High-Density Planting

**Chapter 4**

## Dwarfing Rootstocks for High-Density Citrus Orchards

*Mateus Pereira Gonzatto, Sabrina Raquel Griebeler and Sergio Francisco Schwarz*

#### **Abstract**

There is a worldwide trend regarding high density of fruit planting. In the last four decades, the Brazilian citriculture had increased the average planting density by more than 80%. The main reasons for this increase are the fast return on invested capital, the easiest management of cultural practices, and the control of strategies epidemicsassociated (e.g., *Huanglongbing*). In that regard, the use and development of dwarf and semi-dwarf rootstocks are essential. The main dwarf rootstock known in citriculture is the Flying Dragon trifoliate orange [*Poncirus trifoliata* (L.) Raf. var. *monstrosa* (T. Itô) Swing.] which greatly reduces the canopies volume allowing the design of dense and ultra-dense orchards. Currently, several citrus breeding programs are producing new cultivars of dwarf and semi-dwarf rootstocks. In this chapter, citrus rootstocks with dwarfing potential were approached including physiological aspects, horticultural performance, and behavior to phytosanitary problems. In addition to Flying Dragon, there are other dwarfing rootstocks which are hybrids of trifoliate oranges, like citrandarins, citrangedarins, citrumelandarins, and citrimonianandarins. Dwarfing rootstocks are one of the leading alternatives for citrus orchards in high-density planting systems.

**Keywords:** *Poncirus trifoliata* Raf., *Citrus* spp., Flying Dragon trifoliate orange, citrandarin, citrangedarin, citrumelandarin

#### **1. Introduction**

The high-density planting allows an increase in fruit yield per area in the initial years of production and a reduction in the payback period despite the higher cost of implementing the orchards. Therefore, it has been a trend to enhance the production system [1, 2]. Moreover, high-density planting improves orchard harvesting since there is no need for ladders [3, 4], and also reduces loss by diseases such as *Huanglongbing* (HLB) [5]. However, this technology requires effective control of the canopy growth of citrus plants. A suitable planting density with restricted space available for the growth of these plants and avoidance of excessive intercrossing of scions must be employed [3].

In Southeast Brazil, citrus orchards have shown an increase in planting densities, from an average of 337 trees per hectare in the 1980s to over 600 trees per hectare

since 2013. Since 2014, a stabilization in planting densities of around 650 trees per hectare is noted [6].

Two main classifications of citrus plants size are proposed. To Castle and Phillips [7], a classification was recommended according to the height or volume of scions into four categories regarding a standard plant: dwarf, semi-dwarf, semi-standard, and standard. Dwarf and semi-dwarf occur when the plant is 40% and 40–60% of the standard size, respectively. Semi-standard arises to plant with a size of 60–80% of the standard. Standard, on the other hand, is used for plants having 80–100% of the standard size. In this classification, the standard used was plants grafted onto a rough lemon (*Citrus jambhiri* Lush.). Another classification was proposed by Bitters et al. [8] in which a tree with a height of 6.0 m or more was used as the standard. Sub-standard plants, semi-dwarf plants, and dwarf plants were the ones which have a reduction of 25%, 50%, and 75%, respectively regarding the standard.

Many factors affect citrus plants' size such as rootstock, variety, soil and climate conditions, cultural treatments, and phytosanitary conditions [3]. The effective control of the citrus growth plants can be achieved by means of several strategies: (a) use of scions with restricted growth potential; (b) pruning; (c) biological agents, usually viroids and viruses; (d) restriction of the root system growth; (e) use of dwarfing, semi-dwarfing and intergrafted rootstocks; (f) sloping planting of seedlings, and (g) use of plant growth regulators [3, 9]. Among them, probably the most effective is the use of dwarfing rootstocks [7] because few scion varieties have significantly reduced growth by themselves. In mandarin trees, some cultivars of the Satsuma group (*Citrus unshiu* Marcovitch) such as 'Clausellina' and 'Hashimoto' are highlighted due to their small growth [10].

This chapter presents the most important rootstocks for citrus high-density orchards in addition to the most recent alternatives. The main characteristics and horticultural performance of rootstocks were approached.

#### **2. Dwarfing rootstocks and high-density citrus orchards**

A dwarfing rootstock is the one that in combination with any canopy genotype, generates a mature tree with a height of no more than 2.5 m, independent of environmental and/or viral influences [11]. Currently, several materials from directed hybridization are classified as dwarfing. Nevertheless, few of them seem to provide an increment in the trees yield efficiency. Diversely, Flying Dragon [*P. trifoliata* (L.) Raf. var. *monstrosa* (T. Itô) Swing.] had a high yield efficiency [12–16] probably due to distinct dwarfing mechanisms [17].

In Brazil, densified citrus orchards have densities between 600 and 1250 plants ha−1, with distances of 4–6 m between rows and 2–3 m between plants [2, 5]. Differently, ultra-dense orchards are those where planting densities vary from 1500 to 2000 plants ha−1. Theoretically, these ultra-dense-orchards reach up to tens of thousands of trees per hectare, within the concept of "meadow orchard" [9]. In recent work in India with Nagpur mandarin onto Rangpur lime, a high-density was considered as the one bearing between 555 and 625 plants ha−1 and an ultra-high density planting the one varying from 1250 and 2500 plants ha−1 [18]. In Japan, long-term experiments were accomplished in 'Wase' satsuma mandarin (*C. unshiu* Marc. var. *praecox* Tan.) to evaluate orchards with densities of up to 10,000 plants ha−1 [19, 20].

*Dwarfing Rootstocks for High-Density Citrus Orchards DOI: http://dx.doi.org/10.5772/intechopen.102851*

Densification is a common practice in mandarin orchards in Southern Brazil. There is a spacing recommendation for *P. trifoliata* varying from 6.5 m × 3.0 m to 5.0 m × 2.0 m (512–1000 plants ha−1), depending on soil fertility. For mandarin plants grafted onto Flying Dragon, a spacing of 4.5 m × 1.5 m and 4.0 m × 1.0 m (1480 and 2500 plants ha−1) is recommended in high and low fertility soils, respectively [21]. In Southeast Brazil, row spacing of 4–5 m and plant spacing of 1.5–2.5 m is recommended for the Flying Dragon rootstock [22]. In Florida, despite its limited commercial use, a spacing of 5–7 ft (1.52–2.13 m) is recommended between plants grafted onto Flying Dragon. Instead, for common trifoliate orange, there is a spacing recommendation of 6–8 ft (1.83–2.44 m) [23].

In Iran, three planting spacings/densities were evaluated on 'Unshiu', 'Clementina', 'Page' and 'Ponkan' mandarin grafted onto Flying Dragon (4 m × 4 m, 625 plants ha−1; 4 m × 3 m, 833 plants ha−1; and 4 m × 2 m, 1250 plants ha−1). There was no effect of planting density on yield per plant. Nevertheless, yield per area increased significantly at the highest planting density. 'Ponkan' mandarins showed a better yield performance, while 'Page' mandarins had the worst yield performance and the lowest growth in the first five productive years of the orchard [22]. In later studies, the mandarin tree 'Span Americana', an early variety from the same group as 'Ponkan', performed well over Flying Dragon. Then, it has shown potential for densely planted orchards [23]. Furthermore, reports indicate a better performance of densified systems in citrus plants having columnar canopies.

Biological agents are also explored in citrus high-density planting toward the re-engineering of citrus seedlings. As recently shown, the use of Citrus dwarfing viroid (CDVd) into trifoliate orange rootstock 'Rich 16-6' (*P. trifoliata* (L.) Raf.) reduced canopy volume by up to 50% [24]. Beyond size reduction, the canopy of CDVd-infected trees had a long-lasting phenotype regarding Flying Dragon rootstock. Further, a report aimed to discover the mechanism of CDVd dwarfism. The understanding of this mechanism would allow the development of commercial products absent infectious agents [25].

#### **2.1 Flying Dragon trifoliate orange**

The most important and well-established citrus dwarfing rootstock is the Flying Dragon trifoliate orange, also known as Hiryu or Japanese Hiryo [26–28]. The Flying Dragon [*P. trifoliata* var. *monstrosa* (T. Itô) Swing.] originated as a mutant of a nondwarfing trifoliate orange [*P. trifoliata* (L.) Raf.]. Besides, it has not undergone sexual recombination suggesting a great degree of kinship between *P. trifoliata* and Flying Dragon genotypes [29, 30].

A large number of studies over Flying Dragon rootstock in several environments and with many citrus scions are reported [4, 12–16, 22, 23, 26, 28, 31–37]. Due to the several advantages, it is an interesting alternative for densification of citrus orchards [28], mainly for 'Tahiti' lime [35] and mandarins [22].

The trees grafted onto Flying Dragon rootstock are small or dwarf sized, with a maximum height between 2.5 and 3.0 m [26, 28]. Flying Dragon features curved thorns and tortuous trunk, unlike common trifoliate orange (**Figure 1**). These two characteristics are morphological markers of the dwarfing effect, due to gene linkage or pleiotropy [29]. The tortuosity inheritance seems to be linked to three nuclear genes (Cr1, Cr2 and Cr3), in which the Flying Dragon genotype is entirely heterozygous (Cr1cr1Cr2cr2Cr3cr3), with seedlings of tortuous phenotypes showing

#### **Figure 1.**

*Fruit and branches of trifoliate oranges. (A) common trifoliate orange (*P. trifoliata*); (B) Flying Dragon trifoliate orange (*P. trifoliata *var.* monstrosa*).*

low canopy growth, while the phenotypes with straight structures showed a great variability [27].

As there is a great genetic proximity between Flying Dragon and the trifoliate orange, they have many similar characteristics [10]; excellent fruit quality of the scion variety [38], late maturation, tolerance to cachexia, and sudden death. They are also resistant to the nematode *Tylenchulus semipenetrans* as well as to *Citrus tristeza* virus and to citrus gummosis (*Phytophthora* spp.). Beyond, both rootstocks are susceptible to citrus decline, exocortis, and burrowing nematode (*Radopholus similis*) as well as a high tolerance to cold and waterlogging and low tolerance to drought [39–41]. Further, HLB incidence on Flying Dragon is lower than on Rangpur lime and the other three semi-standard rootstocks. The reduction in canopy volume seems to influence host–vector relationships [42].

Furthermore, incompatibilities between *P. trifoliata* and several canopies such as: 'Pêra', 'Rio Seleta' and 'Crescent' orange; 'Murcott' tangor; 'Sicilian' and 'Eureka' lemon are described [40, 41, 43]. There are also incompatibilities in Flying Dragon under 'Lima-da-Persia' [*Citrus limettioides* (Christm.) Swingle] and kumquat (*Fortunella* sp.) in South Brazil [44]. In Spain, there is a record of incompatibility when the scion is 'Eureka' [10].

In Brazil, there are five cultivars registered as *P. trifoliata* var. *monstrosa* (T. Itô) Swing. in the Ministry of Agriculture, Livestock and Supply (MAPA). Cultivars were also registered by other agricultural Brazilian institutes. Two were registered by the Agronomic Institute of Campinas (IAC, 'IAC 848 Davis A' and 'IAC 718 Flying Dragon'). One cultivar was registered by the Agriculture Research and Extension Agency of Santa Catarina State (EPAGRI, 'Flying Dragon') and by the Rural Development Institute of Paraná (IAPAR-EMATER, 'IPR 150'). Additionally, the 'Citrolima Flying Dragon' is also registered [45].

Flying Dragon has some disadvantages, like the low nucellar polyembryony, requiring a very strict selection of seedlings to be grafted [46–48]. Besides that, this rootstock has seed germination and seedling uniformity between 80 and 90% [39]. It requires a longer period for commercial seedling formation than other rootstocks, mainly in low-temperature climates [49]. It is also a drought-sensitive dwarf rootstock [13], requesting a regular rainfall distribution. If the region has a well-defined dry period, irrigation is needed [50]. Nevertheless, under non-irrigated conditions and in soil without chemical restrictions, Tahiti lime grafted onto Flying Dragon

(1157 plants ha−1) and grown in a no-till system intercropped with *Urochloa ruziziensis* developed higher fruit production in the first 5 years. Apart from that, Tahiti limes grafted on Flying Dragon also showed reduced water stress, a better soil chemical and physical characteristics regarding tilled orchards [51].

The use of trifoliate oranges as rootstock demands specific soil fertility conditions, because of its high demand for nutrients [52]. These rootstocks have restrictions on the presence of toxic aluminum in the soil solution, and consequently, a restriction to acidic soils not corrected with liming [53]. With regard to Flying Dragon, there is poor performance in basic pH soils [39] due to the high requirement for iron [52]. Unlike plants of Citrus genus which have few or no root hairs under field conditions, trifoliate oranges can develop root hairs when grown in sand culture [54].

Flying Dragon is employed to Satsumas mandarins culture (*C. unshiu*) in protected structures of Japanese regions and in the southern United States [55]. In Southeast Brazil, it was used in 3% of total citrus seedlings produced in 2020, mostly to produce seedlings of 'Tahiti' lime (*C. latifolia)* [52], allowing planting densities of up to 2500 plants ha−1 [35]. Hence, in the first 3 productive years of the orchard, an increase in scions volumes and of the yield at the highest densities was observed [35]. For 'Tahiti' lime under irrigated conditions, there was a reduction in the yield efficiency regarding non-irrigated conditions. This lower yield efficiency is associated with an increase of more than 70% in scion volume due to irrigation [37].

In New Caledonia [28], the economic performance of 'Tahiti' orchards over 13 years under two installation conditions were compared: a high-density planting where trees were grafted onto Flying Dragon and a conventional orchard, where trees were grafted onto 'Volkamer' lemon. For high-density planting, the density was set at a rate of 1000 trees ha−1 while for the conventional orchard the density was 208 plants ha−1. The installation cost of the densified orchard was 2.6-folds higher than the conventional orchard because of the higher seedling cost and the planting labor. However, the recovery of invested capital occurred in 4 years for the densified orchard and in seven years for the conventional orchard. Furthermore, the cost of production was US\$ 0.30 and US\$ 0.57 per kg of fruit produced in the high-density plantation and conventional plantation, respectively. Therefore, the high-density orchard generated over 13 years a gross revenue 3.3-folds higher than a conventional orchard. In contrast, densified conditions with mechanical pruning seem to be inappropriate for 'Valencia' orange, 'Hamlin' orange, and 'Murcott' tangor (2020 plants ha−1) due to the small yields obtained [31].

Another option for Flying Dragon use is as an interlock to modulate vegetative growth. Nevertheless, there is a strong interaction with the rootstock and scion varieties employed. When intergrafted between rootstocks such as 'Swingle' citrumelo or sour orange, or scions as 'Star Ruby' grapefruit (*C. paradisi*) or 'Michal' mandarin (*C. clementina* × *C. tangerina*), Flying Dragon seems to reduce the vegetative growth [56]. On the other hand, when intergrafted under 'Tahiti' lime, the effect depends on the rootstock. A reduction in scion was observed when Flying Dragon was grafted onto 'Catania 2' Volkamer lemon (*Citrus volkameriana* Ten. & Pasq.). Oppositely, an increase in vegetative growth was seen when it was grafted onto *P. trifoliata* 'Davis A'. No effect on scion size was noticed when the Flying Dragon was grafted onto 'Morton' citrange and onto the 'Swingle' citrumelo [37].

Orange "Navelina" and lemon 'Kütdiken' plants intergrafted on Flying Dragon using sour orange as rootstock had 41.1% and 22.5% of growth reduction compared to non-intergrafted plants, respectively. In parallel, during winter and spring, the presence of the intergraft increased net CO2 assimilation for both canopies. To Navelina

orange trees, an increase in transpiration was also observed [57]. In 'Mexican' lime trees onto Alemow (*Citrus macrophylla*) rootstock, the use of Flying Dragon interstocks reduced the canopy volume by more than 60%. Then, there is the maintenance of fruit yields at commercially acceptable volumes (80 kg ha−1 ano−1). Also, this would be a viable approach for regions with HLB endemic occurrence [58].

As regards to dwarfing mechanism, the canopies grafted on the Flying Dragon trifoliate tree had a reduced sap flux compared to plants grafted on common trifoliate orange [38]. In comparison to common trifoliate trees, the Flying Dragon reduced the hydraulic conductivity of rootstock and of graft union regions. Further, a restriction of carbohydrate flow to the roots through the grafting region was described [59]. Besides, Flying Dragon had stem and roots xylem vessels larger as well as a lower phloem percentage than the vigorous rootstock Rough lemon (*C. jambhiri)* [60]. The lower carbohydrate flow through the grafting region to the roots supports the reduced root system and the increased production efficiency, expressed in mass of fruit per unit of canopy volume. Additionally, there was a reduction in net CO2 assimilation, of stomatal conductance. A reduction of transpiration between 12:00 and 3:00 p.m in plants grafted onto Flying Dragon compared to those onto common trifoliate orange was noted [59].

Phytohormones have different behaviors on dwarfing and vigorous rootstocks. The highest indolacetic acid (IAA) level was found in 'Eureka' lemon new shoots on 'Swingle' citrumelo and the lowest was found on Flying Dragon. Opposite effects were seen to abscisic acid (ABA). Higher content of ABA was seen in 'Eureka' lemon new shoots on Flying Dragon while lower ABA content was observed on 'Swingle' citrumelo. An assumption is that higher ABA levels account for plant growth reduction [61]. Likewise, the exogenous use of gibberellic acid and inhibitors of its synthesis are involved in the control of vegetative growth in citrus [62, 63].

Recently, *P. trifoliata* as a rootstock displays a potentiality to increase DNA demethylation and the amount of *24-nt small RNAs* on the orange scion compared to *P. trifoliata* grafted onto itself [64]. The evidence of possible epigenetic modifications imparted by grafting may also be associated with the mechanism of rootstock dwarfing.

#### **2.2 Others dwarfing rootstocks**

Several rootstocks are classified as dwarfing: 'Cunningham' and 'Yuma' citranges, 'Cuban' pummelo, *Citrus ichangensis*. Besides, other species belonging to the Rutaceae family, such as the genus *Hesperetusa, Citropsis, Clymenia, Eremocitrus e Microcitrus* have also a dwarfing effect [8, 26]. Nonetheless, in many cases, the dwarfing effect is not fully established. It is not clarified whether this effect is due to the rootstock effect itself, to the environment interaction with viral agents, or even to difficulties linked to rootstock/scion incompatibility [26].

In Spain, two dwarfing rootstocks developed by IVIA (The Valencian Institute of Agrarian Research) highlighted: Forner-Alcaide (FA) 418 and FA 517. The rootstock FA 418 is a citrangedarin, a hybrid of Troyer citrange (*C. sinensis* × *P. trifoliata*) with common mandarin (*Citrus deliciosa* Ten.). FA 517, is a citrandarin (*Citrus nobilis* Lour × *P. trifoliata*). Both rootstocks provided a large reduction in canopy volume and a significantly increase in yield efficiency of Navel orange compared to 'Carrizo' oranges. Along with that, both rootstocks induced the production of good quality fruit, with FA 517 inducing early entry into production. On pioneers roots (diameter 2–4 mm), FA 517 had a higher frequency of xylem vessels with diameters greater than 30 μm, while FA 418 showed higher densities of xylem vessels. These rootstocks reduced the hydraulic conductance, the net CO2 assimilation, the stomatal conductance, and the transpiration. A greater reduction was noticed in Navel orange over FA 418 [65]. Yet, the rootstocks were tested under ultra-high-density conditions, between 1250 and 3333 plants ha−1, and with mechanical harvesting (over-row continuous canopy shaking harvester) [66, 67]. Additionally, FA 517 exhibited resistance to Citrus tristeza virus, to *Phytophthora* sp. gummosis, and to nematode *Tylenchulus semipenetrans.* More*,* a good performance in saline and clayey soils resulting in high fruit yields beheld. On the other hand, FA 418, induced a greater reduction of tree size. Although larger fruits were obtained, they were more susceptible to the nematode *Tylenchulus semipenetrans* and to *Phytophthora* gummosis. Advantageously, FA 418 is tolerant to *Citrus tristeza* virus [68].

In USA, rootstock US-897 citrandarin was released by the US Department of Agriculture with the goal of reducing the size of plants in high-density orchards. His rootstock is used on 7% of the citrus orchards in Florida to high-density plantings in field and in protected structures. US-897 rootstock is a cross of Cleopatra mandarin (*C. reshni* Hort. ex Tan.) × Flying Dragon trifoliate orange (*P. trifoliata*). The yield of trees grafted onto US-897 is low. Nonetheless, due to the small size of the trees, calculations of the potential yield per hectare at the predicted optimum spacing can be very high. Despite the fruit good internal quality of US-897, its size can often be below average. It has tolerance to *Citrus tristeza* virus, citrus nematodes, the *Phytophthora–Diaprepes* complex, and high pH [69]. In-row spacings of 8 and 10 ft (2.42 and 3.05 m) are recommended for this rootstock [39].

Farther, new rootstocks have been produced by the University of Florida breeding program. Many of them are tetraploids, somatic hybrids, or sexual hybrids of two somatic hybrids. Among them, citrandarin UFR-6 (*C. reticulata* 'Changsha' + *P. trifoliata* '50-7') is a candidate for high-density plants, producing small plants, cold-hardy plants, and fruits with high soluble solids content [69, 70]. Beyond that, it is tolerant to *Phythophtora* gummosis and to *Citrus tristeza* virus. Plant spacing between 6 and 8 ft (1.83–2.44 m) is recommended [39].

**Table 1** summarizes the characteristics of rootstocks discussed so far: Trifoliate orange, Flying Dragon, FA 148, FA 517, US 897, and UFR 06. In this table, aspects related to horticultural performance and biotic and abiotic stresses are compiled.

In Brazil, the citrus breeding program of EMBRAPA (Brazilian Agricultural Research Corporation) has developed rootstocks by hybridization. Among the genotypes tested for the 'Valencia' orange, four are important with respect to dwarfing effect along with relatively high fruit yield, high yield efficiency, and good fruit quality. These rootstocks are three citrandarins (TSKC × TRFD-003, TSKC × TRFD-006, TSKC × TRFD-007) and one citrumelandarin (TSKC × CTSW-058), hybrids of Common Sunki mandarin [*Citrus sunki* (Hayata) Hort. ex Tan.] with Flying Dragon trifoliate orange [*P. trifoliata* var. *monstrosa* (T. Itô) Swing.] or with Swingle citrumelo (*C. paradisi* Macfad. × *P. trifoliata*). Apart from that, TSKC × TRFD-003 citrandarin had a similar drought tolerance to Santa Cruz Rangpur lime (*Citrus limonia* Osbeck) [71]. Also, in the 'Valencia' orange several other materials seem to have dwarfing potential. Among them, the TSKC × (LCR × TR)- 059 citrimoniandarin had a high yield efficiency, a dwarfing effect, an induction of earlier fruit-bearing with higher quality, and good drought tolerance [72, 73].

In other experiments with 'Valencia' orange in southeast Brazil, tetraploid Swingle citrumelo had a dwarfing performance which reduced canopy volume by 77% compared to the vigorous standard. In this same experiment, citrandarins offspring of Flying Dragon had no dwarfing behavior [74]. In 'Tahiti' lime, TS × PT 14 citrandarin had a dwarfing behavior and potential tolerance to HLB [75].


*a Sm–small; L–low; I–intermediate; Lg–large; H–high; P–poor; G–good; R–resistant; S–susceptible; T–tolerant. [ ] - Any symbol in brackets indicates a probable or expected behavior. \**

#### *Conflicting data in the literature.*

#### **Table 1.**

*Main features of dwarfing citrus rootstocks and common trifoliate orange (a semi-dwarfing rootstock) [39, 52, 68]<sup>a</sup> .*

Other dwarfing rootstocks are also approached. In hot arid climate in India, Fremont mandarin had dwarfing behavior when grafted on *Citrus pectinifera*, probably a *Citrus depressa* Hayata, compared to vigorous rootstocks (Karna khatta and Rough lemon) [76]. In China, hybrids of Ziyang Xiangcheng (*Citrus junos* Sieb. ex Tan.) and trifoliate orange (*P. trifoliata*) were researched and ZZ6, ZZ31, and ZZ948 rootstocks showed strong alkaline tolerance (pH 8.2). Among these hybrids, ZZ6 and ZZ948 were rootstock dwarfing type [77].

There are several potentially dwarfing rootstocks that have emerged in recent decades from worldwide breeding programs. Nevertheless, the confirmation of these potentials needs further investigations. In those investigations, it is required the evaluation of these materials under different scions and at different environments for a minimum period of time, to generalize this information [78].

#### **3. Conclusions**

Citrus dwarfing rootstocks are the main options to enable the development of designed orchards in high and ultra-high density planting systems allowing easy mechanical harvesting and cultivation under protected structures. Further, it is

*Dwarfing Rootstocks for High-Density Citrus Orchards DOI: http://dx.doi.org/10.5772/intechopen.102851*

paramount to perform a regional studies of different dwarf rootstocks genotypes and their interaction with the different scions as well as economic feasibility. With a well-conducted and designed studies, it is possible to establish recommendations and guide the correct management of dense citrus orchards in different environments. Therefore, the reduction of plant growth provided by rootstocks can be a management strategy to improve the orchard horticultural performance.

#### **Author details**

Mateus Pereira Gonzatto1 \*, Sabrina Raquel Griebeler2 and Sergio Francisco Schwarz2

1 Department of Agronomy, Federal University of Viçosa, Viçosa, Brazil

2 Department of Horticultural Sciences and Forestry, Federal University of Rio Grande do Sul, Porto Alegre, Brazil

\*Address all correspondence to: mateus.gonzatto@ufv.br

© 2022 The Author(s). Licensee IntechOpen. 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.

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Section 3

## Pest Management

#### **Chapter 5**

### Insect Pest Management in Fruit Production

*Murat Helvacı*

#### **Abstract**

Several pests cause destructive damages in fruit production. All of the pests cause yield loss but some of these cause transmission of virus diseases. For example, Brown citrus aphid transmits Citrus Tristeza virus in citrus production. Historically, broadspectrum pesticides were used to prevent the yield loss and transmission of bacteria and virus diseases in the world. These pesticides cause several problems including environmental, human health and also cause negative effects on soil health. At the same time, pesticides have other potential negative effects including food safety. For all these reasons, alternative management methods such as biological, biotechnical, sterile insect techniques are used in fruit growing all over the world.

**Keywords:** biological control, biotechnical method, pest, sterile insect technique

#### **1. Introduction**

The word "pest" describes an organism that harms crops, harms or irritates animals or humans. Agricultural pests include insects, weeds, bacteria, viruses, fungi and animals that reduce crop yield relative to the potential yield that would be possible in a pest-free world [1]. Some of the epidemic diseases have been carried by insects. In the 14th century, the Bubonic Plague epidemic disease influenced the population of Europe negatively and this disease was transmitted by fleas. Each insect species has different periods in its life cycle. The most important biological forms are "complete metamorphosis" and "incomplete metamorphosis" forms. In complete metamorphosis, the adult insect lays its egg in plant tissue or soil. The larvae that emerge from the eggs do not resemble the adult insect. As they feed and develop, they molt and become pupae. Pupation takes place on the plant or mostly underground. After a certain time, adults emerge from the pupa and the life cycle continues in this way. In incomplete metamorphosis, the nymphs that emerge from the eggs that the adult female gives birth are very similar to the adults. They look like a miniature of the adult. However, the wings are not developed. These nymphs molt as they feed, and their resemblance to the mother increases after each molting period [2]. The attacking of several harmful insect's damages plant leaves, buds, stems, fruits, flowers and seeds, causing significant crop losses and decrease the market value of crops. For this reason, applying of management methods against pests is significant in the agricultural production [1].

Pest control aims to safely maintain economic, effective and long-term pest control. Generally, it contains suppressing pest populations to economic injury levels rather than eradicating the pest completely. Many pests negatively affect agricultural production in the world. Many methods are used by the producers to minimize the quality and quantity losses of these pests in agricultural production. The main of these methods, which are considered for Plant Protection or Agricultural Control, are cultural measures, quarantine measures, mechanical and physical methods, biological method, biotechnical method, chemical method and integrated pest management, which expresses the combination of the necessary ones [3]. Today, chemical applications are made for producers in terms of ease of application and results [4]. Depending on pesticides for plant protection is related to undesirable effects on the environment, health, and the sustainable effectiveness of their use. The emergence of synthetic pesticides has made it possible to simplify crop systems and abandon more complex crop protection strategies [5]. Pesticides are chemical matters used to decrease the devastating effects of living forms such as rodents, insects, animals, weeds, fungi, which live on or around plants, human and animal bodies, and reduce or damage the nutritional value of food sources during production, storage and consumption. Pesticide term includes all of the chemicals classified as an insecticide (use for harmful insects), herbicide (use for weeds), fungicide (use for fungal diseases), rodenticide (use for rodents), molluscide (use for slugs), avicide (use for birds), acaricide (use for acars), ovicide (use to kill eggs of harmful insects), bactericide (use for bacterial diseases), nematicide (use for nematodes), etc. [6]. However, using of pesticides raises several environmental concerns, including human and animal health hazards. Food contaminated with toxic pesticides is associated with serious effects on human health, as it is the basic necessity of life. More than 98% of applied insecticides and 95% of herbicides end up somewhere other than their target species, including non-target species, air, water and soil. However, pesticides can contaminate soil, water and vegetation. In addition to killing insects or weeds, pesticides can be toxic to several other organisms, including birds, fish, beneficial insects and non-target plants [7]. Many harmful insects cause economic losses in fruit growing. For example, Stem borer (*Zeuzera pyrina* L., Lepidoptera: Torticidae) is an important pest that causes tree death by attacking stems. On the other hand, aphids, especially *Aphis pomi* De Geer (Homoptera: Aphididae), are serious pests as young pomegranate leaves are highly susceptible to aphid attacks. Although, these harmful negatively affect pomegranate production, the market value of pomegranate fruits is mostly affected by Citrus mealybug, *Planococcus citri* (Risso) (Hemiptera: Pseudococcidae), Medfly *Ceratitis capitata* (Wiedemann) (Diptera: Tephritidae) and Pomegranate butterfly, *Deudorix livia* (Virachola) (Klug) (Lepidoptera: Lycaenidae) [8]. In addition to this, Olive fruit fly (*Bactrocera oleae* Gmel.) (Diptera; Tephritidae) is a major harmful insect of olive and If management methods are not adequately implemented, large product losses can reach up to 80% in olive oil-producing areas and up to 100% in table olive growing areas [9] and Medfly (*C. capitata* Wiedemann) (Diptera; Tephritidae) can cause 20–25% losses in citrus fruits, 91% in peaches, 55% in apricots and 15% in plums [10]. Considering the damage done by insects in fruit growing; insect pests such as Mediterranean fruit fly and Olive fruit fly lay their eggs in the fruit (oviposition damage) and cause fruit drop; pests such as aphid, thrips and whitefly act as vector insect and cause virus diseases to spread. For instance; in most cases, there is a very close relationship between the parasite and the vector, and often the vector is the only means of transmission.

#### *Insect Pest Management in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.103084*

The simplest form of spread is known as mechanical transmission. Typically, the insect picks up the parasite on its body surface while feeding on the host organism and may release the parasite into a new host body or contaminate the food that will later be eaten by the host. However, many insects pests feed on plant sap and blood in vertebrates and can mechanically transmit pathogens and parasites through contamination of the proboscis [11]. It also has many undesirable effects such as resistance to diseases, insects and weeds. For this reason, since issues such as human health and the protection of biodiversity are kept at the forefront, the issue of chemical control has begun to be questioned [4]. In this study, the subject of chemical control and other control methods which are used as a management method against insect pests that cause economically significant losses in agricultural production is included.

#### **2. Management methods of insect pests**

Today, there are pests such as insects, diseases, weeds and animal pests (birds, rodents, etc.) that cause economic losses in agricultural production. Insects and other species that damage crops and also infect humans or animals are therefore pests that should be controlled as much as possible [1]. Some of the harmful insects play a role as vector insect in the spread of important diseases such as virus diseases. In addition, weeds host many disease agents and harmful insect species. Vector insects include aphids, whiteflies and thrips. To give an example, the Brown citrus aphid is the most significant vector insect of citrus tristeza virus (CTV) due to its superior vector productivity, especially for vigorous strains [12]. In the management against these insect pests, Integrated pest management (IPM) is an oncoming based largely on the information of pest biology and ecology to allow farmers to make tactical decisions to optimize ecologically and economically sound control of harmful organisms (pathogens, weeds, insects, vertebrates) [13]. Among these different methods of management; the method of suppressing the pest population with beneficial insects "biological control"; the method of management with using traps, "biotechnical control"; "cultural method", a method of management with using agricultural methods such as plowing, crop rotation; "chemical control" method with using pesticides such as insecticide, fungicide, acaricide; Methods such as "physical control", which includes methods such as manually collecting individual pests, pruning damaged plant tissues and removing excessively damaged plants, are applied. In this study, information is given about these control methods which are applied against pests that cause significant damage and economic losses in fruit growing.

#### **2.1 Chemical method**

Chemical control is the control method against harmful organisms that cause economic loss in plants, by using synthetic or naturally derived chemicals that have a killing effect (toxic effect). These products are called pesticides, synthesized substances or biological agents used to attract, seduce, destroy or mitigate any pest [14]. In addition to the benefits of these chemicals, it is known that they can create extremely important human, animal, plant and environmental health risks. For this reason, these chemicals are produced and sold subject to the most advanced control and inspection systems worldwide. Pesticide is defined by the FAO as a matter or mixture which is used to prevent, repel or destroy organisms such as animal and human vectors and unwanted plants and animals that cause damage in horticultural production.

Besides, FAO defines it as otherwise interfering with the processing, storage, production, transportation or marketing of products such as agricultural crops and animal foods [7]. Historically, in the 1930s, DDT was widely accepted as a pesticide that significantly conduced to the enhancement in the turnover of agricultural crops, especially food products, but then fell out of favor in the 1960s as a result of its different effects than usual [1]. The extent of the damage caused by the pests on agricultural products is high. Problems such as the overuse of pesticides used to minimize this damage and the environment, food poisoning and food insecurity are of great concern. However, insects and other species that cause damage to agricultural production and infect humans or animals have therefore become pests that need to be controlled as much as possible [4]. Pesticides are grouped in many different ways according to their appearance, physical structure and formulation, the pest and disease group they affect and their biological period, the type and group of the active substance they contain, the degree of toxicity and the technique of use. The most commonly used classification forms are the classifications made according to the harmful groups they are used and the active matter group in their structure. Pesticides are grouped by pest species or target organism. In this grouping, there are three main groups of pesticides. These are insecticides, fungicides and herbicides. The most important classifications of pesticides according to their chemical structures are organic chlorine pesticides, phosphorus, carbamates, natural and synthetic prethyroids [15]. The most important way to increase agricultural production; it is to get more products from the unit area, that is, to increase the yield. One of the most significant factors in enhancing the yield is to manage harmful organisms that limit plant production. Pesticide applications are intensively applied in fruit growing because it is easy to apply and effective in a short time.

#### **2.2 Biological method**

Biological method is the whole of the measures taken to use natural enemies, entomopathogenic microorganisms or to make them more effective against pests, diseases and weeds that damage crop plants. In other words, the agricultural control activity carried out by using natural enemies to suppress pests in agricultural areas and keep them below the level of economic damage is called biological control [16]. In the "Regulation on the Import and Release of Exotic Biological Control Agents" issued by FAO in 1996, biological control is defined as "a pest control strategy using living natural enemies, antagonists, competitors and other self-reproducing biological entities. This sentence can be said as the definition that best describes the biological method. Predator, parasitoid and entomopathogens are used as biological method agents. Predators live freely and directly feed on large numbers of prey during their lifetime. Parasites are organisms that live and consume or on a larger host [17]. Insect parasites (more precisely called parasitoids) are smaller than their hosts and develop inside or adhere to the outer part of the body of their hosts [18]. Predator insects lay their eggs next to their prey, and the hatched larvae consume their prey by stinging, sucking or chewing. Generally, predatory insects are polyphagous and therefore they are the most important agents which are used in biological control. Parasitoid insects, on the other hand, usually lay their eggs on the pest itself or its eggs. Parasitoid insect larvae emerging from the eggs cause the death of the pest's egg or itself, and in this way, they suppress the pest population and increase their own population. Entomopathogens include bacteria, viruses, fungi and nematodes used against harmful insects. Naturally occurring entomopathogens attack harmful insects, making them sick and sometimes killing them.

#### *Insect Pest Management in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.103084*

The best example of entomopathogens is the beneficial bacteria named "*Bacillus thuringiensis*", which is known as "Bt spray" in the agricultural companies. This bacterium can also be called a biological insecticide. Natural enemies have been used as a pest control method for centuries. However, in the last 100 years, there has been a significant increase in the understanding of humans and especially producers and the use of these biological control agents about how biological control agents, which are part of safe and effective pest control methods, can better manipulate pests [19]. Since the biological control method does not have negative effects on nature, the environment, in short on biodiversity and human health, it is a control method that should be used predominantly in agricultural production and especially in fruit growing. There are three types of biological control strategies implemented in pest control programs. These are importation (sometimes called classical biological control), augmentation and conservation. Classical biological control is defined as the deliberate introduction of an exotic (non-natural), often co-developed biological control agent for the permanent establishment and long-term pest control [18]. When a new pest enters from one country to another and there are no natural enemies of that pest in the country, its population increases in a short time and causes economic damage. To prevent this damage, natural enemies of the pest are imported from the country of origin and tried to be placed in the fauna where the pest is found. The need to re-establish interactions between harmful organisms and their natural enemies is based on the principle of importing and planting beneficial insects in locations where pests generally have no natural enemies or where the population of existing natural enemies is lower than the pest population. Within the scope of classical biological control against pests, 2000 biological control agent species and more than 5000 placement applications were made in 196 different countries. No negative effects of these practices, which have been carried out for years, have been detected [4]. Augmentation contains the additional release of natural enemies, rising the population which is found naturally. At a crucial stage of the growing period, few amount of beneficial insects can be extricated (inoculative release) or millions can be extricated (inundative release) [18]. The most commonly used biological control agents in this application are entomopathogens. Predator and parasitoid agents are more difficult and expensive to produce. Producing and multiplying predators and parasitoid agents in artificial media is less costly. However, the main problem here is to investigate whether these beneficial insects produced in artificial nutrient media are effective in nature, and accordingly, nutrient media should be prepared and produced. In addition, the production and release of predators and parasitoids into nature must be at certain standards. For example, an egg parasitoid should be made during the period when the pest egg is found in nature and at times of the day that are suitable for the parasitoid. For this reason, the production and release of predators and parasitoids are mostly applied in crops with high economic value and in greenhouses [4]. Conservation of natural enemies in an environment is the third method of biological pest control. Natural enemies are already adapted to the habitat and target pest and their protection through vegetation manipulation can be simple and cost-effective, while Classical Biological Control provides control of both primary and secondary pests, reducing the likelihood of pest outbreaks and resurrections [18]. This type of biological method can be reached in two ways: changing pesticide use and manipulating the growing environment in favor of natural enemies [20]. If natural enemies are adversely affected and their population declines, the pests get rid of the pressure of natural enemies and multiply in a short time and rise above the economic damage threshold.

Biological control, carried out by protecting and supporting native beneficial insects, gives more successful results in large areas than conventional and replicated biological control applications [17].

#### **2.3 Biotechnical method**

Biotechnical Control aims to prevent or control the normal biological or physiological activities of pests by using some artificial or natural compounds. That is, it interferes with the behavior and development of pests in their natural life processes such as feeding, mating, laying eggs, and flying. Some substances such as pheromone, attractant, antifeedant, kairomone, insect growth regulator, repellant, oviposition deterrent and chemosterilant are applied on biotechnical control. This management method can not pollute the environment and is compatible with other control methods and does not cause residue problems in foods. The compounds used in this method specifically target only the harmful organism and ensure the preservation of the natural balance. The biotechnical control method can be used in harmony with Organic Agriculture and Integrated Pest Methods [21]. The most commonly used pheromones for biotechnical control methods used within the scope of agricultural pest control are sexually attractive pheromones, which are secreted by females and invite males to mate, and aggregation pheromones that inform a food source or places suitable for nesting. In general, pheromones can be used for four different purposes; Use in combination with a trap for pest population monitoring (Monitoring), likewise combined with a trap for use in a mass trapping technique to reduce pest populations (Mass Trapping), inhibiting mating by emitting an intense signal, preventing males and females from finding each other and preventing them from mating and the use in the technique of mating (Mating Disruption) and finally, the use of pull and kill (Attract & Kill) technique by using it with an insecticide. Monitoring purposes are mostly aimed at determining the population development such as whether there is a pest, if it is, the first adult emergence, the periods when the population is dense, how long the pest is in the nature, when it goes to winter, and the flight period. The utilization of pheromones for monitor purposes is used in population monitoring of many pests [3]. Attractive traps such as McPhail, yellow sticky traps and delta traps are used against harmful insects belonging to the Tephritidae family such as Mediterranean fruit fly and Olive fruit fly, which cause product losses in fruit growing. However, due to the high cost of this type of traps, alternative traps can be used. These types of traps can be prepared by opening holes in the 1 lt. plastic bottles we use in our house, and putting apple juice + sugar mixture in them, and they can be used against these harmful insects, which belong to this family and cause significant yield losses in fruit growing.

#### **2.4 Cultural method**

One of the oldest methods of pest control in agricultural production is the cultural control method. However, with the development of synthetic pesticides, cultural control methods were quickly abandoned or not focused on, and research on them was largely stopped. The emergence of synthetic pesticides was effective in stopping these studies, as well as the fact that the cultural control method depends on preventive and long-term planning rather than an effective application method. It is applied as a pre-control method because it is less effective than other control methods.

#### *Insect Pest Management in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.103084*

There are many applications such as site selection, planting design and management (crop rotation, planting trap plants, planting and planting timing, placement of alternative hosts, etc.), plowing, irrigation, drainage, fertilization, removal of plant residues, mulching, adjustment of harvest time among cultural control methods [22]. The general principle in the processes considered as "Cultural Control" in the management against diseases, pests and weeds is to reduce the reproduction, shelter and living opportunities of harmful organisms by changing the environment in which they live in a way that is not suitable for the harmful organism. For successful cultural control, the most sensitive periods of harmful organisms should be determined, information about the interaction of host plant, harmful organism and environmental conditions should be learned to prevent the attacks of harmful organisms, to destroy them or to reduce the rate of reproduction, and cultural processes should be changed or developed accordingly. Cultural measures that have been applied for centuries from the past to the present are still important and up-to-date, as they are generally the sum of this knowledge and practices that have been experienced and adopted before, with positive results [23].

#### **2.5 Physical method**

The physical method of pests in fruit production has come to the fore in recent times because of the resistance development of pesticides avoidance from residue which causes pesticide and economic causes [24]. In physical control methods, the physical environment of the pest is changed in such a way that the insects no longer pose a threat to the agricultural crop. This can be achieved by creating stress levels ranging from agitation to death, or by using devices such as physical barriers that protect products or pants from invasion. While many physical control methods target a whole range of physiological and behavioral processes, chemical methods have well-defined and limited modes of action [25]. Physical control practices include repelling pests or restricting the accession of pests to plants, distorting the behavior of insects. In addition to this, this method includes the death of insects directly [4]. Physical methods are divided into two main groups. The name of these groups is active and passive [25]. Active methods include picking up the larvae of harmful insects, pruning of damaged or infected plant tissues, and removal of heavily damaged and infected plants. Generally, passive methods consist of the use of a tool or device to remove pests from a product. This equipment acts as a barrier between plants and pests, protecting plants from damage caused by insects. Other passive tools include repellants and traps [20]. Chemical and biological methods are often inharmonious; however, there is a harmony between cultural, biological, and physical methods and when used together they can be more effective against pests than chemical method.

#### *2.5.1 Sterile insect technique*

The idea of sterilizing insects' dates back to earlier than the invention and use of modern insecticides. Sterilization was first tried on *Lasioderma serricorna* (F.) (Tobacco beetle) in 1916, and the insect produced sterile eggs. However, an American scientist, Dr. E.F.Knipling started to work on this subject since 1937 and investigated the possibilities of management with insects by sterilizing them or making some changes in their genetic structures. As a result of long studies, Knipling was able to

make his first publication on this subject in 1955. There are mainly two sources of insect sterilization. The first is radiation, and the second is some chemical substances called chemosterilants.

Cobalt-60 and Cesium-137 are the most common sources used for this purpose. Radiation produces dominant lethal mutations in the gametes of insects. These lethal mutations actually do not adversely affect the maturation of the sex cells or the formation of the zygote, and they prevent the maturation of the zygote. Radiation, by interrupting the spermatogenesis in male, stops the formation of sperm (aspermia) and reduces the activity of the sperms or causes the loss of mating power. In this case, the male does not mate or fertilization does not occur because it cannot stay in the mating position long enough. In females, on the other hand, egg formation decreases or does not occur at all, since it damages the organia or the nutrient cells or both [26]. This method is applied effectively against pests such as Olive fruit fly and Mediterranean fruit fly and gives positive results as a management method against these harmful insects.

#### **2.6 Integrated Pest management method**

End of the 19th century, the idea of Integrated Pest Management began to emerge and some applications were seen in the early 20th century. It is noteworthy that in these first applications, only biological control was considered and applied besides chemical control. However, the concept of Integrated Pest Management in its current sense was first put forward in 1954 and its principles were determined in the symposium held in Rome in 1965 by the Food and Agriculture Organization (FAO). It is considered to be the most modern application developed in the field of plant protection. This practice, which is commonly known as integrated pest management and integrated pest control in English, has been defined in previous years with names such as Complementary Control, Complementary Pest Control, Integrated Control, Integrated Pest Management. This management method is defined by the FAO as a control method of pests that takes into account population fluctuations of pest species and their relationship with environment, and keeps their populations below the level of economic damage by using all appropriate control methods and techniques appropriately and this definition is accepted in the world. The aim of this method is expressed as the use of multifaceted tactics in good coordination to ensure balanced crop production, to keep the losses caused by pests at the level that will provide the highest economic gain, to meet the other goals of the farmers, to minimize the risks of pesticides on humans, animals and the environment [27]. Integrated pest management aims not only to suppress or eliminate the population of pests, but also seeks solutions that combine viable, economically acceptable, effective and environmentally friendly, sustainable ways. Integrated pest management aims not only to suppress or eliminate the population of pests, but also seeks solutions that combine viable, economically acceptable, effective and environmentally friendly, sustainable ways. Regular inspection of agricultural lands is always critical and must be done in an integrated management programme. Without control, the information needed to decide whether action should be taken in the first place and how severe the pest population is may not be gathered. Without all this information and properly determining how high and how widespread a pest is in the field, it may not be possible to make the right interventions at the correct time. Therefore, the population and spread of a pest should always be known before taking comprehensive action and planning. The basic principle of the integrated control method is to apply the control method when the

pest population rises above the economic damage threshold, not as a routine method that always exists. A carefully planned integrated control program aims to adjust the terrain to prevent the emergence of the pest in the first place and to completely destroy the pest itself or reduce its population if the pest is present in the land [4].

#### **2.7 Plant Defense chemicals**

Plants produce defensive metabolites that do not affect normal vegetative growth and development but reduce the palatability of the tissues in which they are produced [28]. In other words, plants have a variety of inducible and constitutive defense mechanisms to defend themselves against attack. These include structural defenses such as spines and waxy cuticles, as well as protein-based and chemical defenses [29]. Plants respond to herbivory through a variety of molecular mechanisms, biochemical and morphological and exhibit multifactorial traits that are constitutively expressed against herbivory or induced upon attack. Plant defenses activated in herbivores are a complex network of different pathways of direct and indirect defenses. Direct defense compounds such as glucosinolates or protease inhibitors directly affect insect performance and feeding behavior, while indirect defenses, such as the emission of volatile organic compounds after herbivore attack, act as attractants for the parasitic wasp that precedes the attacker. As plants develop new defense compounds or mechanisms, resistance to herbivores, their attackers find new ways to bypass or detoxify them [28]. Plant defense chemicals consist of secondary metabolites whose core structures are predominantly terpenes, benzenoids, phenylpropanoids, flavonoids or N-containing compounds. Plant defense chemicals can be classified according to their inducible or structural production. Initially, these classes were grouped according to their responses to pathogens were called phytoalexins and phytoanticipins. These have been defined as low molecular weight phytoalexins, "antimicrobial compounds that are both synthesized and accumulated in plants after exposure to microorganisms, and phytoanticips" as "low molecular weight antimicrobial compounds that are present in plants before they are threatened by microorganisms or are produced only after infection from pre-existing components". Defense compounds (phytoalexins) induced by these insects may have important functional roles as nutritional deterrents. The disadvantage of inducible defense systems is the delay in the synthesis of new compounds. An alternative strategy is to constitutively produce the compounds in tissues susceptible to attack. The disadvantage of phytoanticipins is the metabolic energy required to produce compounds even in the absence of insect threat and the active form of certain compounds being toxic not only to insects but also to the plant itself a common alternative approach to circumventing the toxicity problem is to store compounds as readily activated non-toxic forms and activate them upon insect attack. These compounds are known as phytoanticipins because they are produced in anticipation of a threat [29].

#### **3. Conclusion**

Global climate change and urbanization have increased the pressure on water, soil and climate, which are the natural resources of agricultural production. As a result of these pressures, existing breeding systems have also been damaged. Urgent measures are required to reduce the increasing pressure and to deliver natural resources suitable for agriculture to future generations. With the increase in the world population,

the production areas are decreasing. However, to meet the needs of people with agricultural products produced in these declining areas, the amount of agricultural products produced per unit area should be increased. It is not possible to increase agricultural production only with plant nutrition. It is imperative that plant protection measures are also fully implemented in agricultural products. Due to living and non-living effects, regressions occur in the growth and development of plants. There are some signs of disease in plants. The severity and intensity of these symptoms indicate the extent of the disease. Therefore, these symptoms in plants are very important to find the source of the problem by detecting it well and taking measures in terms of agricultural management. With this information obtained, methods that cause the least harm to the environment and nature should be applied to combat diseases. These management practices are a physical method, cultural method, biological method, biotechnical method, integrated pest management and sterile insect technique. Time is important in the fight against diseases. When the right time is not selected, the success of the control method applied decreases. It is a costly and challenging process for a diseased plant to become healthy. Therefore, it is important to prevent the plant from contracting the disease. Taking precautionary measures to prevent the plant from contracting the disease will provide longer-term gains. The most effective methods should be used without harming the living creatures in nature. When the 7 control methods, we mentioned above are used in the right time and manner, the yield, quality and pest protection methods in agricultural production will become easier. In order to, we can say that all of the methods we mentioned are used properly in sustainable agriculture. Pest control methods in agricultural areas will be much easier if sustainable farming methods are adopted and used appropriately.

### **Conflict of interest**

The author has no conflict of interest.

### **Author details**

Murat Helvacı European University of Lefke, Lefke, TRNC, Cyprus

\*Address all correspondence to: mhelvaci@eul.edu.tr

© 2022 The Author(s). Licensee IntechOpen. 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.

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#### **Chapter 6**

## Aphid on Almond and Peach in Tunisia: Species, Bioecology, Natural Enemies and Control Methods

*Lassaad Mdellel, Rihem Adouani and Monia Ben Halima Kamel*

#### **Abstract**

Aphids are among the most obnoxious pests of almond and peach in Tunisia. Accurate control of these insect pests requires the determination of their major species as well as the thorough understanding of the biology and identification of their major natural enemies. The scope of this chapter is to identify the main aphid species infesting almond and peach in Tunisia, to describe their biology, to determine their natural enemies and to study their efficiency as biological agents. A field survey was carried out during 2007–2016 period at Almond and Peach orchards in Tunisia. Results demonstrated the presence of *Hyalopterus pruni* Geoffroy, *Hyalopterus amygdali* Blanchard, *Brachycaudus amygdalinus* Schouteden, *Myzus persicae* Sulzer, *Brachycaudus schzartwi* Borner and *Pterochloroides persicae* Cholodkovsky. Biological study of recorded species demonstrated the presence of holocyclic and anholocyclic life cycle depending on host trees and aphid species. For predators, four families (Coccinellidae, Syrphidae, Chrysopidae, Cecidomyiidae) and one parasitoid and two entomopathogenic fungi species were identified. For control of *Pterochloroides persicae*, results showed that *Pauesia antennata* Mukergi was more efficacy than *Coccinella algerica* Kovar. This parasitoid should be reared and used in future integrated pest management program in almond and peach orchard in Tunisia.

**Keywords:** almond, peach, aphids, biology, predators, parasitoids

#### **1. Introduction**

Peach and almond are being considered as the most important fruit trees in Tunisia covering more than 22714.5 and 22139.9 hectares, respectively [1]. These fruit trees are tolerant to stress conditions (salinity, water deficiency) and still bear good yields. Nevertheless, a wide range of insect pests infest almond and peach trees reducing yield's quantity and quality. Among them, *Ceratitis capitata* Wieddeman (Diptera; Tephritidae), *Ruguloscolytus amygdali* Guerin (Coleoptera; Scolytidae) and aphids are considered as the major insect pests that affect almond and peach [2–8]. Of them, aphids are considered as the most destructive [3–5]. There are sap-sucking insects, which feed in colonies, cause

yellow leaf spots and deformity in leaves and flowers, transmit viruses, exude honeydew upon which sooty mold grows, but it also attracts ants. The ants, in return for the honeydew, they facilitate dissemination of aphids and carry wingless form to the trees carried the aphids to the trees when they are wingless [9–11]. In Tunisia, *Myzus persicae* Sulzer, *Hyalopterus pruni* Geoffroy, *Brachycaudus amygdalinus* Schouteden and *Pterochloroides persicae* Cholodokovsky are the most common aphid species that infest peach and almond [5–7, 12, 13]. Currently, protection of peach and almond orchards is mainly achieved by preventive and intensive chemical control. However, excessive pesticide misuse and selection of inappropriate active ingredients result in more crop diseases, auxiliary fauna destruction and environmental pollution. For that reason, selection of resistant cultivars and use of aphids' natural enemies (predators, parasitoids, entomopathogens) as pestcontrol alternatives probably provide the best long-term solution for aphid pest control [14–16]. Aphid biological control programs need the choice of natural enemy (predator, parasitoid, entomopathogen) based on their efficacy and climate adaptation and specificity. Some species of ladybird, hoverfly, ladybird, hover fly, green lacewing, true bugs and wasps are known as aphid natural enemies and considered as potential biological agents.

In Tunisia, extensive traditional growth of almond and peach trees in large cultivated areas can result in a flourishing habitat for attracting several aphid species and their natural enemies. In this chapter, we define the composition of aphid fauna and their natural enemies on almond and peach in Tunisia, and describe bioecology of defined aphid species and control methods of *P. persicae* using *Coccinella algerica* (Coleoptera; Coccinellidae) and *Pauesia antennata* (Hymenoptera; Lachninae).

### **2. Survey of aphid species in almond and peach trees**

This study was held in 11 sites of north, center and south of Tunisia, where wild almonds and peach distributed there. This study lasted ten years: 2006 until 2016,

**Figure 1.** *Tunisia map representing sites of study.*

throughout the aphid injury presence on almonds and peach. Several almond and peach varieties have been chosen (**Figure 1**).

#### **3. Aphids species on almond and peach in Tunisia**

Aphid species were identified according to Blackman and Eastop and using taxonomy keys [17–19]. Our results demonstrated the presence of six species that belonged to the Aphidinae and Lachninae subfamilies. For the Aphidinae, species *Hyalopterus pruni* Geoffroy (**Figure 2A** and **B**), *Hyalopterus amygdali* Blanchard (**Figure 2C** and **D**), *Brachycaudus amygdalinus* Schouteden (**Figure 2E** and **F**), *Brachycaudus schwartzi* Borner (**Figure 2G** and **H**) and *Myzus persicae* Sulzer (**Figure 2K** and **L**) were identified. These species usually feed on the young leaves almond and peach causing a stunted growth [20]. For Lachninae, we identified only the *Pterochloroides persicae* Kolodkovsky species that attacks the bark and trunk of almond and peach trees (**Figure 2I** and **J**) [20–24]. Of them, *H. pruni*, *M. persicae* and *P. persicae* are the most abundant species causing extensive damages on peach and almond [5, 6, 7, 13]. In Egypt and Syria, similar studies on almond and peach demonstrated the presence of the same species that were identified in this work [25–27]. Other aphid species (*Aphis gossypii* Glover, *Macrosiphum rosae* L., *Brachycaudus prunicola* Kaltenbach, *Aphis spiraecola* Patch, *Brachycaudus helichrysi*

#### **Figure 2.**

*Aphid species on almond and peach in Tunisia. (a:* Hyalopterus pruni, *b:* Hyalopterus pruni *on almond leaf, c:*  Hyalopterus amygdali, *d: Symptoms of* Hyalopterus amygdali *attack on almond, e:* Brachycaudus amygdali, *f: Symptoms of* Brachycaudusamygdalinus *attack on almond, g:* Brachycaudus schwartzi, *h: Symptoms of*  Brachycaudus schwartzi *attack on peach, i:* Pterochloroides persicae, *j:* Pterochloroides persicae *population on peach trunk, k:* Myzus persicae, *l: Symptoms of* Myzus persicae *attack on peach).*

Kaltenbach, *Brachycaudus persicae* Passerini, *Brachycaudus schwartzi* Borner, *Hysteroneura setariae* Thomas, *Macrosiphum euphorbiae* Thomas, *Myzus cerasi* Fabricius, *Myzus varians* Davids and *Hyalopterus persikonus* M. were also observed on peach and almond) could be observed on almond and peach and classified as rare [13, 28–30].

#### **4. Aphids bioecology infesting peach and almond trees in Tunisia**

Biology of infestation of different species that were identified in this study was recorded during the four seasons of each year. For *Hyalopterus* species, an ovoid green egg (**Figure 3**) was observed around dormant buds of almond and peach during November, December and January [20]. *Hyalopterus* was also observed on herbaceous plant *Phragmites spp* (Poales; Poaceae) in the rivers. This indicated that *Hyalopterus* species were dioeciously holocyclic, colonizing peach and almond as primary hosts and *Phragmites spp.* as secondary host. For the green peach aphid (*M. persicae*), ovoid and white eggs were found around dormant buds and the trunks of peach (**Figure 4**). The presence of eggs of *M. percicae* on dormant buds and trunks proved their holocyclic life cycle. Results considering egg-laying period were similar to those of the Jerraya's [4, 5]. However, Hulle et al. [31] showed that eggs of *M. persicae* were shiny black. However, Strathdee et al. [32] demonstrated that color of fertilized eggs can change. Holocyclic life cycle of *M. persicae* was demonstrated in several others studies [4, 5, 31]*.* In contrast, on herbaceous plants, only viviparous parthenogenetic females of *M. percicae* are present throughout the year (anholocyclic life cycle) [33, 34]. It is also an heteroecious holocyclic specie [35]. The study on *B. amygdalinus* bioecology showed that almond is the preferential host for this aphid species compared with the peach tree ones. This aphid is holocyclic dioecic, which was

**Figure 3.** Hyalopterus pruni *egg.*

observed on different spontaneous plants such as *Polygonum persicaria* (Caryophyllales; Polygonaceae) [31]. *B. schwartzi* was observed infesting both almond and peach without preference. *P. persicae* was observed on different parts of peach and almond (root, trunk, branch), and it is a parthenogenetic species in temperate regions and holocyclic species in cold regions [21]. Anholocyclic cycle of *P. persicae* in Tunisia was demonstrated in several studies [6, 13, 36]. In other countries, the anholocyclic cycle of this species was demonstrated [26, 37, 38]. The holocyclic cycle was also demonstrated [19, 39, 40].

#### **5. Aphids natural enemies**

Our survey on aphid taxonomy infestating almond and peach orchards in Tunisia revealed the co-existence of a wide range of natural enemies living in the same habitat. Insect natural enemies were collected and identified in laboratory according to Le Monnier and Livory [41], Chandler [42], Rotheray [43], Stary [44] and Lawrence [45]. Our results demonstrated the presence of four families of predators (Coccinellidae, Cecidomyiidae, Syrphidae and Chrysopidae). For Coccinellidae, we identified the following species *Coccinella algerica* Kovar (Coleoptera; Coccinellidae) (**Figure 5**), *Hyppodamia variagata* Goeze (Coleoptera; Coccinellidae) and *Scymnus apetzi* Mulsant (Coleoptera; Coccinellidae). Concerning population abundance, *C. algerica* is the most popular predator of the lady beetle species observed near all aphid colonies [20]. For Syrphidae family, *Episyrphus balteatus* De Geer (Diptera; Syrphidae) larvae (**Figure 6**) and adults (**Figure 7**) and *Metasyrphus carollae* Fabricius adult (**Figure 8**) were the two identified species. Larvae of *Aphidoletes aphidimyza* (Diptetra, Cecidomyiidae) (**Figure 9**) were the observed ear populations of *Hyalopterus species*, *M. persicae* and *P. pericae*. *Chrysoperla carnea* Stephens eggs and larvae were observed on aphid colonies at the end of April, May and June (**Figure 10**). *Aphidius transcaspicus* Telenga (Hymenoptera: Braconidae) (**Figure 11**) was the only identified parasitoid species on *Hyalopterus* species.

**Figure 5.** Coccinella algerica *Kovar.*

**Figure 6.** *Syrphid larva on* Pterochloides persicae *population.*

**Figure 7.** Episyphus balteatus *Degeer.*

**Figure 8.** Metasyrphus carollae *Stephens.*

**Figure 9.** Aphidoletes aphidimiza *larva.*

**Figure 10.** Chrysoperla carnea *larva.*

**Figure 11.** Aphidius transcaspicus *Telenga. a): mummies, b) adult.*

Entomopathogenic fungi naturally infecting *P. persicae* were collected and identified according to Humber [46] and Barnett and Hunter [47]. Two entomopathogenetic fungus were identified: *Beauveria bassiana* (Balsamo) Vuillemin (Ascomycota: Hypocreales, *Cordycipitaceae*) and *Metacordyceps liangshanensis* (Ascomycota: Hypocreales, *Clavicipitaceae*) [48]. In the word, *Capnodium spp*. in Central Asia and *Entomophthora thaxteriana* (Entomophthorales; Entomophthoraceae) were also identified on *P. persicae* population [47].

#### **6. Control methods**

#### **6.1 Efficiency of** *Coccinella algerica* **Kovar**

Efficiency of *C. algerica* to control *P. persicae* under laboratory conditions was studied. *C. algerica* eggs were collected. Emerged larva was separated and placed in test tube. Each larva instar was fed with *P. percicae* adults. Results demonstrated that the mean predation rate of *C. algerica* larvae during larval development time (9.8 ± 4.8 days) was of 30.13 ± 1.65 individuals of adult *P. persicae*. Of them, 72.3% were consumed by the first and second instar. Adults consumed daily 9.18 ± 0.088 *P. persicae* individuals. As for the efficiency of natural enemies, the predation of *P. persicae* by fourth instar larvae and adults of *C. algerica* demonstrated that both larvae and adults feed successfully on *P. persicae*. Several works demonstrated that predation rate of *C. septempunctata*, which is similar to *C. algerica* in morphology and biology [49], reared on *A. gossypii* in the same conditions of temperature and photoperiod was 9.7 aphids per day [50].

#### **6.2 Efficiency of** *Pauesia antennata* **Mukerji (Hymenoptera, Braconidae, Aphidiinae)**

*P. persicae* mummies were collected at May/2011 from almond trees from Iran and imported to entomology laboratory of Higher Agronomic Institute of Chott Mariem,

Chott Mariem, Sousse, 4042, Tunisia. Emerged parasitoids were reared and efficiency was studied. Results demonstrate that longevity of adult parasitoids is of 3 to 4 days. Cross and Poswal [51] showed that *P. antennata* has a very short life span (5–6 days). Longevity of *P. antennata* seems much shorter than that of *Aphidius ervi* Haliday, which was 12.29 ± 0.43 days at 20°C [52]. Parasitism and emergence rates were of 40.5 ± 12.4% and 36.4 ± 17.2%, respectively. The study of impact of aphid density on parasitism and emergence rates demonstrated that parasitism and emergence rates decreased by increasing aphid densities (45 ± 16.1, 36.4 ± 9.9 and 27.5 ± 8.1, for the three densities of *P. persicae*, D1 (50 aphids), D2 (100 aphids), and D3 (150 aphids), respectively). Similarly, emergence rate decreased when aphid density increased (40.8 ± 1.6, 31.2 ± 11.2 and 27.3 ± 12.2 on D1, D2 and D3 densities respectively). The study of aphid's population effect on *P. antennata* parasitism rate demonstrated that, upon introduction of one couple of *P. antennata*, parasitism and emergence rates decreased when the aphid population densities were high (D2 and D 3). Similar results were demonstrated for *Aphidius ervi* when the mean number of parasitized aphids and laid eggs during *A. ervi* female's life time increased with the increase of host density and the daily parasitism rate decreased when the host density increased to 50/ cylinder [53]. These results indicate that the parasitoid can adjust the oviposition strategy in response to host density. Effect of parasitoid number on parasitism rate increased when the number of released parasitoids increases. This is demonstrated also after using *Lysiphlebus testaceipes* parasitoid. Parasitism rate of this parasitoid species increased after release of eight *L. testaceipes* (four males and four females) for a density of 80 individuals of *A. gossypii* compared to parasitism rate after release of four parasitoid individuals [54].

#### **7. Conclusions**

This chapter highlighted the major aphid on almond and peach in Tunisia (species, bioecology, natural enemies and control methods). Among six aphid identified species, *H. pruni, M. persicae* and *P. persicae* were the most damaged species. These species can be multiplied either by parthenogenesis or by sexual form. For natural enemies, six predator's species, one parasitoid and two entomopathogenic fungus are identified. Among predators, *C. algerica* is the most widespread. However, this ladybird (larva and adult) is inefficient to control *P. persicae*. The introduction of specific parasitoid *P. antennata* and its use to control *P. persicae* showed efficiency. It can be used in future program for control of aphid on almond and peach. Future studies should focus on efficiency of *Aphidius transcaspicus* to control *Hyalopterus pruni* and on pathogenicity of *Beauveria bassiana* and *Metacordyceps liangshanensis* to *M. persicae* and *P. persicae* must have realized and used in integrated pest management program.

#### **Conflict of interest**

No conflict of interest to declare.

#### **Author details**

Lassaad Mdellel1 \*, Rihem Adouani<sup>2</sup> and Monia Ben Halima Kamel<sup>2</sup>

1 Plant Protection Department, National Organic Agriculture Center, Unaizah, Kingdom of Saudi Arabia

2 High Institute of Agronomy of Chott-Mariem, University of Sousse, Tunisia

\*Address all correspondence to: mdellell12@gmail.com

© 2022 The Author(s). Licensee IntechOpen. 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.

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