become a source of infection for other insects. In addition, *Lecanicillium lecanii* can colonize certain tissues of the host plant, achieving an induced systemic resistance.

Many studies have shown that *L. lecanii* controls aphids, whitefly, and Thripidae genus. Other studies have proven that *Lecanicillium* sp*.* also controls certain nematode species as well as certain plant diseases, such as the gray mold (**Table 7**).


**Table 7.** Microbiological products to control pests from vegetable crops.

**Figure 24.** Egg of a nematode parasited by *Pochonia chlamydospores* (photograph by L. Lopez-Llorca, 2015).

**Name of product Pest Crop Microorganisms Dose/application**

spores

Protected crops *Verticillium lecanii* fungal spores

kurstaki

*kurstaki*

wettable powder

*Bacillus thuringiensis* var.

2 g/L

applic.)

2–4 tsp/gal water

curative light = 0.1% (2–3 applic.), curative heavy = 0.1% (3–4

1–1.6 kg/ha, depending of crop

1–1.6 kg/ha, depending of crop

Vertalec® Aphids Protected crops *Verticillium lecanii* fungal

Caterpillars Vegetables, fruit,

Bactospeine® Caterpillars Various *Bacillus thuringiensis*

**Table 6.** Biological control agents used in organic farming.

Thuricide® Caterpillars Various *Bacillus thuringiensis* var.

ornamentals

soils where these fungi were not present [43].

42 Integrated Pest Management (IPM): Environmentally Sound Pest Management

PreFeRal®WG (efficacy: 27%) [44].

Mycotal® Whitefly, thrip

Novosol FC® Dipel WP® Bactura WP®

larvae

The literature dealing with this subject mentions tests that proved that the use of these fungi, on soils sterilized using chemical products and solarization and steam, has maintained the soil and the level of nematodes below the damaging threshold for many years, compared to the

*Lecanicillium lecanii* is a pathogenic fungus for numerous species of insects. This fungus acts as follows: the fungus spores lie and remain on the insects' exoskeleton, and then, they germinate and mechanically penetrate the insects' exoskeleton, due to their production of chitinolytic enzymes. From the industrial products containing entomopathogenic fungi, we mention the following: Muscardin M 45® and *Beauveria* spores (from *B. bassiana*), Boverin® (from *B. densa*), and Mitecidin® (from *Streptomyces aureus*), which act against the Colorado beetle and other coleopters (**Table 6**). Applying myco-insecticides, Naturalis-L® (*Beauveria bassiana*) and PreFeRal®WG (*Paecilomyces fumosoroseus*), were applied against adult *Rhagoletis cerasi* (Diptera: Tephritidae). In the first case, *B. bassiana* significantly reduced the number of damaged fruit (efficacy: 69–74%), whereas damage was not significantly reduced with

From the bacteria used to fight against insects, *Bacillus thuringiensis* (**Figure 25**) and *B. subtil‐ lis* are the most popular (**Figure 26**).

**Figure 25.** *Bacillus thuringiensis var. kurstaki (photograph by V.M. Sellitto).*

**Figure 26.** *Bacillus subtillis* (photograph by V.M. Sellitto).

During the last years, strains of *B. thuringiensis* were studied for their effect on the insect, through different toxins (**Table 8**).


**Table 8.** Toxins produced by strains of *Bacillus thuringiensis*.

It laid at the basis of the process of obtaining numerous commercial products: Agritol®, Dipel®, Thuricide®, Novodor 3FC®, Vectobac®, Bactospeine®, Thuringine®, Entobakterin®, Thurintox®, or Foray®. These products are highly efficient in counteracting the larvae of certain butterflies from vegetables crops [37].

Out of more than 300 viruses that cause diseases for more than 175 species of insects, polyhedric viruses are the most known; they are used at obtaining certain preparations industrially, such as Biotrol VHZ® and VSE®, Vitex® (against caterpillars), and Virin-ENS® (recommended in fighting against the cabbage moth). Nuclear polyhedrosis viruses (NPV) and granulosis viruses (GV) are available to get rid of some caterpillar pests (*Mamestra brassicae, Helicoverpa armigera, Autographa gamma, Pieris brassicae, and Euproctis chrysorrhoea*) [45] (**Figure 27**).

**Figure 27.** Uninfected (bottom) beet armyworm (*Spodoptera exigua*) and beet armyworm killed by the nuclear polyhed‐ rosis virus. Photograph credit: David Nanace, USDA ARS.

Genetic methods. The works of ameliorating plants have as their main objective the production of cultivars endowed with greater resistance. This is why the forms providing higher me‐ chanical resistance are promoted (with thicker cuticle or suber, with a waxy protective layer or with abundant porosity), physiological or chemical (by growing the content of substances with repellent or insecticide effect).

Several aphid species can proliferate in winter lettuce crops, such as *Nasonovia ribisnigri* (Mosley), *Myzus persicae* (Sul.), *Aulacorthum solani* (Kalt.), *Macrosiphum euphorbiae* (Th.), and *Hyperomyzus lactucae* (L.). *N. ribisnigri* is the most damaging one because it preferentially develops in the lettuce heart [46, 47]. In addition to feeding damage and the loss of product quality due to their presence when the lettuce is marketed, aphids are also vectors of viruses, such as the lettuce mosaic virus. Finally, slugs (*Deroceras* sp. and *Arion* sp.) and snails can also cause feeding damage to lettuce in winter.

Complete resistance to the aphid *N. ribisnigri* and partial resistance to *M. persicae* are conferred by a dominant gene called Nr, which has been introduced in many European cultivars [48]. However, this resistance was recently bypassed by a new *N. ribisnigri* biotype named Nr:1 [49].

## *2.2.3. Using plants to fight against pests*

**Figure 26.** *Bacillus subtillis* (photograph by V.M. Sellitto).

44 Integrated Pest Management (IPM): Environmentally Sound Pest Management

1 Cry toxins Pore formation on cell membrane; cytolysis activity

2 Vip toxins Wide spectrum of insect activity

4 Hemolysin Lysis of vertebrate red blood cells 5 Beta-exotoxins Inhibition of RNA polymerase 6 Phospholipase-C Cell membrane alteration

**Table 8.** Toxins produced by strains of *Bacillus thuringiensis*.

certain butterflies from vegetables crops [37].

through different toxins (**Table 8**).

**No. Toxins Activities**

3 Thuricin Bacteriocin

During the last years, strains of *B. thuringiensis* were studied for their effect on the insect,

It laid at the basis of the process of obtaining numerous commercial products: Agritol®, Dipel®, Thuricide®, Novodor 3FC®, Vectobac®, Bactospeine®, Thuringine®, Entobakterin®, Thurintox®, or Foray®. These products are highly efficient in counteracting the larvae of

Out of more than 300 viruses that cause diseases for more than 175 species of insects, polyhedric viruses are the most known; they are used at obtaining certain preparations industrially, such as Biotrol VHZ® and VSE®, Vitex® (against caterpillars), and Virin-ENS® (recommended in fighting against the cabbage moth). Nuclear polyhedrosis viruses (NPV) and granulosis viruses (GV) are available to get rid of some caterpillar pests (*Mamestra brassicae, Helicoverpa armigera, Autographa gamma, Pieris brassicae, and Euproctis chrysorrhoea*) [45] (**Figure 27**).

This method relies on certain plants' feature of secreting in the earth or in the air certain substances with repulsive or destructive effects on pests. By and large, these plants can be cultivated in the field, as border or associated with the crops. The important species with insecticide effect are presented in **Table 9**.

Biochemical methods. The products used for protecting plants against harmful insects can be classified according to the raw material used, into two categories: vegetal insecticides and mineral insecticides.


**Table 9.** Plants used in organic farming with a repellent effect.

Vegetal insecticides. Insecticides of natural origin are substances which can cause the death of insects interfere in the development or reproduction being responsible to attract or repel them. Today, worldwide, there are more than 1450 species of plants with insecticide effects, from which only approximately 50 are useful [1]. As far as our country is concerned, too little from the 200 species credited with this action have been or are being effectively used in this purpose, and even fewer have been studied from this point of view.

Stinging nettle (*Urtica dioica*). Action: it stimulates plant growth, it slows down the attack of certain insects, counteracts aphids, and spiders before the formation of leaves and flowers [37].

Fern (*Dryopteris filix-mas*). Leaf purine and decoction, undiluted, are used against shell-less snails (every time needed). At the same time, this product, diluted 10 times with water, is used for the late spring treatments against aphids.

Wormwood (*Artemisia absinthium*). This plant can be used as an undiluted purine (caterpillars, lice), cold extract diluted twice for Solanaceae against the larvae of the Colorado beetle [37], or decoction is used undiluted against the cabbage fly [2].

Tansy (*Tanacetum vulgare*) is used as an undiluted infusion every time it is needed against ants, aphids, fleas and other insects.

Wild garlic (*Allium ursinum*). Wild garlic infusion is used undiluted, by repeatedly aspersing the plants every 3 days against aphids and mites. Purine is also used undiluted against the carrot fly (*Psila rosae*), but only during its flight period.

Garlic (*Allium sativum*). It can be used in the treatment of mites and also in seed treatments. Garlic in its natural state is eventually cultivated in rows, has a nematode effect (*Meloidogyne* sp.), and drives away the striped field mouse.


**Table 10.** The action spectrum of the *Chrysanthemum cinerariaefolium* extract.

Biochemical methods. The products used for protecting plants against harmful insects can be classified according to the raw material used, into two categories: vegetal insecticides and

mineral insecticides.

**Species Controlled pests**

46 Integrated Pest Management (IPM): Environmentally Sound Pest Management

Queen of poisons (*Aconitum* sp*.*) Coleopteran larvae Sweet flag (*Acorum calamus*) White cabbage butterfly Onion (*Allium cepa*) Mites, ants, storehouse pests Garlic (*Allium sativum*) Thrips, storehouse pests

Hemlock (*Conium maculatum*) Coleopteran larvae

Spurge (*Euphorbia* sp.) Caterpillars, aphids White sweet clover (*Melilotus albus*) Colorado beetle Mint (*Mentha* sp.) Colorado beetle

Yew (*Taxus baccata*) Various insects Field penny-cress (*Thlaspi arvense*) Bed bug (repellent) Common nettle (*Urtica dioica*) Aphids, mites Mullein (*Verbascum phlomoides*) Colorado beetle

**Table 9.** Plants used in organic farming with a repellent effect.

for the late spring treatments against aphids.

and even fewer have been studied from this point of view.

Birthwort (*Aristolochia clematitis*) Bed bug

Yarrow (*Achillea millefolium*) Aphids, mites, psyllids, thrips

Absinthium (*Artemisia absinthium*) Nematodes, caterpillars, fleas Mugwort (*Artemisia vulgaris*) Fleas, Colorado beetle

Lamb's quarters (*Chenopodium album*) Colorado beetle, white butterfly

Tobacco (*Nicotiana tabacum*) Aphids, mites, Colorado beetle

Coriander (*Coriandrum sativum*) Aphids, spiders, Colorado beetle (repellent effect)

Black nightshade (*Solanum nigrum*) Aphids, mites, Colorado beetle, cabbage butterfly

Vegetal insecticides. Insecticides of natural origin are substances which can cause the death of insects interfere in the development or reproduction being responsible to attract or repel them. Today, worldwide, there are more than 1450 species of plants with insecticide effects, from which only approximately 50 are useful [1]. As far as our country is concerned, too little from the 200 species credited with this action have been or are being effectively used in this purpose,

Stinging nettle (*Urtica dioica*). Action: it stimulates plant growth, it slows down the attack of certain insects, counteracts aphids, and spiders before the formation of leaves and flowers [37].

Fern (*Dryopteris filix-mas*). Leaf purine and decoction, undiluted, are used against shell-less snails (every time needed). At the same time, this product, diluted 10 times with water, is used *Pyrethrum (Chrysanthemum cinerariaefolium, Pyrethrum cinerariaefolium).* Pyrethrum is a contact insecticide having paralyzing effect and a wide range of actions. The great advantage, ecologically speaking, is that it completely decomposes into harmless compounds in only 48 h after application [50]. Pyrethrum is noticed on a large number of insects and mites with a soft body or when they are still in a larval stage, as a solution with concentration of 0.1% (**Table 10**). The extract of pyrethrum cannot recommend mixture with alkaline products, Bordeaux mixture [1, 39].

Derris powder (*Derris* sp*.*). Derris powder is applied to a large number of aphids, nematodes, and insects, more vulnerable as their ingestion capacity is larger (larvae). Its toxicity for warm blooded animals is null, while for the other ones, it is lethal, used as decoct of ground fresh or dried roots, in a solution of 0.01%.

Gliricidia (*Gliricidia sepium*). Action: repellent, parasitic, rodenticide, mixed with grain, left from place to place on a field or put in warehouses; in a few days, it kills the rodents [9, 51].

Neem (*Azadirachta indica*). It is a repellent, hormonal disruptive (it blocks the larval metamor‐ phosis process), nematocide and antimicotic. Azadirachtin is extracted from this plant's seeds, the active substance of NeemAzal T/S®.

The preparations destroy the eggs, larvae, and adults of more than 200 species of field or storehouse pests in the case of beans, cereals, tomatoes, and field plants from the most various classes: nematodes, ants, bed bugs, grasshoppers, etc. Neem oil is used in fighting against certain pests on plants, and ground marc has a nematode effect [33].

Bitter wood (*Quassia amara*). The active substances of this preparation act as contact and ingestion insecticide but are slower than pyrethrum. It is used in fighting against many pests: aphids, flies, cabbage aphids, etc.

Decoct is made from 100 to 150 g chips of bitter wood at 10 l water. The bitter wood decoction can be improved by adding an equal amount of solution of potassium soap in a concentration of 1–2.5% [51].

Traditionally, in organic fruit growing, the apple sawfly *Hoplocampa testudinea* Klug is con‐ trolled by the use of extracts of bitter wood of 6 g/ha/in 500 l. For a good efficiency, the bitter extract can be mixed with Nemmazal T/S® [52, 53].


**Table 11.** Commercial products permitted to use in organic farming.

## *2.2.4. Repellent mineral products*

Potassium alum. This preparation is used as solution with a concentration of 0.4% with good efficacy against lice and caterpillars. At the same time, aspersing the soil with this solution is quite efficacious against shell-less snails. Basalt flour. It is used as a powder. Its action against pests is explained because of a change of the pH at the surface of aerial organs from weak acid (preferred by most pests) to weak alkaline or mechanical action on the insect's body, their eyes, and trachea [2].

## *2.2.5. Insecticide mineral preparations*

Bitter wood (*Quassia amara*). The active substances of this preparation act as contact and ingestion insecticide but are slower than pyrethrum. It is used in fighting against many pests:

Decoct is made from 100 to 150 g chips of bitter wood at 10 l water. The bitter wood decoction can be improved by adding an equal amount of solution of potassium soap in a concentration

Traditionally, in organic fruit growing, the apple sawfly *Hoplocampa testudinea* Klug is con‐ trolled by the use of extracts of bitter wood of 6 g/ha/in 500 l. For a good efficiency, the bitter

Various Rotenone derived

from *Lonchocarpus utilis and L. urucu*

on neem extract

on neem extract

organic products (e.g., grain) must be removed before use

Store Peroxyacetic acid 0.2%

Store Natural pyrethrum.

Potassium alum. This preparation is used as solution with a concentration of 0.4% with good efficacy against lice and caterpillars. At the same time, aspersing the soil with this solution is quite efficacious against shell-less snails. Basalt flour. It is used as a powder. Its action against pests is explained because of a change of the pH at the surface of aerial organs from weak acid (preferred by most pests) to weak alkaline or mechanical action on the insect's body, their eyes,

Various Fatty acid 1–2%, one applic./week

0.8–1 l/ha

tsp./10 l

tsp./10 l

1 l/3000 m3

Insect repellent, 4–6

Insect repellent, 4–6

**Name of product Pests Crops Agent for control Dose/concentration**

Various insects Various Insect repellent based

Various insects Various Insect repellent based

aphids, flies, cabbage aphids, etc.

**Savona®** Whiteflies,

**Liquid Derris®** Various biting and

**AquaPy®** For insects in

**Jet 5®** For cleaning

*2.2.4. Repellent mineral products*

and trachea [2].

extract can be mixed with Nemmazal T/S® [52, 53].

48 Integrated Pest Management (IPM): Environmentally Sound Pest Management

thrips, aphids, mealy bugs, leafhoppers

sucking insects

grain stores

glasshouses /polytunnels

**Table 11.** Commercial products permitted to use in organic farming.

of 1–2.5% [51].

**Bug-Me-Not Bloom and Leaf Astringent Spray (CP) ®**

**Bug-Me-Not Root and Soil Granules**

**(CP) ®**

Potassium soap is successfully used against mites (red spider) and the cabbage aphid. The treatment is applied alone or in combination with other products (horsetail extract) by repeatedly aspersing the plants with various solution types: 200–300 g soap at 10 l water (lice); 200–300 g soap + 0.5 l alimentary alcohol + 1 table-spoonful of lime and 1 table-spoonful of cooking salt at 10 l of water, against the red spider and the larvae of the Colorado beetle [39].

The preparation is used as solution with concentration of 1–2% with good efficacy against lice and leaf fleas, found under the name Neudosan® or Savona® [9], like as other products presented in **Table 11**.

## **Acknowledgements**

The authors wish to thank Mr. Dean Hufstetler for reviewing article.

## **Author details**

Vasile Stoleru1\* and Vicenzo Michele Sellitto2

\*Address all correspondence to: vstoleru@uaiasi.ro

1 Department of Horticulture, University of Agricultural Sciences and Veterinary Medicine, Iasi, Romania

2 Department of Applied Microbiology, Microspore Ltd., Larino, Italy

## **References**


[19] Schneider JHM, s'Jacob JJ, van de Pol PA. Rosa multiflora 'Ludiek', a rootstock with resistant features to the root lesion nematode *Pratylenchus vulnus*. Scientia Horticul‐ turae. 1995;63(1–2):37–45.

[5] Willer H. The World of Organic Agriculture. Statistics and Emerging. Trends 2015.

[6] Knipling EF. Entomology and the Management of Man's Environment. Australian

[7] Hatman M, Bobes I, Lazar A, Gheorghies C, Glodeanu C, Severin V, Tusa C, Popescu I, Vonica I. Phytopatology. Bucharest: Editura Didactica si Pedagogica; 1989. 468 p.

[9] Stoleru V, Albert IO. Vegetable growing using organic measures. Risoprint; Cluj-

[10] Yun S-H, Koo H-N, Kim HK, Yang J-O, Kim G-H. X-ray irradiation as a quarantine treatment for the control of six insect pests in cut flower boxes. Journal of Asia-Pacific

[11] Osouli S, Ziaie F, Haddad Irani Nejad K, Moghaddam M. Application of gamma irradiation on eggs, active and quiescence stages of *Tetranychus urticae* Koch as a quarantine treatment of cut flowers. Radiation Physics and Chemistry. 2013;90:111–9.

[12] Boiteau G, Heikkilä J. Chapter 12 - Successional and Invasive Colonization of the Potato Crop by the Colorado Potato Beetle: Managing Spread. In: Alyokhin A, Giordanengo CV, editors. Insect Pests of Potato. San Diego: Academic Press; 2013. p. 339–71. [13] Zeleke KT, Nendel C. Analysis of options for increasing wheat (*Triticum aestivum* L.) yield in south-eastern Australia: The role of irrigation, cultivar choice and time of

[14] Pfiffner L, Wyss E. Use of sown wildflower strips to enhance natural enemies of agricultural pests. In: Gurr GM, Wratten SD, Altieri MA, editor. Ecological Engineering for Pest Management: Advances in Habitat Manipulation for Arthropods. Colling‐

[15] Munteanu N. Tomatoes, peppers and eggplants. Iasi: Ion Ionescu de la Brad; 2003. 214

[16] Indrea D, Apahidean S, Apahidean M, Maniutiu D, Sima R. Vegetable growing Editor.

[17] Ciofu R, Stan N, Popescu V, Chilom P, Apahidean S, Horgos A, Berar V, Lauer KF, Atanasiu N. Tratat de legumicultura. Bucuresti: Editura Ceres; 2004. 1165 p.

[18] López-Pérez J-A, Le Strange M, Kaloshian I, Ploeg AT. Differential response of Mi generesistant tomato rootstocks to root-knot nematodes (*Meloidogyne incognita*). Crop

sowing. Agricultural Water Management. 2016;166:139–48.

wood, VIC, Australia: CSIRO Publishing; 2004. p. 167–88.

[8] Georgescu T. Horticultural entomology: Dosoftei Publisher; 2006. 426 p.

Frick: FIBL; 2015. 306 p.

Napoca 2007.

p.

Entomology. 2016;19(1):31–8.

Bucuresti: Ceres; 2012. 624 p.

Protection. 2006;25(4):382–8.

Journal of Entomology. 1972;11(3):153–67.

50 Integrated Pest Management (IPM): Environmentally Sound Pest Management


[45] Kalha CS, Singh PP, Kang SS, Hunjan MS, Gupta V, Sharma R. Entomopathogenic viruses and bacteria for insect-pest control. Integrated Pest Management. Academic Press, Elsevier 2014; pp. 225–244.

[31] Gill HK, McSorley R. Impact of different organic mulches on the soil surface arthropod community and weeds. International Journal of Pest Management. 2012;58(1):33–40.

[32] Gill HK, McSorley R, Treadwell DD. Comparative performance of different plastic films for soil solarization and weed suppression. HortTechnology. 2009;19(4):769–774. [33] Brian Caldwell ES, Abby S, Anthony S, Christine S. Resource Guide for Organic Insect and Disease Management. Ithaca, New York: Arnold Printing Corp; 2013. 201 p. [34] Linker HM, Orr DB, Barbercheck ME. Insect management on organic farms. Center for

[35] Stan N, Munteanu N, Stan T. Vegetable Growing. Iasi: Ion Ionescu de la Brad 2003. 316

[36] Lampkin N. The Principles of Organic Farming. U.K.: Farming Press, Miller Freeman;

[37] Calin M. The guide of the recognition and pest control of vegetable in biological

[38] Lind K, Lafer G, Schloffer K, Innerhofer G, Meister H. Organic Fruit Growing. Wall‐

[39] Stoleru V. The management of organic vegetable systems. Iasi: Ion Ionescu de la Brad;

[40] Lopez-Llorca L, editor Fungal parasites of invertebrates: useful tools for adapting crops to global change. International Congress Soil and Food, Resources for a Healthy Life;

[41] Pires L, Marques E, Wanderley-Teixeira V, Teixeira A, Alves L, Alves S. Ultrastrucure of *Tuta absoluta* parasitized eggs and the reproductive potential of females after

[42] Lecuona R, Riba G, Cassier P, Clement JL. Alterations of insect epicuticular hydrocar‐ bons during infection with *Beauveria bassiana* or *B. brongniartii*. Journal of Invertebrate

[43] McSorley R, Wang KH, Rosskopf EN, Kokalis-Burelle N, Hans Petersen HN, Gill HK, Krueger R. Nonfumigant alternatives to methyl bromide for management of nemato‐ des, soil-borne diseases, and weeds in production of snapdragon (*Antirrhinum majus*).

[44] Daniel C, Wyss E. Field applications of Beauveria bassiana to control the European cherry fruit fly *Rhagoletis cerasi*. Journal of Applied Entomology. 2010;134(9–10):675–

parasitism by *Metharhizium anisopliae*. Micron. 2009;40:255–261.

International Journal of Pest Management. 2009;55(4):265–273.

Environmental Farming Systems. 2009:1–37.

52 Integrated Pest Management (IPM): Environmentally Sound Pest Management

agriculture. Bacau: Tipoactiv; 2005. 376 p.

ingfors: CABI Publishing; 2003. 282 p.

p.

2001.

2013. 250 p.

81.

2015; Iasi: UASVM Iasi.

Pathology. 1991;58(1):10–18.


## **Entomopathogenic Nematodes in Pest Management**

Ugur Gozel and Cigdem Gozel

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/63894

#### **Abstract**

The definition "biological control" has been used in different fields of biology, most notably entomology and plant pathology. It has been used to describe the use of live predatory insects, entomopathogenic nematodes (EPNs) or microbial pathogens to repress populations of various pest insects in entomology. EPNs are among one of the best biocontrol agents to control numerous economically important insect pests, successfully. Many surveys have been conducted all over the world to get EPNs that may have potential in management of economically important insect pests. The term "entomopathogenic" comes from the Greek word *entomon* means insect and *pathogen‐ ic* means causing disease and first occurred in the nematology terminology in refer‐ ence to the bacterial symbionts of *Steinernema* and *Heterorhabditis*. EPNs differ from other parasitic or necromenic nematodes as their hosts are killed within a relatively short period of time due to their mutualistic association with bacteria. They have many advantages over chemical pesticides are in operator and end-user safety, absence of withholding periods, minimising the treated area by monitoring insect populations, minimal damage to natural enemies and lack of environmental pollution. Improve‐ ments in mass-production and formulation technology of EPNs, the discovery of numerous efficient isolates and the desirability of increasing pesticide usage have resulted in a surge of scientific and commercial interest in these biological control agents.

**Keywords:** biological control, safety, entomopathogenic nematodes, *Steinernema*, *Het‐ erorhabditis*

© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

## **1. Entomopathogenic nematodes**

## **1.1. General information of entomopathogenic nematodes**

Entomopathogenic nematodes (EPNs) are soil-inhabiting, lethal insect parasites that belong to the Phylum Nematoda from the families Steinernematidae and Heterorhabditidae, and they have proven to be the most effective as biological control organisms of soil and above-ground pests [1, 2].They have been known since the seventeenth century [3], butit was only in the 1930s that serious care was given by using nematodes for pest control.

So far, the family Steinernematidae is comprised of two genera, *Steinernema* Travassos, 1927 [4] (Poinar, 1990) and *Neosteinernema* (Nguyen and Smart, 1994) [5]. *Neosteinernema* contains only one species *Neosteinernema longicurvicauda* that isolated from the termite *Reticulitermes flavipes* (Koller). The family Heterorhabditidae contains only one genus, *Heterorhabditis* Poinar, 1976 [6].

EPNs are mutually associated with bacteria of the family Enterobacteriaceae; the bacterium carried by Steinernematidae is usually a species of the genus *Xenorhabdus*, and that carried by Heterorhabditidae is a species of *Photorhabdus*. The third juvenile stage of EPNs is referred to as the "infective juvenile" (IJ) or the "dauer" stage. IJs of both genera release their bacterial symbionts in the insect host body and develop into fourth-stage juveniles and adults. The insects die mainly due to a septicemia. Sometimes a bacterial toxaemia precedes the resulting septicemia [7].

Infective juvenile is the only free-living stage and can survive in soil for several months until susceptible insects are encountered. IJs locate and infect suitable insect hosts by entering the insect host through the mouth, anus, spiracles or thin parts of the host cuticle. After infection, the symbiotic bacteria are released into the insect haemocoel, causing septicaemia and death of the insect [1, 8]. When an insect host is infected in the soil by an EPN, development and reproduction within the cadaver can take 1–3 weeks [9].

Surveys for EPNs have been conducted in temperate, subtropical and tropical regions and found that EPNs have a worldwide distribution; the only continent where they have not been found is Antarctica [10]. Soil texture, temperature and host availability are thought to be important factors in determining their distribution [11–13].

Nearly 70 valid species of *Steinernema* [14–16] and 25 species of *Heterorhabditis* [17, 18] have been described worldwide and still surveys for EPNs have been conducted in many parts of the world.

## **1.2. Biology and life cycle of entomopathogenic nematodes**

Through all nematodes studied to control insects, the families Steinernematidae and Hetero‐ rhabditidae have made a sensation and information about them is increasing exponentially. Steinernematids and Heterorhabditids from these families have similar life cycles, and the only difference between the life cycles of *Heterorhabditis* and *Steinernema* is occurred in the first generation. *Steinernema* species are amphimictic; this means that for successful reproduction they require the presence of males and females, whereas *Heterorhabditis* species are hermaph‐ roditic and able to reproduce in the absence of conspecifics.

**1. Entomopathogenic nematodes**

1976 [6].

septicemia [7].

the world.

**1.1. General information of entomopathogenic nematodes**

56 Integrated Pest Management (IPM): Environmentally Sound Pest Management

that serious care was given by using nematodes for pest control.

reproduction within the cadaver can take 1–3 weeks [9].

important factors in determining their distribution [11–13].

**1.2. Biology and life cycle of entomopathogenic nematodes**

Entomopathogenic nematodes (EPNs) are soil-inhabiting, lethal insect parasites that belong to the Phylum Nematoda from the families Steinernematidae and Heterorhabditidae, and they have proven to be the most effective as biological control organisms of soil and above-ground pests [1, 2].They have been known since the seventeenth century [3], butit was only in the 1930s

So far, the family Steinernematidae is comprised of two genera, *Steinernema* Travassos, 1927 [4] (Poinar, 1990) and *Neosteinernema* (Nguyen and Smart, 1994) [5]. *Neosteinernema* contains only one species *Neosteinernema longicurvicauda* that isolated from the termite *Reticulitermes flavipes* (Koller). The family Heterorhabditidae contains only one genus, *Heterorhabditis* Poinar,

EPNs are mutually associated with bacteria of the family Enterobacteriaceae; the bacterium carried by Steinernematidae is usually a species of the genus *Xenorhabdus*, and that carried by Heterorhabditidae is a species of *Photorhabdus*. The third juvenile stage of EPNs is referred to as the "infective juvenile" (IJ) or the "dauer" stage. IJs of both genera release their bacterial symbionts in the insect host body and develop into fourth-stage juveniles and adults. The insects die mainly due to a septicemia. Sometimes a bacterial toxaemia precedes the resulting

Infective juvenile is the only free-living stage and can survive in soil for several months until susceptible insects are encountered. IJs locate and infect suitable insect hosts by entering the insect host through the mouth, anus, spiracles or thin parts of the host cuticle. After infection, the symbiotic bacteria are released into the insect haemocoel, causing septicaemia and death of the insect [1, 8]. When an insect host is infected in the soil by an EPN, development and

Surveys for EPNs have been conducted in temperate, subtropical and tropical regions and found that EPNs have a worldwide distribution; the only continent where they have not been found is Antarctica [10]. Soil texture, temperature and host availability are thought to be

Nearly 70 valid species of *Steinernema* [14–16] and 25 species of *Heterorhabditis* [17, 18] have been described worldwide and still surveys for EPNs have been conducted in many parts of

Through all nematodes studied to control insects, the families Steinernematidae and Hetero‐ rhabditidae have made a sensation and information about them is increasing exponentially. Steinernematids and Heterorhabditids from these families have similar life cycles, and the only difference between the life cycles of *Heterorhabditis* and *Steinernema* is occurred in the first generation. *Steinernema* species are amphimictic; this means that for successful reproduction Both nematode genera reproduction is amphimictic in the second generation [4]. However, a hermaphroditic Steinernematid species was isolated from Indonesia [19]. Only the free-living, IJ stage is able to target insect host and the only form found outside of the host. EPNs occur naturally in soil and locate their host in response to carbon dioxide, vibration and other chemical cues, and they react to chemical stimuli or sense the physical structure of insect's integument [1].

IJs penetrate the host insect via the spiracles, mouth, anus, or in some species through intersegmental membranes of the cuticle, and then enter into the haemocoel [20]. IJs release cells of their symbiotic bacteria from their intestines into the haemocoel. The bacteria multiply rapidly in the insect hemolymph, provide nematode with nutrition and prevent secondary invaders from contaminating the host cadaver, and the infected host usually dies within 24– 48 hours by bacterial toxins.

Nematodes reproduce until the food supply becomes limiting at which time they turn into IJs. The progeny nematodes go through four juvenile stages to the adult. Based on the available resources, one or more generations may occur within the host cadaver, and a great number of IJs are released into environment to infect other host insects and continue their life [1].

The insect cadaver becomes red if the insects are killed by Heterorhabditids and brown or tan if killed by Steinernematids (**Figure 1**). The colour of the insect host body is indicative of the pigments produced by the monoculture of mutualistic bacteria growing in the host insects [1].

**Figure 1.** Different colours of the dead *Curculio nucum* larvae on white traps after EPNs infection.

The foraging strategies of EPNs change between species, and they use two main foraging strategies: ambushers or cruisers [21]. *Steinernema carpocapsae* is an example of ambushers, which have an energy-conserving approach and lie in wait to attack mobile insects (nictitating) in the upper layer of the soil. *Steinernema glaseri* and *Heterorhabditis bacteriophora* are examples of cruisers are highly active and generally subterranean, moving significant distances using volatile cues and other methods to find their host underground. But they are also successful to attack white grubs (Scarab beetles), which are less mobile. Other species, such as *Steinernema feltiae* and *Steinernema riobrave*, use an intermediate foraging strategy (combination of ambush and cruiser type) to find their host.

Selection of an EPN to control a particular pest insect is based on various factors: the nema‐ tode's host range, host finding or foraging strategy, tolerance of environmental factors and their effects on survival and efficacy. The most critical factors are moisture, temperature, pathogenicity for the targeted pest insect and foraging strategy [1, 22–24]. The activity, infectivity and survival of EPNs can be profoundly influenced by soil composition, through its effects on moisture retention, oxygen supply and texture [25–27].

Within a favourable range of temperatures, adequate moisture and a susceptible host, those EPNs with a mobile foraging strategy (cruisers and intermediate foraging strategies) could be considered for use in subterranean and certain above-ground habitats (foliar, epigeal and cryptic habitats). Those EPNs with a sit and wait foraging strategy (ambushers) will be most effective in cryptic and soil surface habitats [28].

## **1.3. Advantages of entomopathogenic nematodes**

These nematodes have many advantages; EPNs and their associated bacterial symbionts have been proven safe to warm-blooded vertebrates, including humans [29, 30]. Cold-blooded species have been found to be susceptible to EPNs under experimental conditions at very high dosages [31, 32]. However, under field conditions, the negative results could not be reproduced [33, 34].

Most biological agents require days or weeks to kill the host, yet nematodes can kill insects usually in 24–48 hours. They are easy and relatively inexpensive to culture, live from several weeks up to months in the infective stage, are able to infect numerous insect species, occur in soil and have been recovered from all continents except Antarctica [1, 35].

Foliar applications of nematodes have been successfully used to control the quarantine leafeating caterpillars as *Tuta absoluta*, *Spodoptera littoralis*, *Helicoverpa armigera*, *Pieris brassicae* on several crops and have the potential for controlling various other insect pests. Application of EPNs does not require masks or other safety equipment like chemicals. EPNs and their associated bacteria have no detrimental effect to mammals or plants [29, 30, 36].

## **2. Use of entomopathogenic nematodes**

Potential of EPNs as insecticidal agents has been tested against a wide range insect species by many researchers all over the world. They have been used with different success against insect pests occurred in different habitats. Much success has been obtained against soil-dwelling pests or pests in cryptic habitats such as inside galleries in plants where IJs find excellent atmosphere to survive and protect themselves from environmental factors. Commercial use of EPNs against some pest insects is given in **Table 1**.


a Nematodes listed provided at least 75% suppression of these pests in field or greenhouse experiments. b Abbreviations of nematode species; Hb: *Heterorhabditis bacteriophora*, Hd: *H. downesi*, Hi: *H. indica*, Hm: *H. marelata*, Hmeg: *H. megidis*, Hz: *H. zealandica*, Sc: *Steinernema carpocapsae*, Sf: *S. feltiae*, Sg: S. *glaseri*, Sk: *S. kushidai*, Sr: *S. riobrave*, Sscap: *S. scapterisci*, Ss: *S. scarabaei*.

c Efficacy against various pest species within this group varies among nematode species.

**Table 1.** Use of entomopathogenic nematodes as biological control agentsa [37].

to attack white grubs (Scarab beetles), which are less mobile. Other species, such as *Steinernema feltiae* and *Steinernema riobrave*, use an intermediate foraging strategy (combination of ambush

Selection of an EPN to control a particular pest insect is based on various factors: the nema‐ tode's host range, host finding or foraging strategy, tolerance of environmental factors and their effects on survival and efficacy. The most critical factors are moisture, temperature, pathogenicity for the targeted pest insect and foraging strategy [1, 22–24]. The activity, infectivity and survival of EPNs can be profoundly influenced by soil composition, through

Within a favourable range of temperatures, adequate moisture and a susceptible host, those EPNs with a mobile foraging strategy (cruisers and intermediate foraging strategies) could be considered for use in subterranean and certain above-ground habitats (foliar, epigeal and cryptic habitats). Those EPNs with a sit and wait foraging strategy (ambushers) will be most

These nematodes have many advantages; EPNs and their associated bacterial symbionts have been proven safe to warm-blooded vertebrates, including humans [29, 30]. Cold-blooded species have been found to be susceptible to EPNs under experimental conditions at very high dosages [31, 32]. However, under field conditions, the negative results could not be reproduced

Most biological agents require days or weeks to kill the host, yet nematodes can kill insects usually in 24–48 hours. They are easy and relatively inexpensive to culture, live from several weeks up to months in the infective stage, are able to infect numerous insect species, occur in

Foliar applications of nematodes have been successfully used to control the quarantine leafeating caterpillars as *Tuta absoluta*, *Spodoptera littoralis*, *Helicoverpa armigera*, *Pieris brassicae* on several crops and have the potential for controlling various other insect pests. Application of EPNs does not require masks or other safety equipment like chemicals. EPNs and their

Potential of EPNs as insecticidal agents has been tested against a wide range insect species by many researchers all over the world. They have been used with different success against insect pests occurred in different habitats. Much success has been obtained against soil-dwelling pests or pests in cryptic habitats such as inside galleries in plants where IJs find excellent atmosphere to survive and protect themselves from environmental factors. Commercial use

soil and have been recovered from all continents except Antarctica [1, 35].

associated bacteria have no detrimental effect to mammals or plants [29, 30, 36].

its effects on moisture retention, oxygen supply and texture [25–27].

58 Integrated Pest Management (IPM): Environmentally Sound Pest Management

effective in cryptic and soil surface habitats [28].

**1.3. Advantages of entomopathogenic nematodes**

**2. Use of entomopathogenic nematodes**

of EPNs against some pest insects is given in **Table 1**.

[33, 34].

and cruiser type) to find their host.

## **2.1. Efficacy of entomopathogenic nematodes against tomato leaf miner** *Tuta absoluta*

In our laboratory, we investigated the use of native EPN isolates to control various pest insects, and one of these pests was tomato leaf miner. The tomato leafminer, *T. absoluta* (Meyrick) (Lepidoptera: Gelechiidae), is a very devastating pest and was first recorded in 2009 in the Urla District of Izmir Province in Turkey [38]. It has been a serious problem to tomato production in Çanakkale since the first detection in our country [39]. *T. absoluta* can attack all parts and stages of the tomato plant, overwinter in the egg, pupal or adult stage and can cause up to 100% losses in tomato crops [40].

Since its dispersal in the 1970s, chemical control has been the main method to control *T. absoluta*. Producers have tried to decrease its damages by using insecticides twice a week during a cultivation period, sometimes every 4–5 days/season with 8–25 sprays [41]. Although with the many applications of chemicals, effective control is difficult due to the behaviour of these mine-feeding larvae.

Moreover, the use of pesticides in plant production has numerous disadvantages as pesticide residues on human health and on the environment so biological control may be considered as an alternative method to chemical control [42]. In this respect, EPNs can be an alternative to chemicals. The aims of the work were to determine the efficacy of native EPN isolates against *T. absoluta* in tomato field and to reduce the use of pesticides.

## **2.2. Materials and methods**

## *2.2.1. Entomopathogenic nematodes culture*

Four native species of nematodes: *Steinernema affine* (Bovien) (isolate 46) *S. carpocapsae*(Weiser) (isolate 1133), *S. feltiae* (Filipjev) (isolate 879) and *H. bacteriophora* (Poinar) (isolate 1144), were tested against *T. absoluta* larvae. Each isolates was reared in the last instar of wax moth larvae *Galleria mellonella* L., which is the most commonly used insect host for in vivo production of EPNs because of its rich nutrient source available in body and easy to multiply in economical diet source [43, 44].

Nematode-infected *G. mellonella* larvae were placed on white traps [45] at 25°C and IJs that emerged from cadavers were harvested.

## *2.2.2. Tuta absoluta culture*

Larvae, pupae and adults of *T. absoluta* used in the trials were obtained from infested tomato fields in Çanakkale. They reared in wooden rearing cages (50 × 50 × 50 cm) on tomato plants at 25 ± 1°C, 65 ± 5% RH, with a 16:8 L:D photoperiod in climate room.

## *2.2.3. Field trials*

Field trials were carried out in the training and research area of Agriculture Faculty in Çanakkale between 2012 and 2013. In both seasons, nearly 1000 m2 area was cultivated with tomato and seedlings were controlled periodically and closed by a cage when they reached 20 cm height. Each tomato plant was grown in a single cage (50 × 50 × 50 cm). After 30 days, two males and two females were put into each cage.

EPNs were applied at dusk to utilise the higher air humidity for the nematodes with a conventional airblast sprayer at a rate of 50 IJs/cm2 . Tomato plants remained wet in cages after application for 2 hours and that provides EPNs enough time with perfect condition to find and infect the target pest. The experiment was carried out with two replicates per nematode species and exposure day and repeated twice.

After releasing the adults of *T. absoluta*, EPNs were sprayed on tomato plants at the 7th, 14th and 21st days. Tomato plants were cut from the soil line at the 3rd, 5th 7th, 9th, 11th, 13th and 15th days after EPN applications and analysed to determine the mortality of *T. absoluta*. Dead *T. absoluta* larvae were immediately dissected and checked for nematode infection (**Figure 2**). EPNs most likely entered feeding canals in the leaves of tomatoes. Many larvae of *T. absoluta* died inside these galleries, which indicate that IJs were able to find and infect them.

**Figure 2.** Emerged EPNs from infected *Tuta absoluta* larvae.

## **2.3. Results**

**2.1. Efficacy of entomopathogenic nematodes against tomato leaf miner** *Tuta absoluta*

100% losses in tomato crops [40].

these mine-feeding larvae.

**2.2. Materials and methods**

diet source [43, 44].

*2.2.3. Field trials*

*2.2.2. Tuta absoluta culture*

*2.2.1. Entomopathogenic nematodes culture*

emerged from cadavers were harvested.

In our laboratory, we investigated the use of native EPN isolates to control various pest insects, and one of these pests was tomato leaf miner. The tomato leafminer, *T. absoluta* (Meyrick) (Lepidoptera: Gelechiidae), is a very devastating pest and was first recorded in 2009 in the Urla District of Izmir Province in Turkey [38]. It has been a serious problem to tomato production in Çanakkale since the first detection in our country [39]. *T. absoluta* can attack all parts and stages of the tomato plant, overwinter in the egg, pupal or adult stage and can cause up to

Since its dispersal in the 1970s, chemical control has been the main method to control *T. absoluta*. Producers have tried to decrease its damages by using insecticides twice a week during a cultivation period, sometimes every 4–5 days/season with 8–25 sprays [41]. Although with the many applications of chemicals, effective control is difficult due to the behaviour of

Moreover, the use of pesticides in plant production has numerous disadvantages as pesticide residues on human health and on the environment so biological control may be considered as an alternative method to chemical control [42]. In this respect, EPNs can be an alternative to chemicals. The aims of the work were to determine the efficacy of native EPN isolates against

Four native species of nematodes: *Steinernema affine* (Bovien) (isolate 46) *S. carpocapsae*(Weiser) (isolate 1133), *S. feltiae* (Filipjev) (isolate 879) and *H. bacteriophora* (Poinar) (isolate 1144), were tested against *T. absoluta* larvae. Each isolates was reared in the last instar of wax moth larvae *Galleria mellonella* L., which is the most commonly used insect host for in vivo production of EPNs because of its rich nutrient source available in body and easy to multiply in economical

Nematode-infected *G. mellonella* larvae were placed on white traps [45] at 25°C and IJs that

Larvae, pupae and adults of *T. absoluta* used in the trials were obtained from infested tomato fields in Çanakkale. They reared in wooden rearing cages (50 × 50 × 50 cm) on tomato plants

Field trials were carried out in the training and research area of Agriculture Faculty in Çanakkale between 2012 and 2013. In both seasons, nearly 1000 m2 area was cultivated with tomato and seedlings were controlled periodically and closed by a cage when they reached 20

at 25 ± 1°C, 65 ± 5% RH, with a 16:8 L:D photoperiod in climate room.

*T. absoluta* in tomato field and to reduce the use of pesticides.

60 Integrated Pest Management (IPM): Environmentally Sound Pest Management

The efficacy of EPNs in field in 2012 changed between 0 and 90.7 ± 1.5%. The least efficient species was *S. affine* and the most efficient species was *S. feltiae* with the mortality of 39.3 ± 1.5% and 90.7 ± 1.5%, respectively. *S. affine* caused 0–39.3 ± 1.5% mortality and found as the least efficient species. *S. carpocapsae* caused 0–43.7 ± 1.5% mortality, while *S. feltiae* caused 0–90.7 ± 1.5% mortality. *H. bacteriophora* caused 0–81 ± 3.5% mortality and was the second efficient species after *S. feltiae* against *T. absoluta* in tomato field in 2012.

The efficacy of EPNs in field in 2013 changed between 0 and 94.3 ± 2.0%. The least efficient species was *S. affine* and the most efficient species was *S. feltiae* with the mortality of 43.7 ± 2.3% and 94.3 ± 2.0%, respectively. *S. affine* caused 0–43.7 ± 2.3% mortality and was the least efficient species. *S. carpocapsae* caused 0–49.3 ± 2.4% mortality, while *S. feltiae* caused 0–94.3 ± 2.0% mortality. *H. bacteriophora* caused 0–83.0 ± 2.1% mortality and was the second efficient species after *S. feltiae* against *T. absoluta* in field in 2013.

## **2.4. Discussion**

The tomato leafminer, *T. absoluta*, is one of the most important lepidopteran moth associated with tomato plants and because of its biology and behaviour, it is difficult to control. Effective chemical control of *T. absoluta* is not possible because it feeds internally within the plant tissues. Resistance to insecticides is another significant problem in chemical control of this pest because of its high reproduction capacity, short generation cycle and intensive use of insecticides [46– 50].

Pesticides are so widely used and that destroys populations of natural enemies and conse‐ quently decreases biological control of *T. absoluta*. Because of these negative effects of insecti‐ cides, other approaches need to be considered seriously for this devastating pest.

Some insects can be controlled by a combination of methods, which are not totally effective when used alone. *T. absoluta* is one of these insects, which requires more than one method to be controlled successfully. For this reason, integrated pest management (IPM) programmes are continuously being progressed in different countries to control infestations of tomato leaf miner. EPNs have been considered as potential biocontrol agents for leafminers in recent years [50]. They can be applied, in combination with other biological and chemical pesticides, fertilisers and soil amendments and in the form of adjuvants or antidesiccants [51, 52].

Various studies about EPNs have been conducted all over the world, but only few research has been carried out on the efficacy of EPNs against *T. absoluta*. This is the first study conducted both in çanakkale and in Turkey based on the efficacy of native EPN isolates to *T. absoluta* in a tomato field.

The efficacy of the three EPNs after foliar application to potted tomato was tested under greenhouse conditions. High larval mortality (78.6–100%) and low pupal mortality (<10%) in laboratory were reported. In the leaf bioassay, high larval parasitisation (77.1–91.7%) was recorded. In the pot experiments, it was found that nematode application decreased insect infestation of tomato by 87–95%. These results showed the suitability of EPNs to control *T. absoluta* [53].

The efficacy of soil treatments of three native EPNs (*S. carpocapsae, S. feltiae* and *H. bacterio‐ phora*) against *T. absoluta* larvae, pupae and adults was determined under laboratory conditions in another study [54]. The effect of three commonly used insecticides against *T. absoluta* was also evaluated in the survival, infectivity and reproduction of these EPNs. When the larvae dropped into the soil to become pupa, soil application of nematodes resulted in a high larval mortality: 100, 52.3 and 96.7% efficacy for *S. carpocapsae, S. feltiae* and *H. bacteriophora*, respec‐ tively. No mortality of pupae was recorded, and mortality of adults emerging from soil was 79.1% for *S. carpocapsae* and 0.5% for *S. feltiae*. An insignificant effect of the insecticides tested was reported on nematode survival, infectivity and reproduction. No sublethal effects were observed. These findings proved that larvae of *T. absoluta*, falling from leaves following insecticide application, could be favourable hosts for nematodes, thereby increasing their concentration and persistence in the soil.

The efficacy of *S. feltiae, S. carpocapsae* and *H. bacteriophora* was evaluated against larvae of *T. absoluta* inside leaf mines in tomato leaf discs by means of an automated spray boom. They reported that all EPNs used in the study were effective to all four larval instars of *T. absoluta* but caused higher mortality in the later instars (fourth instar: 77.1–97.4%) than in the first instars (36.8–60.0%). *S. feltiae* and *S. carpocapsae* showed better results than *H. bacteriophora*. *S. carpocapsae* and *H. bacteriophora* performed better at 25°C (55.3 and 97.4% mortality, respec‐ tively) than at 18°C (12.5 and 34.2% mortality, respectively), while *S. feltiae* caused 100% mortality at both temperatures. Their results demonstrated that under laboratory conditions, *S. feltiae* and *S. carpocapsae* showed effective performance against the larvae of *T. absoluta* inside tomato leaf mines [55].

Our results agree with other reports showing that larvae of *T. absoluta* were highly susceptible to the EPNs tested and these EPNs can be used as efficient biological control agents against *T. absoluta*. All EPNs used in the study showed efficacy at different rates against *T. absoluta*. They were able to find and infect *T. absoluta* larvae both inside and outside of the tomato leaf. According to these findings, it could be suggested that EPNs have a great potential to use as biocontrol agents for the management of *T. absoluta*.

It should be noted that to understand their life cycles and functions, match the correct species of EPNs with the correct species of insect pests, apply them under optimum environmental conditions, such as soil temperature, soil moisture, angle of sun rays, and apply only with compatible pesticides are the keys to success with EPNs.

## **3. Conclusions**

**2.4. Discussion**

a tomato field.

*absoluta* [53].

concentration and persistence in the soil.

50].

The tomato leafminer, *T. absoluta*, is one of the most important lepidopteran moth associated with tomato plants and because of its biology and behaviour, it is difficult to control. Effective chemical control of *T. absoluta* is not possible because it feeds internally within the plant tissues. Resistance to insecticides is another significant problem in chemical control of this pest because of its high reproduction capacity, short generation cycle and intensive use of insecticides [46–

Pesticides are so widely used and that destroys populations of natural enemies and conse‐ quently decreases biological control of *T. absoluta*. Because of these negative effects of insecti‐

Some insects can be controlled by a combination of methods, which are not totally effective when used alone. *T. absoluta* is one of these insects, which requires more than one method to be controlled successfully. For this reason, integrated pest management (IPM) programmes are continuously being progressed in different countries to control infestations of tomato leaf miner. EPNs have been considered as potential biocontrol agents for leafminers in recent years [50]. They can be applied, in combination with other biological and chemical pesticides, fertilisers and soil amendments and in the form of adjuvants or antidesiccants [51, 52].

Various studies about EPNs have been conducted all over the world, but only few research has been carried out on the efficacy of EPNs against *T. absoluta*. This is the first study conducted both in çanakkale and in Turkey based on the efficacy of native EPN isolates to *T. absoluta* in

The efficacy of the three EPNs after foliar application to potted tomato was tested under greenhouse conditions. High larval mortality (78.6–100%) and low pupal mortality (<10%) in laboratory were reported. In the leaf bioassay, high larval parasitisation (77.1–91.7%) was recorded. In the pot experiments, it was found that nematode application decreased insect infestation of tomato by 87–95%. These results showed the suitability of EPNs to control *T.*

The efficacy of soil treatments of three native EPNs (*S. carpocapsae, S. feltiae* and *H. bacterio‐ phora*) against *T. absoluta* larvae, pupae and adults was determined under laboratory conditions in another study [54]. The effect of three commonly used insecticides against *T. absoluta* was also evaluated in the survival, infectivity and reproduction of these EPNs. When the larvae dropped into the soil to become pupa, soil application of nematodes resulted in a high larval mortality: 100, 52.3 and 96.7% efficacy for *S. carpocapsae, S. feltiae* and *H. bacteriophora*, respec‐ tively. No mortality of pupae was recorded, and mortality of adults emerging from soil was 79.1% for *S. carpocapsae* and 0.5% for *S. feltiae*. An insignificant effect of the insecticides tested was reported on nematode survival, infectivity and reproduction. No sublethal effects were observed. These findings proved that larvae of *T. absoluta*, falling from leaves following insecticide application, could be favourable hosts for nematodes, thereby increasing their

The efficacy of *S. feltiae, S. carpocapsae* and *H. bacteriophora* was evaluated against larvae of *T. absoluta* inside leaf mines in tomato leaf discs by means of an automated spray boom. They

cides, other approaches need to be considered seriously for this devastating pest.

62 Integrated Pest Management (IPM): Environmentally Sound Pest Management

Biological control is an action that involves the use of natural enemies of insect pests to increase negative effects of insect pest as destroying important crops and plantation, plant growth destruction or development infections caused by pests [56].


**Table 2.** Advantages and disadvantages of entomopathogenic nematodes [58].

EPNs are a group of soil-dwelling organisms that attack soilborne insect pests that live in, on or near the soil surface and can be used effectively to control economically important insect pests. Different nematode species and strains exhibit differences in survival, search behaviour and infectivity, which make them more or less suitable for particular insect pest control programmes [57]. As the other biological control agents, also EPNs have advantages and disadvantages (**Table 2**).

There is a great interest in finding wild populations to obtain new species and strains for possible use in biological control. The use of EPNs is one potential non-chemical approach to control insect pests. EPNs are widely spread geographically and have many hosts. They are currently used as biological control agents in many studies to control several important insect pests worldwide [59–61].

It is highlighted that there is a need for more in-depth basic information on EPNs biology, including ecology, behaviour and genetics, to help understand the underlying reasons for their successes and failures as biological control organisms. Most appropriate nematode species/ strain, abiotic factors such as soil type, soil temperature and moisture are important for getting success [1].

Proper match of the nematode to the host entails virulence, host finding and ecological factors are essential before application to the field. Matching the appropriate nematode host-seeking strategy with the pest is essential, because poor host suitability has been the most common mistake occurred in application of EPNs [62]. Also application strategies, such as field dosage, volume, irrigation and appropriate application methods, are very important. Furthermore, plant morphology and phenology must be considered in predicting whether nematodes are viable control candidates [63].

## **Author details**

Ugur Gozel\* and Cigdem Gozel

\*Address all correspondence to: ugozel@comu.edu.tr

Canakkale Onsekiz Mart University, Agriculture Faculty Plant Protection Department, Çanakkale, Turkey

## **References**


of the efficacy of foliar application of two strains of *Steinernema feltiae* (Filipjev) and spraying with thiametoxam. Journal of Plant Disease Protection, 117: 129–135.

[3] Nickle W.R. 1984. History, development, and importance of insect nematology. In: Nickle W.R. (Ed.) Plant and Insect Nematodes. New York: Marcel Dekker, pp. 627–653.

EPNs are a group of soil-dwelling organisms that attack soilborne insect pests that live in, on or near the soil surface and can be used effectively to control economically important insect pests. Different nematode species and strains exhibit differences in survival, search behaviour and infectivity, which make them more or less suitable for particular insect pest control programmes [57]. As the other biological control agents, also EPNs have advantages and

64 Integrated Pest Management (IPM): Environmentally Sound Pest Management

There is a great interest in finding wild populations to obtain new species and strains for possible use in biological control. The use of EPNs is one potential non-chemical approach to control insect pests. EPNs are widely spread geographically and have many hosts. They are currently used as biological control agents in many studies to control several important insect

It is highlighted that there is a need for more in-depth basic information on EPNs biology, including ecology, behaviour and genetics, to help understand the underlying reasons for their successes and failures as biological control organisms. Most appropriate nematode species/ strain, abiotic factors such as soil type, soil temperature and moisture are important for getting

Proper match of the nematode to the host entails virulence, host finding and ecological factors are essential before application to the field. Matching the appropriate nematode host-seeking strategy with the pest is essential, because poor host suitability has been the most common mistake occurred in application of EPNs [62]. Also application strategies, such as field dosage, volume, irrigation and appropriate application methods, are very important. Furthermore, plant morphology and phenology must be considered in predicting whether nematodes are

Canakkale Onsekiz Mart University, Agriculture Faculty Plant Protection Department,

[1] Kaya H.K., Gaugler R. 1993. Entomopathogenic nematodes. Annual Review of

[2] Laznik Ž., Tóth T., Lakatos T., Vidrih M., Trdan S. 2010. Control of the Colorado potato beetle (*Leptinotarsa decemlineata* [Say]) on potato under field conditions: a comparison

disadvantages (**Table 2**).

pests worldwide [59–61].

viable control candidates [63].

and Cigdem Gozel

Entomology, 38: 181–206.

\*Address all correspondence to: ugozel@comu.edu.tr

**Author details**

Çanakkale, Turkey

**References**

Ugur Gozel\*

success [1].


[28] Lacey L.A., Georgis R. 2012. Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology, 44(2): 218–225.

[16] Orozco R.A., Hill T., Stock S.P. 2013. Characterization and phylogenetic relationships of *Photorhabdus luminescens* subsp. *sonorensis* (gamma-Proteobacteria: Enterobacteria‐ ceae), the bacterial symbiont of the entomopathogenic nematode *Heterorhabditis*

[17] Plichta K.L., Joyce S.A., Clarke D., Waterfield N., Stock S.P. 2009. *Heterorhabditis gerrardi* n. sp (Nematoda: Heterorhabditidae): the hidden host of *Photorhabdus asym‐ biotica* (Enterobacteriaceae: Gamma-Proteobacteria). Journal of Helminthology, 83:

[18] Edgington S., Buddie A.G., Moore D., France A., Merino L., Hunt D.J. 2011. *Heterorhab‐ ditis atacamensis* n. sp (Nematoda: Heterorhabditidae), a new entomopathogenic nematode from the Atacama Desert, Chile. Journal of Helminthology, 85: 381–394. [19] Griffin C.T., O'callaghan K.M., DIX I. 2001. A self-fertile species of *Steinernema* from Indonesia: further evidence of convergent evolution amongst entomopathogenic

[20] Bedding R.A., Molyneux A.S. 1982. Penetration of insect cuticle by infective juveniles of *Heterorhabditis* spp. (Heterorhabditidae: Nematoda). Nematologica, 21: 109–110. [21] Grewal P.S., Lewis E.E., Gaugler R., Campbell J.F. 1994. Host finding behavior as a predictor of foraging strategy in entomopathogenic nematodes. Parasitology, 108: 207–

[22] Kung S.P., Gaugler R., Kaya H.K. 1991. Effects of soil temperature, moisture, and relative humidity on entomopathogenic nematode persistence. Journal of Invertebrate

[23] Campbell J.F., Lewis E.E., Stock S.P., Nadler S., Kaya H.K. 2003. Evolution of host search strategies in entomopathogenic nematodes. Journal of Nematology, 35: 142–145. [24] Grewal P.S., Ehlers R-U., Shapiro-Ilan D.I. 2005. Nematodes as Biological Control

[25] Kaya H.K. 1990. Soil ecology. In: Gaugler R., Kaya H.K. (Eds.) Entomopathogenic Nematodes in Biological Control. Boca Raton (FL): CRC Press, pp. 93–115.

[26] Ellsbury M.M., Jackson J.J., Woodson W.D., Beck D.L., Stange K.A. 1996. Efficacy, application distribution, and concentration by stemflow of *Steinernema carpocapsae* (Rhabditida: Steinernematidae) suspensions applied with a lateral-move irrigation system for corn rootworm (Coleoptera: Chrysomelidae) control in maize. Journal of

[27] Koppenhofer A.M., Fuzy E.M. 2006. Nematodes for white grub control: Effects of soil type and soil moisture on infectivity and persistence. USGA Turfgrass Environmental

*sonorensis* (Nematoda: Heterorhabditidae). Current Microbiology, 66: 30–39.

309–320.

215.

Pathology, 57: 242–249.

nematodes? Parasitology 122: 181–186.

66 Integrated Pest Management (IPM): Environmentally Sound Pest Management

Agents. Wallingford: CABI Publishing.

Economic Entomology, 85: 2425–2432.

Research Online, 5: 1–10.


[54] Garcia del Pino F., Alabern X., Morton A. 2013. Efficacy of soil treatments of entomo‐ pathogenic nematodes against the larvae, pupae and adults of *Tuta absoluta* and their interaction with the insecticides used against this insect. BioControl, 58(6): 723–731.

[41] Temerak S.A. 2011. The status of *Tuta absoluta* in Egypt, 16–18. EPPO/IOPC/FAO/NEPP Joint, International Symposium on Management of *Tuta absoluta* (tomato borer),

[42] Gill H.K., Garg H. 2014. Pesticide: environmental impacts and management strategies. In: Solenski S., Larramenday M.L. (Eds.) Pesticides-Toxic Effects. Rijeka, Croatia:

[43] Bedding R.A., Akhurst R.J., 1975. A simple technique for the detection of insect parasitic

[44] Kaya H.K., Stock S.P. 1997. Techniques in insect nematology, In: Lacey L.A. (Ed.) Manual of Techniques in Insect Pathology. Biological Techniques Series, San Diego,

[45] White G.F. 1927. A method for obtaining infective nematode larvae from cultures.

[46] Salazar E.R., Araya J.E. 1997. Detection of resistance to insecticides in the tomato moth.

[47] Salazar E.R., Araya J.E. 2001. Tomato moth, Tuta absoluta (Meyrick) response to

[48] Siqueira H.A.A., Guedes R.N.C., Picanço M.C. 2000. Insecticide resistance in popula‐ tions of *Tuta absoluta* (Lepidoptera: Gelechiidae). Agricultural and Forest Entomology,

[49] Siqueira, H.A.A., Guedes R.N.C., Fragoso D.B., Magalhaes L.C. 2001. Abamectin resistance and synergism in Brazilian populations of *Tuta absoluta* (Meyrick) (Lepidop‐

[50] Olthof Th. H.A., Broadbent A.B. 1990. Control of a chrysanthemum leafminer, *Liriomyza trifolii* with the entomophilic nematode, *Heterorhabditis heliothidis*, 379. Abstracts of Papers, Posters and Films Presented at the Second International Nematology Congress,

tera: Gelechiidae). International Journal of Pest Management, 47(4): 247–251.

11–17 August, Veldhoven the Netherlands, Nematologica, 36(1990): 327–403.

[51] Glazer I., Navon A. 1990. Activity and persistence of entomogenous nematodes used against *Heliothis armigera* (Lepidoptera: Noctuidae). Journal of Economic Entomology,

[52] Baur M.E., Kaya H.K., Gaugler R., Tabashnik B. 1997. Effects of adjuvants on entomo‐ pathogenic nematode persistence and efficacy against *Plutella xylostella*. Biocontrol,

[53] Batalla-Carrera L., Morton A., Garcia-del-pino F. 2010. Efficacy of entomopathogenic nematodes against the tomato leafminer *Tuta absoluta* in laboratory and greenhouse

Conference, Agadir, Morocco, November, 18 pp.

68 Integrated Pest Management (IPM): Environmentally Sound Pest Management

California: Academic Press, pp. 281–324. 409 pp.

insecticides in Arica, Chile. 61(4): 429–435.

Rhabditid nematodes in soil. Nematologica, 21: 109–110.

Intech, pp. 187–230.

Science, 66: 302–303.

Simiente, (1–2): 8–22.

2: 147–153.

83: 1795–1800.

Science and Technology, 7: 513–525.

conditions. Biocontrol, 55: 523–530.

