There is no evidence of the species being invasive in the regions and countries where it is present. L. cicerina is not on the alert lists of either the International Union for Conservation of Nature (IUCN) or th...
There is no evidence of the species being invasive in the regions and countries where it is present. L. cicerina is not on the alert lists of either the International Union for Conservation of Nature (IUCN) or the Invasive Species Specialist Group (ISSG). It is not listed as a regulated species by EPPO in the ‘Action A1/A2 Lists of pests recommended for regulation’ for any of the countries of its occurrence. Its host specialization to only a few plants from the Fabaceae family, the climatic limitations and the great numbers of naturally-occurring parasitoids are some of the factors that prevent the species from becoming an invasive. There are no data about any major introductions of any economic importance.
Leaf-mines were first recorded in the literature towards the end of the seventeenth century when Beckmann (1681) (as quoted in Spencer, 1973) discussed and illustrated the strange forms that had appeared in great numbers the previous year on cherry trees in the Frankfurt/Oder area in Germany. He was able to show that the mines were caused by insects and illustrated the lepidopterous larvae responsible. Fifty years later, Reaumur (1737) (as quoted in Spencer, 1973) discussed and illustrated Agromyzid leafminers on Sonchus oleraceus, Trifollium, Ranunculus and Lonicera for the first time. These species were not given names, but are readily identifiable from their host-plants.
The first record of damage to crops was given by Rondani (1875), when describing L. cicerina attacking Cicer arietinum.
The genera in the two sub-families Agromyzinae and Phytomyzinae are readily identifiable by the course of the sub-costa, which joins vein R1 in the Agromyzinae, and runs straight to the costa, at least as a fold, in the Phytomyzinae (Spencer, 1973). Among the 25 genera in the family, genus Liriomyza is ranking second in significance (Spencer, 1973).
There are 376 species currently recognized in the genus Liriomyza (family Agromyzidae), with 136 of these species found naturally in Europe (Seymour, 1994). The adult flies of all these species look very similar. They are all small, being between 1 and 3 mm in length, and from above are seen to be mostly black with, in most species, a bright-yellow scutellum. As a result, separating these species can be difficult. Close examination reveals small external differences that can be used to separate the species such as the relative length of sections along particular wing veins, the presence, position and size of certain setae or the colour of the cuticle at the point where particular head setae arise. However, considerable variation in these character states is seen in the polyphagous pest species. As a consequence, for the pest species concerned, the ranges of the variation of these characters often overlap, limiting their diagnostic value.
Very small, dark species, with darkened third antennal segment (Spencer, 1973).
Frons 1.5 times width of eye, increasingly projecting above eye towards base of antennae, orbits conspicuously differentiated, raised and paler than frons: 1 reclinate ors, 2 or sometimes 3 incurved ori, orbital setulae sparse, reclinate; jowls deeply extended at rear, they are half the vertical height of eye, cheeks forming broad ring below eye; third antennal segment small, round.
3+1 dc, acrostichals sparse, irregularly in 2-4 rows (Spencer, 1973).
Length from 1.3- 1.5 mm, costa extending strongly to vein M 1+2, discal cell small, l-st section of M 3+4 3 times length of penultimate (Spencer, 1973).
Frons orange-yellow, orbits distinctly paler-yellow, sometimes narrowly darkened beside eye margin and blackish around base of ors; vertex dark, at least outer vertical bristle on black ground; jowls orange, face somewhat grayish, palps black; third antennal segment variably darkened, in darkest specimens almost entirely black, first and second segments yellowish; mesonotum deep black, shining from behind, but more mat viewed from front; mesopleura normally black along lower and front margins, paler above, more rarely with only a small black patch on lower margin; legs dark, femora although basically yellow, largely darkened by variable black striations (Spencer, 1973).
Larval posterior spiracles each with 7-9 pores; the two processes widely separated (Spencer, 1973).
With more than 2500 described species belonging to 27 genera in the world, Agromyzidae (leafmining flies) is one of the largest fly families. From this family, 776 species were identified in Europe. (Spencer, 1972, 1976, 1990).
As a hole the greatest number of genera in Agromyzidae - 75, is distributed in Europe, Japan and temperate Asia, followed by North America - 35 genera, Tropical Asia and Pacific - 25, Africa - 19, South America - 17 and Australia and New Zealand - 14 . Leaf-mining genera, such as Liriomyza and Phytomyza are dominant in more temperate areas and are reduced to insignificant numbers in the tropics (Spencer, 1973; Parrella, 1987).
Believed to be of Neotropic origin, the geographical distribution of Liriomyza species was restricted to the New World until the mid-1970s. As a result of anthropogenic activities, these species now occur in most of the temperate and tropical regions in the world (Minkenberg and van Lenteren, 1986).
In Europe many species have been locally troublesome, such as Liriomyza cicerina on chickpea, L. bryoniae on tomatoes and cucurbits, L. cepae and L. nietzkei on onions, etc. (Spencer, 1973), which are different from the species, mentioned for South America, US, New Zealand, Australia, etc.
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
According to Spencer (1973) the species is native to the Mediterranean area. L. cicerina occurs commonly on Ononis species in western Europe and it seems probable that this is the primary host, from which it colonized Cicer arietinum when this was introduced into southern Europe from India in classical times. He made this conclusion based on the fact that there were very few Oriental Liriomyza species and no records of L. cicerina from India or elsewhere in western Asia where C. arietinum was native.
The host plants of L. cicerina are only from the Fabaceae family: Cicer arietinum (chickpea) (Hering, 1957; Spencer, 1973); Hymenocarpus circinnatus (disc trefoil) (Hering, 1957); Melilotus alba (white sweet clover); Melilotus officinalis (yellow sweetclover) (Robbins, 1983); Ononis species, including Ononisarvensis (field restharrow) (BMNH), Ononishircine (Hering, 1957), Ononis repens (common restharrow) (Hering, 1957), Ononisspinosa (spiny restharrow) (Hering, 1957). There is new record of L. cicerina found as a pest of faba bean (Vicia faba) at Damnhour region in Egypt (El-Serwy, 2003).
Spencer (1973) suggested that the primary host plants are likely to be the European plant Ononis spp. because he assumed the centre of origin of L. cicerina to be in Europe. Since chickpea was introduced from India he supposed that a host switch to Cicer was established in Europe. However, recently L. cicerina was confirmed from India (Naresh and Malik, 1989). It is unknown whether or not
L. cicerina damages the host plant in two ways; females puncture the plants to feed before ovipositing, but the more serious damage is caused by the larvae, mining the leaves (Lahmar and Zeouienne, 1990). The adult females puncture the upper surface of chickpea leaflets with their ovipositor and feed on the exudates from these, which causes a stipple pattern on the leaflets. In some of the feeding punctures, eggs are inserted just under the epidermis (Weigand, 1990a). The leafminer larvae feed in the leaf mesophyll tissue forming a serpentine mine that later becomes a blotch. The mining activity of the larvae reduces the photosynthetic capacity of the plant and heavy infestation may cause desiccation and premature fall of leaves (Weigand, 1990a).
In his original description of this species in 1875, Rondani wrote: “Larva mining the leaves of C. arietinum, frequently causing substantial damage” (Spencer, 1973). Shevtchenko (1937) recorded that mined leaves turned yellow, dry up and many fall prematurely. Lower leaves were attacked first and often only three or four healthy leaves remained on each stem.
L. cicerina was found quite common in all the surveyed chickpea fields in Syria (Sithanantham and Reed, 1980), attacking the spring-sown crop more severely than the winter-sown crop and varieties with large leaflets more than those with small leaflets.
Shevtchenko (1937) made a detailed study of this species in Ukraine. He found that there could be as many as four generations between April and August. Adults emerge from overwintering pupae as temperatures increase at the beginning of Spring. In Slovakia, adults of the hibernating populations emerged in May; the next emergence was in July. Part of this generation completed its life cycle in mid-August and disappeared; the other part remained in diapauses during the winter and completed its life cycle the following Spring (Pastucha, 1996). In Romania, the pest had three to four generations per year and larvae were present throughout the vegetative period (Banita et al., 1992). In a much warmer climate (Morocco), the date of emergence varied between years, but in a single year, most L. cicerina emerged within a week, with little difference between geographical areas (Lahmar and Zeouienne, 1990). In 1983, the time between the first appearance of adults in the fields and the first larval damage was 12 days. In Turkey, Hincal et al. (1996a) reported that the adults of L. cicerina emerged in the second half of April and the first half of May, when average temperature was 9.0-14.3oC and the ground temperature was 19.2-21.2oC. The larvae appeared 3 to 20 days after adult emergence when the plants were 5-10 cm high. There were two peaks in the population density of the leafminer: one at the end of May; and the second at the end of June.
According to Shevtchenko (1937), the egg stage lasts for 2-3 days, and 42% of the leaves contain a single egg, 45% - two, 9% - three, 2% - four and 2% - five eggs. The larval mine is on the upper or lower surface of the leaf and is linear, shallow, at first greenish, later whitish, winding irregularly and frequently forming a secondary blotch. The life cycle is completed in between 20 and 30 days, the pupal stage lasting generally from 10-12 days in the early generation. Under the conditions of Morocco, the development time of the first generation was only 25 days and was followed by three overlapping generations before the Summer diapauses in July (Lahmar and Zeouienne, 1990).
Del Canizo (1934) has studied the species in Spain where the main areas of cultivation of Cicer arietinum are Castille, Estramadura and Andalucia and he has confirmed the very large populations frequently present in the early generation when fields of chickpea can be seen with scarcely a single plant unaffected.
Judging from the distribution, L. cicerina prefers arid, semi-arid and temperate (especially Mediterranean) climate conditions. Higher humidity and higher irrigation levels cause increase of the leafminer population density (Cikman and Civelek, 2006).
A braconid in Spain was found to parasitize up to 90% of larvae of the first generation of L. cicerina on chickpea, thus effectively reducing populations later in the year (Del Canizo, 1934). The identity of this species is not certain, but it is possibly Opius pygmaeus, which has been confirmed parasitizing L. cicerina in Surrey, England (Fischer, 1972). In more recent studies, again in Spain, Garrido et al. (1992) found the parasitoid Opius monilicornis and Tormos et al. (2008) found Dacnusa cicerina sp. n. Eurytoma sp. is reported as a possible hyperparasitoid of D. cicerina. A comparison is made between the larvae and the adults of several Dacnusa species (Tormos et al., 2008): the adults of D. cicerina are similar to those of Dacnusa rodriguezi. The immature larvae are similar to those of Dacnusa areolaris and Dacnusa dryas, and the mature larvae are very similar to those of D. dryas, from which they differ in having scale-like sensilla on the thorax and abdomen. The venom apparatus is very similar to that of Dacnusa flavicoxa, differing from it in length of the reservoir and the number of gland filaments. The mature larva of Eurytoma illiger has well-differentiated pleural and ventral setae.
In Morocco, O. monilicornis was identified (Lahmar and Zeouienne, 1990). Hincal et al. (1996b) reported O. monilicornis in chickpea fields in the region of Izmir, Denizil and Usak, Turkey in 1991-1994. In a study of the parasitoids on Agromyzidae pests in cultivated and non-cultivated areas in Turkey among which L. cicerina was included, a total of six parasitoids from Braconidae and 12 parasitoids from Eulophidae (Hymenoptera) were registered (Cikman and Uygun, 2003). It is not clear which parasitoid parasitizes which host. Later, in the region of Sanhurfa, Turkey, Cikman et al. (2008) found a total of eight parasitoid species on L. cicerina on chickpea: the braconids O. monilicornis and Opius tersus; and the eulophids Diaulinopsis arenaria, Neochrysocharis formosa, Diglyphus crassinervis, Neochrysocharis ambitiosa, Neochrysocharis sericea and Pediobius metallicus. In Ankara province, Gencer (2004) found only one parasitoid attacking larvae and pupae of L. cicerina – Pediobius acantha.
Sithanantham and Reed (1980) established that many of the collected larvae and pupae in chickpea fields in Syria were parasitized, but no information was given about the species. Later Weigand (1990a) reported two parasitoids on L. cicerina in Syria: Diglyphus isaea and Opius monilicornis, and El-Bouhssini et al. (2008) reported the parasitoid O. monilicornis. D. isaea has been reported for the first time from Tehran and West Azerbaijan as a parasitoid of L. cicerina (Adldoost, 1995).
Several parasitoids are mentioned as present in faba bean fields at Damnhour, Sids and El-Zarka in Egypt on L. cicerina, Liriomyza bryoniaeand Liriomyza sativae: D. isaea; Hemiptarsenus zilahisebessi; Chrysonotomyia sp.; Pnigalio sp.; Opius sp.; and Cirrospilus sp. (El-Serwy, 2003). No data is given on which of the parasitoids have emerged from L. cicerina.
In Romania, Banita et al. (1992) established the rate of parasitism of L. cicerina in chickpea crops, in Dolj district.
Cicer arietinum (Kabuli chickpea) grown on about 10 million ha, is the world’s third most important pulse crop (Rheenen, 1991). Kabuli chickpea is important not only as a source of human food, but is also a valuable fodder crop. In the Mediterranean region the chickpea leafminer, mainly L. cicerina, but also Phytomyza lathyri, is the main insect pest occurring in several countries in high densities every year (Weigand, 1990a). In the arid and semi-arid conditions of this region, L. cicerina is listed among the most stressing factors for chickpea growth together with Ascochyta blight (Ascochyta rabiei), and cold (Singh and Jana, 1993). In a report on the cultivation of chickpea in Spain (Govantes and Montanes, 1982), it is mentioned that L. cicerina is the most important pest of the culture. Del Canizo (1934) refers to fields of chickpeas in Spain in which virtually all plants show evidence of leaf-mining attack. The plants were not destroyed, but substantially weakened, with a consequent reduction of yield. Damage to the leaves actively facilitates subsequent fungal attack, referred to locally as “la rabia”, caused by Phyllosticta rabiei. Shevtchenko (1937) refers to the fungal disease in Ukraine as “Ascochyta”.
Some economic loss, both in the pea harvest and in foliage for fodder, undoubtedly occurs wherever this crop is cultivated (Del Canizo, 1934). It can be assumed that the mass outbreak that occurred in Ukraine in 1934 was exceptional, but nevertheless L. cicerina must be considered as a major pest, liable at any time when a significant build up of population occurs, to cause serious damage.
In a review of the insect pests of faba, lentils, and chickpea in North Africa and West Asia, Cardona (1983) listed L. cicerina and Heliothis spp. as the most important pests of chickpea in the field. In Turkey, in a study of the Agromizid fauna in Sanliurfa province, L. cicerina was found to be seriously damaging cultivated plants together with Liriomyza trifolii (Cikman and Uygun, 2003). In Syria, L. cicerina was found to be quite common in all the surveyed chickpea fields (Sithanantham and Reed, 1980) and Hariri and Tahhan (1983a) pointed out Heliothis armigera, Heliothis viriplaca and L. cicerina as the most economically important pests of chickpea. In another publication, the same authors (Hariri and Tahhan, 1983b) also added Callososbruchus chinensis in addition to these pests. A survey of the damage caused to chickpea in Syria and Jordan carried out in May 1983 (Sithanantham and Cardona, 1984) showed that the damaged caused by L. cicerina was greatest in Northern Syria. The damage caused by L. cicerina was estimated by Weigand (1990a) as serious, reaching up to 30% of seed yield loss.
The attacks of L. cicerina, although considered less serious than in spring, are strong enough to cause considerable losses in case of drought at the beginning of the cycle in the south part of Morocco (Kamel, 1990).
In India, the major pest problems in chickpea are the pod borer (Helicoverpa armigera and Helicoverpa punctigera), the leafminer L. cicerina, the cutworm Agrotis ipsilon, aphids (Aphis craccivora), semilooper (Autographa nigristigna) and bruchids (Callosobruchus spp.) (Sharma et al., 2007).
A study in Romania in 1986-1990 established that about two-thirds of the pest fauna in chickpea crops in the Dolj district comprised of L. cicerina (Banita et al., 1992). The attack was maximal during pod formation and the losses of the leaf mass reached 31-86%. In former Czechoslovakia, L. cicerina was first found in 1988 (Kolesik and Pasticha, 1992) in the region of Borovce and in the next 2 years large infestations were recorded.
There are also results showing no significant impact of L. cicerina on the yield. In Slovakia, Pastucha (1996) reported 41% mined leaves from the first generation of the fly and 85% from the second generation. Although quite high, the percentage of the mined leaves did not influence yield, but reduced seed weight. A study on the populations of L. cicerina on eight chickpea cultivars in Turkey in Sanliurfa province showed that there were very minor differences in yield among them, and there was no correlation found between larval density and yield loss (Cikman and Civelek, 2007).
A survey in three regions in Turkey (Yozgat, Konya and Eskisehir), showed that L. cicerina and thrips were the most widespread pests of chickpea, but were not economically important (Tamer et al., 1998).
The effect of planting date on chickpea leafminer infestation along with other items was studied in Aleppo, Syria (El-Bouhssini et al., 2008). Chickpea (Cicer arietinum) planted in Spring had a significantly higher number of damaged leaflets than the winter-sown crop. There were a significantly higher number of damaged leaflets on the local cultivar, as compared with an improved variety (Flip 82-150, ‘Ghab 3’) in both planting dates and both years. For the spring and winter cultivars, there were 1183 and 320 damaged leaflets, respectively, for the local cultivar and 968 and 244 for Ghab 3 in 1998; i.e. a nearly four-fold increase in the number of damaged leaflets between Winter and Spring planting. This study shows that chickpea leafminer could be effectively managed by integrating different pest management options such as winter sowing and use of tolerant cultivars.
El-Serwy (2003) is suggesting several agricultural practices i.e. deep ploughing and applying kerosene as control measures against pupae of the leafminer.
Higher irrigation levels caused increase of the population density of the leafminer, but on the other hand, yield was higher too (Cikman and Civelek, 2006). Based on the results, highest irrigation levels are recommended in the Sanhurfa province in Turkey.
Yellow, moistened traps were more effective in capturing adults than Tullgren funnels or net sweeps (Banita et al., 1992). El-Serwy (2003) tested the effect of spreading the harvested plants on plastic sheets to facilitate collection of the accumulated leafminer pupae.
In most seasons, the populations of L. cicerina are effectively controlled by its parasites. A braconid in Spain was found to parasitize up to 90% of larvae of the first generation of L. cicerina on chickpea, thus effectively reducing populations later in the year (Del Canizo, 1934). In more recent studies, again in Spain, Garrido et al. (1992) found the parasitoid Opius monilicornis and Tormos et al. (2008) found Dacnusa cicerina sp.n. Eurytoma sp. was reported as a possible hyperparasitoid of D. cicerina. In Morocco, O. monilicornis was identified (Lahmar and Zeouienne, 1990). The braconid parasitoids in general were described as the most important natural enemies of L. cicerina, parasitizing 20-35% of the first generation of the leafminer.
Hincal et al. (1996b) studied the rate of parasitism of L. cicerina larvae by O. monilicornis in chickpea fields in the region of Izmir, Denizil and Usak, Turkey in 1991-1994. They found that in May and June, parasitism in Izmir was 0-23.91%, 0-29.82% in Denizil and 0-28.33% in Usak. In a study of the parasitoids on Agromyzidae pests in cultivated and non-cultivated areas in Turkey, among which L. cicerina was included, a total of six parasitoids from Braconidae and 12 parasitoids from Eulophidae (Hymenoptera) were registered (Cikman and Uygun, 2003). Later, in the region of Sanhurfa, Turkey, Cikman et al. (2008) found a total of eight parasitoid species only on L. cicerina on chickpea. Leaves with mines were sampled weekly and kept in the laboratory to observe the emerging parasitoids. The braconids O. monilicornis and Opius tersus, and the eulophids Diaulinopsis arenaria and Neochrysocharis formosa occurred both during the Winter and the Summer seasons. Diglyphus crassinervis, Neochrysocharis ambitiosa, Neochrysocharis sericea and Pediobius metallicus occurred only in the Summer growing areas. D. arenaria was the predominant parasitoid with 4-7.7% parasitism rate whereas N. ambitiosa and O. monilicornis were the second and third most predominant species. The results of these trials show that because D. arenaria occurs throughout every season in Turkey, it could potentially be used for control of L. cicerina.
Several parasitoids are mentioned as present in faba bean fields at Damnhour, Sids and El-Zarka in Egypt on L. cicerina, Liriomyza bryoniaeand Liriomyza sativae: D. isaea; Hemiptarsenus zilahisebessi; Chrysonotomyia sp.; Pnigalio sp.; Opius sp.; and Cirrospilus sp. (El-Serwy, 2003). No data is given on which of the parasitoids have emerged from L. cicerina. Synchronization was found between the time of host emergence and the abundance of the larval parasitoid D. isaea in the active season, but not in the diapause season. Asynchrony was observed between the larval-pupal parasitoid Opius sp. and the leaf-mining flies. The population growth rates of larval parasitoids were lower than those of the flies, which retarded the biological control, particularly at the beginning of the season.
In Romania, Banita et al. (1992) established the rate of parasitism of L. cicerina in chickpea crops, in Dolj district, and according to the authors it was low; not exceeding 3-4%.
Application of insecticides inevitably reduces the population density of the parasitoids and hence, their efficacy. The population of the parasitoid O. monilicornis on L. cicerina on chickpea in Syria was significantly reduced by treatments with deltamethrin compared to treatments with neem oil or the control (El-Bouhssini et al., 2008). In their study, Cikman and Kaplan (2008) established that treatments with azadirachtin influence the rate of parasitism less than treatments with cyromazine. The rate of parasitism in the experimental plots was 35.08-31.64% and 16.98-18.18%, respectively.
The insecticidal efficacy of aqueous and methanol extracts from fruits of the Chinaberry tree, Melia azedarach was tested against the chickpea leafminer in Syria (Al-Housari et al., 2003). The results revealed that both extracts significantly reduced the mean percent of the leaflet damage and feeding punctures at all concentrations compared with the control. The highest concentration of methanol extract (2%) gave the highest reduction in percent leaflet damage. No phytotoxicity was observed on treated plants. The insecticidal effect of different seed extract levels (1, 2, 3 and 4 kg seeds/10 litres water) of the same plant (M. azedarach) on the larvae of L. cicerina was investigated at Usak and Denizil-Tavas, Turkey (Hincal et al., 2000). The larvae were counted on 25 damaged leaves in each plot. The seed extract level of 3 and 4 kg seed/10 litres water was effective against the larvae of L. cicerina for 15 days when both adults and larvae were present.
Cikman et al. (2008) investigated the effect of Bacillus thuringiensis on L. cicerina in the chickpea growing region of Sanlurfa, Turkey. B. thuringiensis was applied at a concentration of 60 x 106/mg B. thuringiensis spores. It was applied at the recommended rate of 75g/100 litres water. Application dates were chosen when the pest density reached a level of two to three larvae/leaf in 50% of the plants in the field, which is the economic threshold. The leaves were sampled weekly from treated (with cyromazine and B. thuringiensis) and control plots and kept in the laboratory under observation to compare the number of emerging leafminer adults and their parasitoids. Both cyromazine and B. thuringiensis reduce the number of the leafminer compared to the control. There was no difference between cyromazine and B. thuringiensis treated plots for average number of adults and larvae. The percentage of parasitism in the B. thuringiensis-treated plots was higher than in cyromazine-treated plots and was 37.70-35.08% and 15.79-13-33%, respectively.
A commercial neem insecticide was compared with cyromazine for its efficacy against L. cicerina (Cikman and Kaplan, 2008). Field trials were carried out from March to June 2006-2007 in chickpea-growing areas of Sanliurfa, Turkey. Azadirachtin was applied at a concentration of 1% (NeemAzl T/S 0.01% A.I.). For comparison, cyromazine 75% (Cyrogard 75 WP) was applied at the recommended rate of 20g/100 litres water. There was no difference between azadirachtin A and cyromazine treated plots for average yield.
In 1990 in Syria, a recommendation was given for application of Nuvacron or Thiodan at flowering (Weigand, 1990a). However, the use of insecticides may not be either practical or economical for the small farm holders in the region. In a study in 1986-1990, Banita et al. (1992) established that various chemicals applied at commencement of pod formation substantially reduced infestation of L. cicerina and increased yield, especially Trigard (cyromazine), Thiodan (endosulfan) and Fastac (alpha-cypermethrin).
El-Bouhssini et al. (2008) tested the efficacy of deltamethrin and neem oil against L. cicerina and their influence on the parasitoids. Both neem oil and deltamethrin significantly reduced leaflet damage in the two cultivars tested. However, deltamethrin significantly reduced the number of adult parasitoids compared with the unsprayed control and neem oil treated for the Spring-sown chickpea.
Although the breeding history of C. arietinum is short, considerable progress has been made in cultivar improvement (Rheenen, 1991). Breeding cultivars with resistance to freezing, Fusarium oxysporum f. sp. ciceris, Ascochyta rabiei and Helicoverpa armigera, and for short duration, are examples of successes. Yield stability has increased and yield gains of 1.6% per annum have been achieved. In the West Asia and Mediterranean regions, drought avoidance by Winter sowing has been achieved by incorporating disease resistance and changing the sowing date. This has resulted in a 75% yield increase. A 20% yield increase was recorded in Peninsular India because of the extra-short duration. Desirable traits include resistance to high temperature, salinity, Botrytis cinerea, Sclerotinium rolfsii, L. cicerina and stunt caused by bean leaf roll luteovirus. Attention should also be given to the problems of chilling and lodging in the most productive chickpea-growing areas. The possibility of applying new biotechnological methods for genetic improvement, particularly the use of interspecific crossing, micropropagation, somaclonal variation, and isoenzyme and RFLP mapping, are discussed.
The main approach for chickpea integrated control in Syria is screening for resistance to L. cicerina (Weigand, 1990b). In 1991, a catalogue of kabuli chickpea germplasm was published (Singh et al., 1991), presenting data on the evaluation of 6330 Winter-sown accessions of resistance to eight biotic and abiotic stresses (Ascochyta rabiei, Fusarium oxysporum f. sp. ciceris,L. cicerina, Callososbruchus chinensis,Heterodera ciceri, cold, herbicides and iron deficiency). Lists were provided of passport information (donor and origin) and evaluation data (24 descriptors) for each accession.
Two hundred accessions of wild Cicer species were evaluated for resistance to L. cicerina in Aleppo, Syria (Singh and Weigand, 1995). Accessions were screened under natural insect infestation in the field in March-June along with a susceptible control line (C. arietinum ICL482). Two accessions of Cicer cuneatum (ILWC40 and ILWC 187) and 10 accessions of Cicer judaicum (all ILWC lines) were rated as 2 on a scale of 1-9, where 1 = free from any damage and 9 = maximum damage. Another 18 lines of C. judaicum, four of Cicer pinnatifidum and one of Cicer reticulatum were rated as 3 (resistant). Three species were incompatible in crossing with chickpea, but C. reticulatum is being used in a breeding programme. Seeds from one leafminer (L. cicerina) resistant line (ILC5901) were exposed to 40, 50 and 60 kR (Omar and Singh, 1995). The M1 generation was sown at Tel Hadya, Syria during Winter. Germination was reduced at high dosages. Survival to maturity was drastically reduced especially after the 60 kR treatment. The percentage of sterile plants was highest at a dosage of 40 kR g rays. The parental lines and the M1 generation were grown in 1993. Of the 3292 progenies harvested from the M1, three were very early, six were early, 295 were medium and the remaining 2994 were late to very late in maturity. The six early plants were harvested individually; seeds from five of the six produced early maturing progeny. None of them segregated for maturity or any other observable character. All of these early mutants produced a higher seed yield than the parental lines and resistance to ascochyta blight or leafminer.
Singh et al. (1998) evaluated data on 228 accessions of eight annual wild Cicer species and 20 cultivated chickpea check lines for diversity in response to six of the most serious biotic and abiotic stresses that reduce crop yield and production stability of chickpea, i.e. ascochyta blight (A. rabiei), fusarium wilt (F. oxysporum f. s. ciceris), leafminer L. cicerina, bruchid C. chinensis, cyst nematode H. ciceri and cold. Relative frequencies of score reactions to the above six stresses were recorded from all the annual wild Cicer species and the cultivated taxon. Patterns of distribution and amount of variation of the resistance reactions differed between stresses and species. Cicer bijugum, Cicer pinnatifidum and Cicer echinospermum showed accessions with at least one source of resistance (1 to 4 score reactions) to each stress. Overall, C. bijugum showed the highest frequencies of the highest categories of resistance. Next in performance was C. pinnatifidum followed by C. judaicum, C. reticulatum and C. echinospermum. Furthermore, C. bijugum had the highest number of accessions with multiple resistance to the six stresses: two accessions were resistant to five stresses and 16 to four. According to Shannon-Weaver diversity indices (H’), five species showed discrete mean diversity indices that varied from 0.649 in C. pinnatifidum to 0.526 in C. judaicum, whereas Cicer chorassanicum, Cicer cuneatum and Cicer yamashitae showed the lowest H’ values, which were 0.119, 0.174 and 0.216, respectively. Pair-wise correlation among the six biotic and abiotic stresses showed the possibility of combining these resistances. Interestingly, multiple resistant accessions were predominantly of Turkish origin.
The International Center for Agricultural Research in the Dry Areas (ICARDA) screened 6025 germplasm lines of chickpea for resistance to L. cicerina (Singh and Weigand, 1996). ILC3800 and ILC7738 (PI58039 to PI587041, respectively) were consistently rated resistant (3 on a scale of 1 [free from insect damage] to 9 [severe mining on almost all leaflets]) and >30% defoliation for three seasons. ILC3800 and ILC7738 are introductions from Mexico and ILC5901 is from the former USSR. All three lines are of the kabuli type, have small, multipinnate leaves and have a medium plant height. ILC3800 is medium-maturing whereas the other two lines are late-maturing. These lines were released in 1994 for researchers in the Mediterranean region.
Several years later, Malhorta et al. (2007) reported about the registration of seven chickpea breeding lines developed by ICARDA that were resistant to chickpea leafminer: FLIP 2005-1C (Reg. No. GP-264, PI 645455); FLIP 2005-2C (Reg. No. GP-265, PI 645456); FLIP 2005-3C (Reg. No. GP-266, PI 645457); FLIP 2005-4C (Reg. No. GP-267, PI 645458); FLIP 2005-5I (Reg. No. GP-268, PI 645459); FLIP 2005-6I (Reg. No. GP-269, PI 645460); and FLIP 2006-7C (Reg. No. GP-270, PI 645461). They were released in 2006 for distribution to chickpea researchers for use in breeding programmes. These lines were developed from five crosses: ILC3805/ILC3379; ILC3805/ILC5309; ILC5901/ILC3397; ILC5901/ILC5309; and ILC3397/ILC5309. From the F2 to F5 generations, all evaluation was conducted for leafminer resistance following a pedigree method of selection. From the preliminary yield trial, seven of the best lines that possessed good agronomic background and seed quality and that were also relatively high yielders were selected and assigned Food Legume Improvement Program (FLIP) numbers.
Singh et al. (1997) registered the line ILWC39 as resistant to L. cicerina, cold and F. oxysporum f. sp. ciceris. It is prostrate in growth habitat, late maturing and low yielding.
The interrelation of semiochemicals and other factors for resistance to insects, mainly to Helicoverpa armigera and L. cicerina, is examined on the basis of their use as chemical markers for breeding strategies. Four volatiles (pentan – 1 –ol, D-3-carene, a-pinene and myrcene) were identified from the distance-perceivable signals as components of the chickpea kairomone (Rembold et al., 1989). Chickpea exudates for contact resistance had malate and oxalate as the main components present in variable absolute and relative concentrations, and there were characteristic differences depending on the variety, diurnal cycle and growth stage. Varieties with the highest amount of malic acid had the highest resistance to H. armigera and L. cicerina.
Along with the most important control methods in IPM systems in chickpea crops against diseases, Trapero-Casas (1999) mentions weed control and insecticide treatments to control L. cicerina and H. armigera. According to El-Bouhssini et al. (2008), L. cicerina could be effectively managed by integrating different pest management options such as winter sowing and the use of tolerant cultivars. Pimbert (1990) suggested the use of maps showing the severity and extent of pest damage (including caused by L. cicerina) to determine integrated pest management research priorities for different agro-ecological zones in India. El-Bouhssini et al. (2000) give a brief outline of an integrated pest management package developed in West Asia and North Africa using plant resistance, planting dates and botanical insecticides to control L. cicerina with minimum effect of the natural enemies of the pest, with particular reference to neem oil.
Monitoring and Surveillance
Methods for sampling populations of L. cicerina were investigated in chickpea crops in Syria between 1980 and 1982. Sweep net catches of adults were influenced by adult activity, which varied diurnally and seasonally according to the weather (Sithanantham et al., 1985). More adults were caught on vertical blue boards coated with Tanglefoot glue than on those orientated horizontally or of a different colour. Sugar solutions, molasses, vinegar, yeast and protein hydrolysate were tested as possible adult attractants in sticky traps, but none was found to be effective. Sticky sheets placed underneath individual plants were found to trap larvae that fell to the ground to pupate.