Abstract
Citrus fruits are among the most consumed fruits in the world. However, the world production of citrus fruits is faced with several constraints which hinder its development. Furthermore, the spread of pests such as mealybugs, mites and Mediterranean fruit fly has impacted negatively on citrus quality and yield. Therefore, the main objectives of this review were to identify the key harmful organisms to the citrus crops and to highlight the appropriate methods to manage them. In this paper, more attention was given to root rot and dry root rot diseases caused by Phytophthora spp. and Fusarium spp., respectively. It was concluded that the control of citrus pests was relied on the use of chemicals. The use of integrated orchard management methods remains the best practice to minimize the adverse effects of pesticides on the environment. Two fungicides, Fosetyl-Al and Metalaxyl, were widely curatively used to control Phytophthora root rot. Moreover, the control of dry root rot disease due to Fusarium spp. requires the optimization of irrigation and fertilization inputs. In addition to the use of sanitation practices, scouting and monitoring the appearance and development of key pests and diseases help to strengthen the control methods and reduce the use of pesticides.
Keywords: Citrus, pests and diseases, root rot, Phytophthora spp., Fusarium spp., integrated pest management strategy, Morocco
INTRODUCTION
WORLD SITUATION OF CITRUS FRUITS
Citrus fruit production and consumption worldwide have increased significantly since the mid-1980s. Production of oranges, mandarins, lemons and limes has increased rapidly, and even faster growth has been observed for processed citrus products. Partially, thanks to the improvements in transport and packaging that have led to lower costs and improved quality (FAO, 2004).
However, the rapid expansion of production and the slower growth in demand for oranges and grapefruits have led to lower prices of fresh and processed oranges and grapefruits. The rate of new plantings has slowed and the expected growth rates of production and consumption over the next ten years are expected to be lower than those recorded over the past ten years (FAO, 2004).
The citrus sector has changed significantly in recent decades. Italy was the leading producer until the 1970s, while Spain is now the leading producer in Europe and accounts for a quarter of world citrus fruit production. The new competitors are Australia, Morocco, Egypt, South Africa, Turkey, Portugal, Florida (USA), California (USA) and Uruguay (Anonymous, 2018).
World citrus production decreased slightly in 2015, influenced by a continued decline in orange production in the United States. This accounted for a decrease from about one million tons to 4.8 million tons. After growing by more than 10 percent per year for almost thirty years, citrus production in China increased by only about one percent in 2015. In Brazil, production increased by 3% (16.7 million tons) due to higher yields, but remains about 20% below its record level (FAO, 2016).
In South Africa, citrus production increased slightly to 1.5 million tons (+4.5%). This country is the main exporter of oranges in the world with 1.1 million tons, with the main destinations being the European Union and Russia. Egypt is the 6th largest orange producer in the world, its production for the 2012/2013 season is estimated at 2.5 million tons, with an increase of 4% compared to the previous season. Egypt is the world’s 2nd largest exporter of oranges with a volume of 1.1 million tons in 2012/13 (+10% compared to 2011/12) (MAPMDREF, 2013).
CITRUS FRUIT PRODUCTION AND AREA DISTRIBUTION IN MOROCCO
The citrus fruit sector in Morocco plays an important socio-economic role. This crop covers a surface area of 126, 600 ha and the average production is around 2.6 million tons per year. Since the program contract signed in 2008 between the government and the profession under the Green Morocco Plan came to effect, the citrus fruit sector has undergone significant development (Anonymous, 2018).
The main production regions are Souss Massa, Gharb, Moulouya, Tadla and Haouz, which alone account for more than 93% of the national area. The distribution of the surface area of citrus crops citrus by region is shown in figure 1.
A wide range of varieties characterizes the national citrus orchards, the three most cultivated varieties are the Clementine group (35%), Maroc-Late (21%) and Navels (18%). Table 1 shows the evolution of citrus production and the distribution of citrus fruits by variety group.
With most of the harvest now completed, Moroccan citrus production for 2018/19 attained about 2.6 million metric tons, an 18% increase over the previous marketing year. Mandarin production increased by 14% over the previous year to 1.35 MMT, while orange production increased by 18% to 1.2 MMT and lemon/lime production by 45,000 tons. Much of the increase in production is due to favorable weather conditions and an increase in the area harvested, as young trees begin to bear fruit. Exports of mandarins are expected to amount to about 585,000 tons, while exports of oranges are expected to reach about 190,000 tons (Anonymous, 2019).
KEY PESTS IN CITRUS ORCHARDS
Scale insects
In Morocco, mealybugs cause very serious damage to citrus fruits. The scale insect species inventoried in Moroccan citrus orchards are: Aonidiella aurantii Mask, Parlatoria pergandii, Lepidosaphes beckii Newman, Parlatoria ziziphus Lucas (Benziane et al., 2003).
Californian red scale, Aonidiella aurantii Maskell (Hemiptera: Diaspididae), is a major pest of citrus worldwide. The presence of scales on fruits reduces considerably their market value, resulting in important economic losses. Currently, integrated pest management, especially rational pesticide application, mineral oil sprays are used to control Californian red scale infestations in citrus orchards (Jacas et al., 2010).
The Mediterranean fruit fly (Ceratitis capitata)
In Morocco, the Mediterranean fruit fly causes significant damage to citrus fruits. It is considered a great challenge for researchers and farmers all over the world. C. capitata control programs have used conventional insecticides (organophosphates and pyrethroids). The combination of bait and insecticide sprays for fruit fly control has been used since the early 20th century (Roessler, 1989). Other control strategies, such as sterile insect techniques, have been used in the past, but their effectiveness was often limited (Mitchell and Saul, 1990). The use of synthetic insecticides has resulted in insecticide resistance, toxicity to non-target organisms, food residues and environmental pollution (Desneux et al., 2007).
Citrus mites
In Morocco, the main mites associated with citrus trees are the red mite (Panonychus citri), the yellow mite (Tetranuchus urticae) and the bud mite (Aceria sheldoni, Ewing) (Mazih, 2008). Panonychus citri is one of the most serious citrus pests. In addition to citrus, the mite inhabits many other plants, such as deciduous fruit trees, ornamental trees, vegetables and herbs (Bowman and Bartlett, 1978; Osakabe, 1987). It causes severe damage to citrus fruits, rapidly developing harmful populations in early spring, late spring and mid-fall. Acaricides have been widely used to control pest mites in orchards. However, occurrence of resistance problems are mostly caused by frequent acaricide use (Gerson and Cohen, 1989; Van Leeuwen et al., 2010) and have become more toxic to natural enemies. The use of synthetic acaricides has caused enormous concern for the environment and human health. Therefore, it is urgent to seek an effective acaricide against spider mites while preserving auxiliary fauna.
Snails
Snails are considered as one of the most important agricultural pests in humid regions of the world (Kiss et al., 2005). Molluscs cause enormous damage in Moroccan citrus orchards. They are well adapted to variations in air humidity. Therefore, it is important to continuously inspect the orchard, especially after rainfall or rising humidity (Ouzine, 2012).
There is a wide variety of methods for controlling citrus snails, but a strategy that combines several control methods is the most effective way to reduce snail damage. Regular application of 5% granulated metaldehyde after any increase in humidity from the environment to the plants, as well as tillage around the edges of the plots to destroy the pest and weed outbreaks is an effective method for snail control (Ouzine, 2012).
Aphids associated with citrus
Many aphid species attack citrus fruits. Among them, Aphis spiraecola, Aphis gossypii Glover and Toxoptera aurantii Boyer are widely distributed in citrus orchards (Kalaitzaki et al., 2019). Aphids cause considerable damage to trees directly by removing sap from the phloem of the plant while injecting saliva and this causes the plant to become phytotoxic. In addition, aphids cause indirect damage by secreting honeydew during sap feeding and moulds frequently develop on the honeydew, thus hindering photosynthetic activity (Blackman and Eastop, 2000). Aphids indirectly damage plants by transmitting the citrus virus Tristeza (Delkhosh and Tousi, 2009).
KEY DISEASES ASSOCIATED WITH CITRUS ORCHARDS
In agriculture, plant diseases are mainly responsible for the reduction of production, which leads to economic losses.
Tristeza
The Citrus tristeza Virus (CTV) is one of the most dangerous viruses infecting citrus trees. Its most dramatic expression is a quick decline, a syndrome in which a tree with normal appearance starts showing wilt symptoms and completely collapses in a few weeks. Commonly, infected trees show dull green or yellow thin foliage, leaf shedding and twig dieback, small chlorotic leaves resembling the effects of nitrogen deficiency, and small pale-coloured fruits are unmarketable (Moreno et al., 2008). CTV induces obliteration, collapse and necrosis of sieve tubes and companion cells close to the bud union, producing an excessive amount of non-functional phloem (Schneider, 1959). This causes progressive reduction of the root system with deficient supply of water and minerals, which results in wilting, chlorosis and dieback symptoms. As this specific interaction does not occur with many other citrus species, the tristeza syndrome can be avoided using decline-tolerant species as rootstocks (Schneider, 1959).
The ability to control disease damage depends to a large extent on the CTV incidence and on the virus strains and citrus varieties predominant in each region (Garnsey et al., 1998). Effective quarantine and budwood certification programmes are the best measures to avoid CTV introduction or dispersal in CTV-free areas where citrus are still propagated on sour orange rootstock (Navarro et al., 2002).
Citrus Greening
Citrus greening (Huanglongbing [HLB]) is one of the most serious and destructive diseases
of citrus worldwide. It is also called Yellow Dragon caused by a bacterium (Candidatus Liberibacter asiaticus) and transmitted by two species of psyllids Diaphorina citri in Asia and Trioza erytreae in Africa. The bacterium invades conductive tissues and causing citrus fruits decline by making them unproductive (Da Graça, 1991). Zinc deficiency and several other conditions can cause similar symptoms to citrus Greening, such as yellowing of the veins and adjacent tissues, followed by yellowing or staining of the entire leaf. These symptoms are sometimes accompanied by clogging of the veins, followed by premature defoliation, twig dieback, root rots, decreased in plant vigour and finally the plant die (Da Graça, 1991).
Greasy spot disease
Greasy spot is a disease caused by Mycosphaerella citri Whiteside. Its symptoms manifest on leaves or fruits. The disease begins with the appearance of yellow mottling on the leaf surface. Often, he infected surfaces turn a dark brown to black colour and take on a greasy appearance (Timmer et al., 2000). Affected leaves often fall before the dark black colour develops. The application of CaCO3, dolomites and urea helps to reduce inoculum at ground level (Mondal and Timmer, 2003). Copper-based fungicides are very effective in disease control. The application of benomyl is also effective in disease management, except that resistance to it is developing rapidly (Timmer et al., 2000).
Diseases caused by Alternaria spp.
The genus Alternaria can cause two diseases on citrus fruits: brown spot disease and black rot. These diseases begin with necrotic spots of a dark brown to black coloration on the fruit and manifests as black necrotic spots on leaves that can follow the veins of the leaves, and the stems also produce blackened lesions (Timmer, 1998). To limit the spread of the infection, it is recommend to avoid injuries during picking and dispose of contaminated fruit. For chemical control, the application three times of copper fungicides t are recommended. In rainy season, more frequent applications may be necessary for disease control (Timmer, 1998).
Citrus anthracnose
The genus Colletotrichum was recently named the eighth most important group of plant pathogenic fungi worldwide, based on its scientific relevance and economic importance (Dean et al., 2012). Colletotrichum species are responsible for anthracnose disease and post-harvest rot of many tropical, subtropical and temperate fruits, crops and ornamentals (Bailey and Jeger, 1992; Freeman and Shabi, 1998; Damm et al., 2012).
Two species, C. acutatum and C. gloeosporioides, are the main causal agents of citrus diseases (Damm et al., 2012). Post-harvest anthracnose was initially attributed to C. gloeosporioides, which was also reported responsible for preharvest symptoms such as shoot wilting, sunken spots or lesions (blight) of various colours in leaves and fruit decay (Benyahia et al., 2003). More recently, C. gloeosporioides has been more frequently associated with anthracnose in preharvest orange crops (Ramos et al., 2016; Rhaiem and Taylor, 2016; Guarnaccia et al., 2016). C. acutatum causes Postbloom fruit drop (PFD) of citrus and lime anthracnose (KLA) on citrus fruits. PFD is a disease restricted to flowers of sweet orange and most other citrus, and symptoms include petal necrosis, abscission of developing fruit, and the formation of persistent calyces (Pers et al., 2008; Lima et al., 2011). KLA is a complex of diseases related to leaves, flowers and fruits. Symptoms of KLA include necrotic lesions on leaves, fruits, twigs, flowers and shoot blight (Brown et al., 1996; Peres et al., 2008).
The most key symptoms of anthracnose on the leaves are the appearance of flat, light tanned areas that are more or less circular and slightly mottled. Brown to black spots, sometimes turning silvery grey, appears on ripe fruit. These lesions had a diameter of approximately 1.5 mm or more. Black fruiting are observed on the surface of the lesions and on the dried tips of infected twigs (Rhaiem and Taylor, 2016). Decay often progresses slowly and withers leaves eventually fall (Aiello, 2014). On fruits, symptoms appear as small, slight, irregular and sunken lesions, with a diameter of 0.5 cm or more, which could turn black (Aiello, 2014).
Orchard crop control methods mainly involve the use of appropriate sanitation techniques during processing of harvested fruits, transport, packaging and storage to avoid exposure of the fruits to the pathogen. As well as proper handling to avoid abiotic factors such as mechanical injuries and extreme temperatures, which can predispose fruit to pathogenic infection. The availability of primary inoculum of Colletotrichum spp. leads often rapid to epidemic development of the disease under appropriate conditions and reduces the effectiveness of many pre-harvest chemical treatments. However, general sanitation practices in orchard are essential in integrated disease control as the elimination of obvious sources of inoculum, such as diseased leaves and fruits, can increase the effectiveness of chemical control (Waller, 1972).
Overall, Colletotrichum diseases can be controlled by a wide range of chemicals such as copper compounds, dithiocarbamates, benzimidazole, triazole compounds, and other fungicides such as chlorothalonil, imazalil and prochloraz (Waller, 1993). In addition, other fungicide groups can be used to effectively control Colletotrichum species, including external quinone inhibitors “Strobilurins” (e.g. Azoxystrobin and pyraclostrobin) that interfere with mitochondrial respiration (Piccirilloa et al., 2018).
Phythophthora spp.
Phythophthora spp. diseases are the most threatening fungal diseases on citrus fruits under Moroccan conditions (Vanderweyen et al., 1982; Benyahia et al., 1998). Phythophthora pathogens cause extensive damage to the tree by attacking all parts and causing root rot, collar rot often with gum exudation on the trunk near ground level, and brown rot on fruit (Whiteside, 1988; Timmer, 2002). Both P. citrophthora R.E. Sm & E.H. Sm and P. parasitica Dastur are both cited as causal agents of gummosis and root rot of citrus (Javaherdehi et al., 2008). P. nicotianae is more common in subtropical regions of the world and causes foot rot and root rot. This species sometimes attacks the aerial parts of the tree and the fruit. P. citrophthora induces also brown rot on fruit (Graham et al., 2003). In addition, other Phytophthora species such as P. boehmeriae, P. cactorum, P. cinnamoni, P. citricola, P. dreschleri, P. hibernalis, P. megasperma, P. palmivora and P. syngiae have been reported pathogenic on citrus from different citrus-producing areas of the world (Erwin et al., 1996).
It was noticed that severely damaged and infected trees become dry in 1 or 2 months and then die. However, a careful monitoring allows usually early stages of the disease to be detected quickly and easily, such as wilting branches, which are generally observed two weeks after rainfall (Mahdavian, 2014). Furthermore, diseased trees show leaf chlorosis and shoot decline with reduced fruit production (Francis et al., 2015).
Phytophthora spp. infects the root cortex and causes degradation of fibrous roots. The cortex becomes soft, a little discoloured and appears to be soaked in water. The fibrous roots cover their cortex, giving the root system a stringy appearance. In the advanced stages of the decline, the production of new fibrous roots cannot keep pace with root death. Therefore, the tree is unable to maintain adequate absorption of water and minerals, and repeated fungal attacks deplete the root’s nutrient reserves (Graham and Timmer, 2003).
Diseased trees show cankers and gum exudations on the above-ground parts on the scions, especially on the major limbs, whereas rootstocks generally remain healthy (Francis et al., 2015). Infected bark remains firm with the formation of small cracks through which an abundant exudation of gum occurs. Citrus gum, which is water-soluble, disappears after heavy rains but is persistent on the trunk under dry conditions (Graham et al., 2003). Diseased bark becomes darker than the surrounding healthy tissues (Francis et al., 2015). It is often cracked and detached as the disease progresses. Lesions extend around the circumference of the trunk, slowly girdling the tree, and when they surround the trunk, trees eventually die (Francis et al., 2015).
Factors contributing to the Phytophthora disease and its control strategies
The irrigation system: In fact, there are significant correlations between the prevalence of the disease and a set of agronomic factors, particularly the irrigation system (Vincent et al., 2012). Inoculum density is higher in regions adopting surface irrigation systems, as soils in these regions are saturated with water due to the large amounts of water applied during each irrigation (Yaseen et al., 2010). It has been shown that the high populations of Phytophthora spp. and the incidence of the disease may be due to the number of zoospores released by sporangia when the soil becomes saturated (Lutz and Menge, 1986).
Good drainage and irrigation system management are essential for the regeneration of replacement roots. If Phytophthora spp. populations reach harmful levels, i.e. more than 10 to 20 propagules/cm3 of soil, their numbers will increase during wet periods, due to increased root infection (Graham and Menge, 1999). Infection in saturated soils is due to the fact that roots become damaged by reduced mineral forms and toxic metabolites, which predispose the tree to infection (Graham and Menge, 1999). So, farmers are advised to use the drip irrigation system, which gradually applies water to the soil, and only the soil directly under the dripper is saturated (Yasseen et al., 2010).
Soil salinity: Soil and irrigation water salinity has become a major constraint in Morocco’s citrus-growing regions (Chetto et al., 2015), and sour orange is the most widely used rootstock in because of its adaptation to most soils and its positive effect on the fruit quality (Omari et al., 2012). Although, its assets are numerous, its resistance to Phytophthora spp. attacks is drastically weakening in saline soil or by irrigation water (Sulistywati and Keane, 1992; Benyahia et al., 2003).
The climate: Environmental conditions are a key factor of infection rate of Phythophtora rot. P. citrophthora is more active during the coldest periods and probably survives as dormant sporangia or as chlamydospores and oospores (Graham et al., 2003). This pathogen develops well at moderate to low temperatures in the Mediterranean areas. It is more active during the winter when rainfall occurs. In addition, soil clogging increases the risk of Phytophthora propagules being dispersed by rainfall splashes from the soil to the tree fork (Vicent et al., 2012). For effective management of Phytophthora diseases, it is essential to integrate cultural practices such as the use of Phytophthora-free plant material and resistant rootstocks as well as the adoption of adequate watering system (Graham et al., 2003).
Resistant rootstocks: The use of resistant rootstocks is one of the most effective cultural methods for controlling Phytophthora spp. diseases. Although, this resistance is not absolute, but it was considered acceptable by Moroccan’s citrus growers (Benyahia et al., 2003). However, Benyahia et al. (2003) indicated that this resistance might be affected by the soil and water salinity observed in most citrus-growing regions. According to Benyahia et al. (2003) resistance to Phytophthora spp. is present in most citrus rootstock including trifoliate oranges, lemons, rough lemons, tangelos, macrophylla and volkameriana.
Preventive measures: To achieve exclusion, several measures are needed, including:
• Use of propagating material from listed and certified pathogen-free sources.
• Use of well water Phytophthora spp.-free for plant watering.
• Choice of selection site to avoid runoff from surrounding areas entering the nursery.
• Copper fences and footbaths at the entrances.
• Plants grown in containers containing soil-free from Phytophthora spp., nematodes and other harmful pathogens to citrus.
• Propagation must be carried out on benches 40 cm at least above the ground.
• Other recommended sanitation measures in nursery include frequent washing and disinfestation of soil, walls and benches (Graham and Feichtenberger, 2015). In case of susceptible rootstocks, foot rot on young trees can be mitigated by cultural practices such as ensuring adequate soil drainage (Feichtenberger, 2000; Feichtenberger et al., 2005; Graham and Menge, 1999).
Chemical control: Chemical control is necessary when other control methods are unable to effectively control Phytophthora root rot (Graham et al., 2011). Fungicide treatments should begin after the appearance of foot rot lesions. Fungicides applied as a spray to the trunk are the most effective (Feichtenberger, 1997).
Preventive treatments: Some fungicides, applied at high concentrations as a trunk injection, have long-term activity on zoospores of Phytophthora spp.; Captafol is a Phytophhtora spp. inhibitor at concentrations well below those of Captan or copper, but some copper-based fungicides are effective as captafol for long-term control. Captafol or some copper-based fungicides applied at high concentrations are much more effective than the equipment currently used for long-term control of Phytophthora infection (Timmer et al., 1977). The persistence of fungicidal activity varies considerably. Liquid copper formulations performed well than wettable powders. In addition, materials containing a high proportion of large particles, such as basic copper sulphate, were quickly washed off (Timmer et al., 1977). Pyroxychlor applied as a trunk paint has significant activity 13 days post-application on Phytophthora disease. In treated trees with pyroxychlor, the control activity covered only the bark surface in the treated area. Since the development of the disease is often limited to the bark and cambium tissue, the limited movement of the fungicide should theoretically reduce the growth of Phythophthora in infected trees. In addition, when pyroxychlore was applied on infected trees as a trunk paint, a curative action was observed. However, the product did not succeed in reducing the spread of the lesion on infected trees when it was applied to the ground (Timmer et al., 1977).
Curative treatments: It was reported that applying systemic fungicides likes Metalaxyl and Fosetyl-Al increased the weight of the fibrous roots of citrus rootstocks and reduced the propagules of P. parasitica (Sandler et al., 1989). Their applications of Fosetyl-Al and Metalaxyl should coincide with the onset of Phytophthora activity. This generally occurs at the beginning of the rainy season, from September to October (Feichtenberger, 1990). In major cases, one application of Fosetyl-Al/Metalaxyl is effective only in reducing the size of lesions on the trunk. Therefore, several applications of these systemic fungicides are necessary for adequate control of citrus gummosis. It was indicated that at least two foliar sprays of Fosetyl-Al during the rainy season are required for the complete control of P. citrophthora and P. parasitica (Feichtenberger, 1990). It should be stressed that adequate control of Phytophthora diseases on citrus relies on integrated strategy combining systemic fungicides with other control measures that includes the use of resistant or tolerant rootstock and other biological and sanitation practices (Feichtenberger et al., 1990). Consequently, the use of fungicides should be alternated in order to minimize the risk of developing resistant strains of the pathogen (Graham et al., 2011). Furthermore, applying fungicides after planting, i.e. metalaxyl and phosphite-based fungicides, should be determined by:
• The sensitivity of rootstocks;
• The probability of infection in the nursery;
• The history of Phytophthora diseases on the site (Feichtenberger et al., 1990).
Foliage or soil surface applications are less effective against root rot diseases. Fungicide treatments must be conducted for at least one growing season for tolerant rootstocks and beyond two growing seasons for susceptible rootstocks (Feichtenberger et al., 1990). Moreover, disease incidence can be lowered by adopting an integrated management approach that includes sanitation practices at the orchard level (i.e. prophylactic methods, pre-harvest fungicide application (e.g. copper-based fungicides) (Adaskaveg et al., 2015).
Dry root rot
Dry root rot of citrus (DRR), caused by Fusarium spp., is commonly widespread in nurseries and orchards. In nurseries, symptomatic infections can occur on citrus seedlings by producing dry root rot (Khouja et al., 2008). Several species of Fusarium have been identified and associated to dry root rot disease, including Fusarium solani which is considered the main species isolated from diseased citrus trees. Other species such as Fusarium oxysporum was also isolated and characterized (Hafizi et al., 2013). F. oxysporum is a ubiquitous pathogens of agricultural importance. It is widely distributed throughout the world, it has been isolated from diseased roots and rhizosphere (Hafizi et al., 2013). Fusarium equiseti (Corda) Saccardo, is a phytopathogenic fungus that produces secondary metabolites that can be toxic for cultivated plants (Kosiak et al., 2005). F. equiseti and F. semitectum Berkeley & Ravenel are rarely isolated from citrus roots (Smith et al., 1988); they are economically important species because they have been reported responsible for vascular wilt and root rot in various crops (Hafizi, 2013).
The phytopathogenic fungus F. equiseti can cause damage to various crops, including maize, rice and wheat in fields and during storage (Hasem et al., 2010). Palmero et al. (2011) reported that all Fusarium spp. isolates tested were shown pathogenic to tomato and melon. Abu Bakar et al. (2013) concluded that Fusarium species are among the common pathogens of post-harvest diseases causing rot on tomatoes and other perishable fruits and vegetables. A total of 180 Fusarium isolates were obtained from 13 locations throughout Selangor. F. solani was the most abundantly isolated (34%) followed respectively by F. semitectum (31%) and F. oxysporum (31%), F. subglutinans (3%) while the latter was F. equiseti (1%). In Tunisia, this pathogen has infected potato plants (Ayed et al., 2005).
The disease is commonly chronic, with symptoms beginning with a prolonged decline, accompanied with slight wilting and low vegetation outbreak (Khouja et al., 2008). At advanced decline stage, the canopy appears thin and sparse. In some cases, there is also the production of an unusually high number of fruits, resulting from flowering delay (Khouja et al., 2008).
Roots: Dry rot of citrus acts by invading the root system; the infected root turns from purple to greyish black (Sakovich, 2003). Kunta et al. (2015) observed that symptoms may include a reddish-purplish to greyish colour. One or more major roots structures are often blackened or dead, and brown discoloration extends into and through the trunk of the tree, and stopping at the union of buds (Figure 2).
Bark: DRR symptoms on the bark appear as a dark tinted colour, observation of the cross-section of infected trunk shows a greyish brown discolouration in the wood tissue (Sakovich, 2003). Nemec et al. (1980) demonstrated that in an advanced stage of the disease, leaves suddenly fade and dry out in a few days while remaining attached to the tree, which ends in a total collapse (Khouja et al.,2008). The discoloration of infected tissue may be limited to one section and not the entire tissue. Diseased trees become weak and lose their ability to produce good fruit (Adesemoye et al., 2013). In addition, leaves turn yellow and then brown, and followed immediately by a quick dieback (Kunta et al., 2015). Moreover, some trees apparently healthy wither and die suddenly, and their roots are blackened and rotten, with brown vascular discoloration in the rootstock trunk (Kunta et al., 2015).
Morphological and molecular characterization
In most cases, morphological identification is performed by preparation of fresh fungal cultures on a PDA medium in order to assess certain morphological traits, such as colour of the colony, growth rate, type of fructification, arrangement of spores and pigmentation. With regard to molecular characterization, colonies with same traits are grouped together and, in each group, a representative isolate is identified by DNA sequencing to confirm the exact identity (Khouja et al., 2008). Previous studies have shown that morphological traits are not reliable for species identification due to their variability under varying environmental conditions. Hence the need to use molecular tools to determine species by using specific primers T1 (5’ -AACATGCGTGTGAGATTGTAAGT-3’) and T2 (5’ -TAGTGACCCTTGGCCCAGTTGTTGTTG-3’) (Khouja et al., 2008).
Fusarium solani: Leslie et al. (2006) showed that colonies of F. solani on PDA medium developed abundant mycelium with purple-brown pigmentation, macroconidia are broad, straight, generally with 5 septate, with a basal cell in the shape of a poorly developed foot (Figure 3). The abundant, oval microconidia show 0 to 1 septate produced in false heads of long monophialidic conidiogenous cells (Leslie and Summerell 2006; Nelson et al., 1983). Hafizi et al. (2013) reported that, on palm trees, F. solani isolates have a brown to greenish-brown cottony mycelium with dark brown areas, as well as other isolates have a creamy white to greyish-white mycelium. The macroconidia were 27.0 to 37.3 µm long and 3.1 to 4.3 µm wide. Conidiophores are characterized by branched and long monophyalids. Chlamydiospores production is depending on the isolate. It was abundant in some isolates, while in others it was rare, even a- four-week post-incubation (Kunta et al., 2015). Kunta et al. (2015) found that the size of macroconidia ranged from 13-15×3-4 µm to 27-29×4-5 µm and that of microconidia ranged from 3-4×1-2 µm to 9-10×1-3 µm. The number of septa in macroconidia and microconidia is 3-5 and 0-1, respectively, and conidia are hyaline. Macroconidia are sickle-shaped with blunt ends and microconidia are round to oval. Intercalar and terminal chlamydospores were observed in all isolates of F. solani.
Fusarium oxysporum: Hafizi et al. (2013) described F. oxysporum as fungus with a cottony mycelium and pigmentation of colonies ranging from pale to dark purple or from white to pale purple. Macroconidia have a width of 30 to 40 µm and have 3 to 7 septate (Figure 4). Fungal isolates on PDA medium showed variable appearances with purple-peach colony colour.
Pathogenicity
Some authors attempted to reproduce the symptoms of citrus dry rot by artificial inoculation of healthy citrus seedlings with sporal suspension from different Fusarium species. The results differed from experiment to another. In Morocco, Bouhart (1993) inoculated citrus seedlings after their predisposition to nitrogen excess, leading to rapid development of the disease and the death of some inoculated plants. In Texas, Kunta et al. (2015) underlined that F. solani caused decline symptoms in inoculated seedlings 9 months post-inoculation; the inoculated seedlings showed reduced growth compared to the uninoculated control. In Tunisia, the pathogenicity test performed on olive seedlings showed the appearance of Fusarium disease symptoms within 20 to 25 days after inoculation (Rhaiem et al., 2017). Furthermore, some researchers’ successfully inoculated different citrus varieties by Fusarium spp. after weakening the plant material by various factors other than nematodes. Malikoutsaki‐Mathioudi et al. (1987) performed the pathogenicity of F. solani by exposing plants to abiotic stresses such as excess nitrogen, water stress, and excessive watering. Surprisingly, the highest mortality rates occurs in plants weakened by excess nitrogen and having mechanical injuries in the roots.
Factors favouring dry root rot disease of citrus
Water stress: The disease can spread over the field due to water stress, which predispose the plant to infection by Fusarium spp. However, the pathogen can colonize roots in the absence of stress, giving rise to an asymptomatic infection (Dandurand and Menge, 1992). Fusarium spp. has been shown to act by depleting the tree’s reserves of starch due to stresses conditions. Furthermore, some factors including poor drainage, excessive irrigation and poor aeration, might increase the possibility of Fusarium spp. infections on citrus trees (Kunta et al., 2015). Trees stressed due to environmental factors have shown a higher incidence of root rot disease than trees growing without stress (Polizzi et al., 1992). In addition, it was outlined that trees weakened by frost are prone to infection by F. solani (Nemec, 1987). Graham et al. (2003) found that F. solani infects only weakened citrus trees with reduced vigour. Intrinsically, F. solani seems to be a primary colonizer of citrus roots with less starch reserves in the tree due to stressful conditions.
Climate: The climate strongly affects the disease dispersal; a study carried out by Ippolito (1992) showed a peak of the disease within May and July, probably related to the temperature increase. Pathogen population increase may also result from root activity (Sandler et al., 1989), by starting to develop on May and ends on November; the presence of abundant nutrient in roots can stimulate the growth and provide a suitable substrate for the proliferation of the pathogen. This is in line with findings of Malikoutsaki et al. (1987) who reported that symptoms of dry root rot are more obvious and severe in summer likely due to high temperatures.
Resistance to dry root rot disease
Screening of a large number of citrus rootstocks has shown that resistance to F. solani is quasi-absent (Krueger and Bender, 2015). It is therefore necessary to seek sources of resistance by avoiding stressful conditions described above (Adesemoye et al., 2013). Other possible stresses include invasion by other pathogens, such as Phytophthora, which predisposes citrus trees to F. solani infections (Dandurand and Menge,1994), Tristeza virus (CTV), injuries caused by rodents, insects or weed control operations strongly influence the spread of the disease (Adesemoye et al., 2013).
Dry rot management
The management of dry root rot of citrus relies mainly on integrated control method. This strategy includes different measures such as eliminating the stressful factors that predispose citrus to sudden death; careful site selection with good surface drainage, and accurate monitoring of irrigation to avoid excessive watering. The use of inter-row cover crops can also improve soil structure (Donovan et al., 2007). Irrigation should be carried out with care, the trunk should be kept dry, and care should be taken with drainage because water should not be into contact with the treetops for an extended period of time (Adesemoye et al., 2013). The movement of equipment facilitates the spread of the pathogen, so the equipment must be thoroughly cleaned before moving it between orchards (Donovan et al., 2007).
There is a need for applying integrated disease management based directly on knowledge of the pathogen and its life cycle. This approach is an eco-friendly alternative to chemicals. Therefore, integrating sanitation practices and biological methods might help to overcome the dry rot disease on citrus. Furthermore, calcium is an important nutrient that has been used to control Phytophthora by reducing the release of zoospore, could be applied for dry rot control (Donovan et al., 2007). Sanitation practices is very useful and permit to clean plantations from remaining plants debris, which might harbour the pathogen primary inoculum. In addition, managing other devastating pathogens, which predispose the trees to DRR likes Phythophtora spp. is also essential. Finally, rational fertilization helps to minimize stress and disease occurrence; the application of insufficient or excessive nutrients should be avoided. The rational use of herbicides and other chemicals will also be useful (Donovan et al., 2007).
CONCLUSION
The citrus industry plays an important socio-economic role in Morocco. However, the development of this sector is hampered by a series of constraints, in particular pest and diseases problems. It appears that the most serious phytosanitary problems are caused by Mediterranean fruit fly, mites and mealybugs, Phytophthora root rot and dry root rot diseases. Managing of these constraints in the field relies on the adoption of integrated management practices, which include the use of pesticides, chemical copper treatments, and Fosetyl-Al for managing Phytophthora root rot.
REFERENCES
Abu Bakar A.I., Nur Ain Izzati M.Z., Umi Kalsom Y. (2013). Diversity of Fusarium species associated with post-harvest fruit rot disease of tomato. Sains Malaysiana, 42: 911–920.
Adaskaveg J. E., Hao W., Förster H. (2015). Postharvest Strategies for Managing Phytophthora Brown Rot of Citrus using Potassium Phosphite in Combination with Heat Treatments. Plant Disease, 99: 1477–1482.
Adesemoye A., Eskalen A., Faber B., Bender G., O’connell N., Kallsen C., Shea T. (2013). Curent knowledge on Fusarium dry root rot of citrus. Citrograph, 2011: 29-33
Aiello D., Carrieri R., Guarnaccia V., Vitale A., Lahoz E., Polizzi G. (2014). Characterization and Pathogenicity of Colletotrichum gloeosporioides and C. Karstii Causing Preharvest Disease on Citrus sinensis in Italy. Journal of Phytopathology, 163: 168–177
Anonymous (2019). Agrumes: des rendements record en 2018-2019. https://www.agrimaroc.ma/agrumes-rendements-record/
Anonymous (2018) (2). Maroc Citrus, 2018. http://maroc-citrus.com/statistiques-2, Consulted on 15/01/2019
Ayed F. (2005). La flétrissure fusarienne de la pomme de terre: comportement variétal approches de lute chimique et biologique. Mastère en Protection des Plantes et Environnement de l’Institut Supérieur Agronomique de Chott-Mariem, Tunisie, p 85.
Bailey J.A., Jeger d M.J. (1992). Colletotrichum: biology, pathology, and control. Wallingford, Oxon, UK : C.A.B. International.
Benyahia A., Ifi Jr., Smaili C. (2004). First report of Colletotrichum gloeosporioides causing withertip on twigs and tear stain on fruit of citrus in Morocco. Plant Pathology, 52:798-798.
Benyahia A., Jrifi A., Smail C., Afellah M., Timmer L. W. (2003). First report of Colletotrichum gloeosporioides causing withertip on twigs and tear stain on fruit of citrus in Morocco. New Disease Reports ,7, 20.
Benyahia H. (1998). Effet de la salinité sur le développement des maladies à Phytophthora des agrumes au Maroc, Univ. Cadi Ayyad, thèse, Fac. Sci., Semlalia, Marrakech, 170 p.
Benyahia H. (2003). Amélioration de la résistance des porte-greffes d’agrumes vis à vis des contraintes biotiques et abiotiques. Thesis, Cadi Ayyad University, Faculty of Science, Marrakech.
Benziane T. (2003). De la lutte dirigée a la lutte intégrée contre les principaux ravageurs en vergers d’agrumes au Maroc: cas de la région du Gharb. Thèse de Doctorat es-sciences. Université Moulay Ismail, Meknes (MR), 206.
Blackman R.L., Eastop V.F. (2000). Aphids on the World’s Crops. An Identification and Information Guide. 2nd ed. John Wiley & Sons, Chichester, 414 pp.
Bouhart. (1993). La pourriture sèche des racines et collet d’agrumes au Maroc : Agent causal et conditions d’infection. Thèse d’obtention du diplôme des études supérieures. Université Mohamed V. Faculté des sciences de Rabat.
Bowman C. E., Bartlett P W. (1978). Panonyhus citri (McGregor) (Acari: Tetranychidae) infesting imported citrus mites in England. Plant Pathology, 27: 201.
Brown A.E., Sreenivasaprasad S., Timmer L.W. (1996). Molecular characterization of slow-growing orange and key lime anthracnose strains of Colletotrichum from citrus as C. acutatum. Phytopathology, 86: 523–527.
Chetto O., Dambier D., Fadli A., Benkirane R., Talha A., Benyahia H. (2015). Mise au point d’un test in vitro de comportement au sel de quatre génotypes d’agrumes. Journal of Applied Biosciences, 88:8154– 8166.
Da Graca J.V. (1991). Citrus Greening disease January 1991, Annual Review of Phytopathology, 29:109-136.
Damm U., Cannon P., Woudenberg J.H.C., Crous W.P . (2012). The Colletotrichum acutatum species complex. Studies in Mycology, 73:37-113.
Dandurand L.M., Menge J.A. (1994). Influence of Fusarium solani on chemotaxis of zoospores of Phytophthora parasitica and Phytophthora citrophthora and on distribution of 14 C in citrus tissues and root exudates. Soil Biol. Biochem., 26:75–79.
Dean R., Van Kan J.A., Pretorius Z.A., Hammond-Kosack K.E., Di Pietro A., Spanu P.D., Rudd J.J., Dickman M., Kahmann R., Ellis J., Foster G.D. (2012). The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol., 13:414-30.
Delkhosh H.R., Tousi N. (2009). Historical review of Citrus tristeza virus and its vectors in Iran. In : D’Onghia A.M. (ed.), Djelouah K. (ed.), Roistacher C.N. (ed.). Citrus tristeza virus and Toxoptera citricidus: a serious threat to the Mediterranean citrus industry. Bari : CIHEAM, 2009. p. 135-140.
Desneux N., Decourtye A., Delpuech J.M. (2007). The Sublethal Effects of Pesticides on Beneficial Arthropods. Annu. Rev. Entomol., 52:81-106.
Donovan N., Macarthur E. (2007). Managing sudden death in citrus. Primefact: 755.
Oerke E.-C. (2006). Crop losses to pests. The Journal of Agricultural Science, 144: 31–43.
Erwin D., Ribeiro O. (1996). Phytophthora Diseases Worldwide. The American Phytopathological Society. Minnesota, USA; 562p.
FAO (2004). Perspectives à moyen terme pour les produits agricoles. http://www.fao.org/3/y5143f/y5143f10.html
FAO (2016). Situation et perspectives à court terme des marchés des produits.http://www.fao.org/3/a-mr076f.pdf
FAOSTAT (2016). Citrus fruit fresh and processed statistical bulletin. http://www.fao.org/3/a-i8092e.pdf. Consulté le 25/09/2019.
Feichtenberger E. (1997). Effect of systemic fungicide applications on growth responses and fruit yields of sweet orange trees in Phytophthora infested soil. Proc. Int. Soc. Citrus Nurserymen, 5: 267-279.
Feichtenberger E., Bassanezi, Rb, Spósito, Mb, Belasque, J. (2005). Maladies des agrumes (Citrus spp.). Dans: Kimati, H .; Amorim, L .; Rezende, Jam; Bergamin Filho, A .; Camargo, Lea (Ed.). Manuel de phytopathologie: maladies des plantes cultivées. São Paulo: Agronômica Ceres 2: 475-476.
Feichtenberger E. (1990). Control of Phytophthora gummosis of citrus with systemic fungicides in Brazil. EPPO Bulletin, 20: 139–148.
Feichtenberger, E., Spósito, Mb; Vianna Jht. (2000). Traitements fongicides contre la tache noire (Guignardia citricarpa) chez l’oranger ‘Valencia’. Summa Phytopathologica 26: 118.
Francis C. B., Vicent A. (2015). Gummosis of citrus in Ghana caused by Phytophthora citrophthora. Australasian Plant Pathology Society Inc.
Franco J.C., Garcia Mari F., Ramos A.P., Besri. (2006).Survey on the situation of citrus pest management in Mediterranean countries M. Bulletin OILB/SROP 29: 335-346.
Freeman S., Katan T., Shabi E. (1998). Characterization of Colletotrichum Species Responsible for Anthracnose Diseases of Various Fruits. Plant Disease, 82:596-605.
Garnsey S.M., Barrett H.C., Hutchinson D.J. (1987).Identification of citrus tristeza virus resistance in citrus relatives and its potential applications. Phytophylactica, 19: 187–191.
Gerson U., Cohen E. (1989). Resurgences of spider mites (Acari: Tctranychidae) induced by synthetic pyrcthroids. Exp. & Appl. Acarology, 6: 29-46.
Graham J.H., Feichtenberger E. (2015). Citrus phytophthora diseases: Management challenges and successes. Journal of Citrus Pathology 2.
Graham J.H., Menge J.A. (1999). Root health: Fungal diseases. Pages 126-135 in: Citrus Health Management. L. W. Timmer and L. W.Duncan, eds. APS, St. Paul, MN. Plant Dis. 73: 902-906.
Graham J.H., Timmer L.W. (2003). Phytophthora disease of citrus. Plant disease of international importance. Edis.ifas.ofl.edu. 5: 13-14.
Graham JH. (2011). Phosphite for control of Phytophthora diseases in citrus: model for management of Phytophthora species on forest trees? New Zealand J. of For .Sci., 41:S49-S56.
Guarnaccia V., Vitale A., Cirvilleri G. (2016). Characterisation and pathogenicity of fungal species associated with branch cankers and stem-end rot of avocado in Italy. European Journal of Plant Pathology, 146: 963–976.
Hafizi R., Salleh B., Latiffah Z. (2013). Morphological and molecular characterization of Fusarium solani and F. oxysporum associated with crown disease of oil palm.Brazilian Journal of Microbiology, 3: 959-968.
Hashem M., Moharam A., Zaied A., Saleh F. (2010). Efficacy of essential oils in the control of cumin root rot disease caused by Fusarium spp. Crop Protection, 29: 111-117.
Jacas J.A, Karamaouna F., Vercher R. , Zappalà L. (2010).Citrus Pest Management in the Northern Mediterranean Basin (Spain, Italy and Greece). In “Integrated Management of Arthropod Pests and Insect Borne Diseases”.
Javaherdehi S., Rahnama K., Alian M. (2008). Study of citrus gummosis in west of Mazandaran province. Proc.18th Iran. Plant Prot. Cong., Hamedan, Iran. 193 (Abst.).
Kafeshani F. A., Rajabpour A., Aghajanzadeh S., Gholamian E., Farkhari M. (2018). Spatial Distribution and Sampling Plans With Fixed Level of Precision for Citrus Aphids (Hom., Aphididae) on Two Orange Species. Journal of Economic Entomology, 111: 931–941.
Kalaitzaki A. et al. (2019). Aphid species composition in populations from citrus orchards in a region of the island of Crete. Bulletin of Insectology, 72: 143-149
Khouja H.R, Yaseen T., D’onghia A.M., Cherif M., Ippolito A. (2008). Etiological and epidemiological aspects of dry root rot in nurseries and orchards in Tunisia. Proc. Int. Soc. Citriculture 406p.
Kiss L., Labaunce C., Magnin F., Aubry S. (2005). Plasticity of the life cycle of Xeropicta derbentina (Krynicki¸ 1836) a recently introduced snail in Mediterranean France. J. Mollus Stud., 71:221-231.
Kosiak E.B., Holst-Jensen A., Rundberget T., Gonzalez Jaen M.T., Torp M. (2004). Morphological, chemical and molecular differentiation of Fusarium equiseti isolated from Norwegian cereals. International Journal of Food Microbiology, 99:195-206.
Kunta M, Salas B, Gonzales M, Da Graça Jv., (2015). First report of citrus dry root rot caused by Fusarium solani on sour orange rootstock in Texas. Journal of Citrus Pathology, 27974.
Leslie J.F., Summerell B.A. (2006). The Fusarium Laboratory Manual. Blackwell Publishing, Hoboken, 1-2.
Lima J. M., Camara A. C. L., Batista J. S., Soto-Blanco B. (2011). Clinical and pathological effects of Calotropis procera exposure in sheep and rats. Toxicon, 57: 183-185.
Lutz A.L., Menge J. A. (1986). Phytophthora root rot. Citrograph, 72, 33–39.
Mahdavian E., Javadi S. (2014). The Root and Crown Rot Disease in the Citrus of the West of the Mazandaran Province, North of Iran. Sci. Agri., 7:40-43.
Malikoutsaki-Mathioudi M., Bourbos V.A., Skoudridakis M.T. (1987). La pourriture sèche des racines – une maladie très grave des agrumes en Grèce. Bulletin OEPP/EPPO Bulletin 17: 335-340.
MAPMDREF (2013). Ministère de l’Agriculture et de la Pêche Maritime - Direction de la Stratégie et Statistiques. http://www.agriculture.gov.ma/sites/default/files/131126note_veille_strategique_agrumes-sl.pdf.
Masahiro M.H., Osakabe (1987). Esterase Activities and Developmental Success of the Citrus Red Mite, Panonychus citri (MCGREGOR) (Acarina: Tetranychidae), on Several Plants. Applied Entomology and Zoology, 22:35-44.
Maroc Citrus (2018). http://maroc-citrus.com/statistiques-2/, Consulté le 15/01/2019.
Mazih A. (2008). Current situation of citrus pest and the control methods in use in Morocco. IOBC/wprs Bulletin 38: 10-16.
Menge J.A., Nemec S. (1997). Citrus. In: RJ Hillocks, JM Waller, eds. Soilborne Diseases of Tropical Crops. Wallingford, UK: CAB International, 185-227.
Menge, J.A., Timmer L.W. (1982). Procedures for innoculation of plants with VA mycorrhizae in the laboratory greenhouse, and field, Pages 59-68. In N.C Schenck. Ed Methods and principles of Mycorrizal Research. Am Phytopathol Soc. MN. USA.244 pp+X.
Mitchell W.C., Saul S. 1990). Current control methods for the Mediterranean fruit fly, Ceratitis capitata and their applications in USA. Rev. Agr. Entomol., 78: 923-940.
Mondal S.N., Timmer L.W. (2003). Relationship of Epiphytic Growth of Mycosphaerella citri to Greasy Spot Development on Citrus and to Disease Control with Fenbuconazole. Plant Disease, 87:186-192.
Moreno P., Ambros S., Albiach-Marti M. R., Guerri J., Pena L. (2008). Plant diseases that changed the world - Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Molecular Plant Pathology, 9: 251-268.
Navarro L., Pina J.A., Juárez J., Ballester‐Olmos J.F., Arregui J.M., Ortega C., Navarro A., Duran‐Vila N., Guerri J., Moreno P., Cambra M., Medina A., Zaragoza S. (2002). The Citrus Variety Improvement program in Spain in the period 1975–2001 In: Proceedings of the 15th Conference of the International Organization of Citrus Virologists (Duran‐Vila N., Milne R.G. and Da Graça J.V., eds), pp. 306–316. Riverside, CA: IOCV.
Nelson P.E., Toussoun T.A., Marasas W.F.O. (1983). Fusarium Species: An Illustrated Manual for Identification, Pennsylvania State University Press, University Park.
Nemec S. (1978). Symptomatology and histopathology of fibrous roots of rough lemon (citrus limon) infected with Fusarium solani. Mycopathologia, 63: 35-40.
Nemec S., Baker R., Burnett H. (1980). Pathogenicity of Fusarium solani to citrus roots and its possible role in blight etiology. Proceedings of the Florida State Horticultural Society, 93:36-41.
OEPP (2004). European and Mediterranean Plant Protection Organization EPPO. Good Plant protection practice. Citrus, PP 2/27(1).
Ollitrault P., Navarro L. (2012). Citrus In Fruit Breeding: Handbook of Plant Breeding 8 (Badenes M.L., editor; and Byrne D.H., editor. eds), pp. 623–662. New York, USA: Springer.
Omari Fz., Beniken L., Gaboune F., Zouahri A., Benkirane R., Benyahia H. (2012). Effet de la nutrition azotée sur les paramètres morphologiques et physiologiques de quelques porte greffes d’agrume. Journal of Applied Biosciences, 53: 3773–3786.
Osakabe M. (1987). Esterase activities and developmental successof the citrus red mite, Panonychus citri (McGregor) (Acarina:Tetranychidae), on several plants. Applied Entomology and Zoology, 22: 35-44.
Ouzine M. (2012). Escargots: lutte en verger d’agrumes. Agriculture du Maghreb, 57: 92.
Palmero D., De Cara M., Iglesias C., Galvez L., Tello J.C. (2011). Comparative study of the pathogenicity of seabed isolates of Fusarium equiseti and the effect of the composition of the mineral salt medium and temperature on mycelial growth. Brazilian J. Microbiol., 42:948–953.
Peres N., Mackenzie S., Peever T. (2008). Postbloom fruit drop of citrus and key lime anthracnose are caused by distinct phylogenetic lineages of Colletotrichum acutatum. Phytopathology, 98: 345–352.
Piccirilloa G., Carrieria R., Polizzib G., Azzaroc A., Lahoza E., Dolores F.O., Vitale A. (2018). In vitro and in vivo activity of QoI fungicides against Colletotrichum gloeosporioides causing fruit anthracnose in Citrus sinensis. Scientia Horticulturae, 236:90-95.
Polizzi G. , Magnano G , Catara A. (1992). Dry root rot of citranges in Italy. Proc. Int. Soc. Citriculture, 2: 890-893.
Ramos A., Talhinhas P., Sreenivasaprasad S. (2016). Characterization of Colletotrichum gloeosporioides, as the main causal agent of citrus anthracnose, and C. karstii as species preferentially associated with lemon twig dieback in Portugal. Phytoparasitica, 44: 549–561.
Rhaiem A., Taylor P.W. (2016). Colletotrichum gloeosporioides associated with anthracnose symptoms on citrus, a new report for Tunisia. European Journal of Plant Pathology, 146: 219–224.
Roessler Y. (1989). Insecticidal bait and cover spray. In: Robinson A.S., Hooper G., editors. Fruit Flies, Their Biology, Natural Enemies and Control. Volume 3A. Elsevier; Amsterdam, the Netherlands: pp. 329–335.
Rosseler Y. (1989). Insecticidial bait and cover sprays. In : Robinson AS, Hooper G (eds) World crop pests : Fruit flies : their biology, natural enemies and control.
Sakovich N. (2003. Dry Root Rot of Citrus. Topics in Subtropics. University of California Cooperative Extension 1 (2).
Sandler H.A., Timmer L.W., Graham J.H., Zitko S.E. (1989). Effect of fungicide applications on population of Phytophthora parasitica and on feeder root densities and fruit yield of citrus trees. Plant Disease, 73: 902-906.
Schneider H.(1959). The anatomy of tristeza-virus-infected citrus. In: Citrus Virus Diseases (Wallace, J.M., ed.), pp. 73–84. Berkeley, CA: University of California Division of Agricultural Sciences.
Sulistyowati L., Keane P.J. (1992). Effect of soil salinity and water content on stem rot caused by Phytophthora citrophthora and accumulation of phytoalexin in Citrus rootstocks. Phytopathology, 82: 771–777.
Tennant P.F., Robinson D., Fisher L., Bennett S.M., Hutton D., Coates-Beckford P., McLaughlin W. (2009). Diseases and pests of Citrus (Citrus spp.). Tree and Forestry Science and Biotechnology, 3: 81-107.
Timmer L.W., Brown G.E., Zikto S.E. (1998). The role of Colletrichum spp. in postharvest anthracnose of citrus and survival of C. acutatum on fruit. Plant Disease, 82:415-418.
Timmer L., Garnsey S., Broadbent. (2003). Diseases of Citrus. In: Ploetz RC, editor. Diseases of Tropical Fruits Crops. CABI Publishing, CABI International, Wallingford, UK. 2003. p. 163-95.
Timmer L.W., Brown G.E. (2000). Biology and control of anthracnose diseases of citrus in :Prusky D.,Freeman,S. and Dickman , M.B.(eds), Colletrichum: Host specificity, Pathology and Host Pathogen interaction, 300-316 p. Am. Phytopathol. Soc. (APS), St. Paul, Minn, USA.
Timmer L.W., Garnsey S.M., Graham J.H. (2002). Compendium of citrus diseases, Am. Phytopathol. Soc. (APS), St. Paul, Minn, USA.
Vanderweyen A. (1982). Contribution à l’étude de la gommose à Phytophthora des agrumes au Maroc. Thèse de doc. Ing. Univ. de Nancy. 160p.
Van Leeuwen T., Vontas J., Tsagkarakou A., Dermauw W., Tirry L. (2010). Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol., 40: 563-72.
Vicent A., Botella-Rocamora P., Lopez-Quilez A., De La Roca E., Bascon J., Garcia-Jimenez J. (2012). Relationships between agronomic factors and epidemics of Phytophthora branch canker of citrus in southwestern Spain. European Journal of Plant Pathology, 133: 577–584.
Waller J. M., Bridge P. D., Black R., Hakiza G. (1993). Characterisation of the Coffee Berry Disease Pathogen, Colletotrichum kahawae Sp. nov. Mycological Research, 97: 989-994.
Waller J.M. (1972). Water-borne spore dispersal in coffee berry disease and it’s relation to control. Annals of Applied Biology, 71: 1-18.
Whiteside J.O., Garsnay S.M., Timmer L.W. (1988). Compendium of citrus diseases, Am. Phytopathol. Soc. (APS), St. Paul, Minn, USA, 105 p.
Yaseen T., Schena, Nigro, Ippolito. (2010). Phytophthora citrophthora is the predominant Phytophthora species in Syrian citrus groves. Phytopathologia Mediterranea, 49: 205-211.