OROBANCHE ( OROBANCHE SPP.) IN LENTIL ( LENS CULINARIS MEDIC.): HOW HUGE ARE THE LOSSES OF YIELD, QUALITY, MARKETING PRICES AND PROFITABILITY?

: This research aimed to inspect the impacts of severe parasitic plants ( Orobache spp . ) on grain yield, some quality characteristics, marketing price and profitability loss of red lentil in the major lentil growing area of south-east Anatolia. Farmer field trials were carried out in two neighbouring fields planted with Yerli K ırmızı (landrace) and Firat -87 varieties of lentil employing a split-plot experimental design in the Yollar basi location of Viransehir in the 2018–2019 crop growing season. Lentil varieties were placed into main plots and the broomrape infestations (i.e. 0, 5, 10, and 15 plants m -2 ) in the subplots respectively. Grain yield, hectolitre weights and 1000-kernel weights and protein contents (%) were scored. All grain samples were presented to randomly chosen grain purchasers in the local commodity market and marketing price offers were scored respectively. Results showed that broomrape infestation from zero to 15 broomrapes m -2 reduced the grain yield significantly from 2033.33 kg ha -1 to 833.33 kg ha -1 by 59%. Although being non-significant, Firat-87 (1512, 5 kg ha -1 ) was found to be higher yielding than Yerli Kırmızı concluded that an infestation over 15% might result in a disastrous yield loss in lentil production. Therefore, some agronomic measures must be taken quickly.


Introduction
Lentil (Lens curinalis Medic.) is an important food legume crop used both as food and feed due to its protein-rich grain and straw. Worldwide, lentil is cultivated on 3.85 million hectares (m ha) with 3.59 million tons (mt) production under rain fed conditions (Erskine et al., 2011).
Lentil is also a nutritious food legume. The seed has a relatively high content of protein (22%), carbohydrates and calories (3250 kcal kg -1 ) including fast cooking characteristics (Muehlbauer, 1985;Saskatchewan Agriculture and Food, 2005). Lentil (Lens culinaris Medic.) is a cool-season annual cash crop, classified as a grain legume or pulse in south-east Anatolia (Ozberk et al., 2006).
Turkey is one of the major lentil producer ranking third globally after Canada and India with 410000 tons of annual production on 214,788 ha (TUİK, 2014). Green lentil is grown in the central and transitional zones of Turkey while red lentil is grown in the south-east of Anatolia (Ozberk et al., 2006).
By far, the most economically damaging root parasitic weeds in Europe and neighboring regions are members of the Orobachaceae, mainly species belonging to the genera Orobanche and Phelipanche (broomrapes) (Joel et al., 2007a;Parker, 2009). In Turkey, 36 species of Orobanche have been recorded (Gilli, 1987). However, only four of them have resulted in considerable damage to crops. Phelipanche ramosa (L) Pomel (syn. O. ramosa L.) Phelipanche aegyptiaca (Pers) Pomel (syn. O. aegyptiaca Pers.) (Joel et al., 2007;Parker, 2009) and O. crenata Forsks also result in damage in lentil (Kıtıkı et al., 1993;Uludag and Demir, 1997;Aksoy and Uygur, 2003;Bulbul and Uygur, 2009). In a survey carried out in neighbouring Diyarbakir province, it was found that the most abundant broomrape species infesting lentil plants were: Orobanche crenata Forsk., and Phelipanche aegyptiaca (Pers.) Pomel (syn. Orobanche aegyptiaca Pers.). The frequency of the occurrence of broomrape species ranged between 12% and 41% (Ozaslan et al., 2017). In legumes, the most intensive growth of Orobanche usually coincides with the flower and pot stages of the host. Broomrapes spend most of their life cycle underground, where they undergo processes of germination, haustorial differentiation from the radicle, haustorial penetration of the host formation of vascular connection with the host, utilization of host nutrients and the storage of resources in a parasite organ called the tubercle or nodule (Fernandez- Aparicio et al., 2011). This results in flower dropping and low amount of pod formation due to an increase in competition receiving more plant nutrients. The wilting symptoms occur due to the reduced water uptake because of a deficiency of energy in the host roots, as a result of the flow of carbon hydrates to the parasite (Anonymous, 1997).
Yield losses due to Orobanche ranged from 5 to 100% (Aksoy et al., 2016;Erskine et al., 2011;Bulbul et al., 2009; Australian Department of Agriculture and Food, 1999;Anonymous, 1997). An economical loss of lentil of about 60 million euros is estimated annually (Uludağ and Demirci, 2005;Bulbul et al., 2009). Only in the Middle East, it could reach about 1.3 and 2.6 billion dollars (Aly, 2007). Several strategies have been developed for the control of broomrape, ranging from cultural practices to chemical control (Habimana et al., 2014;Joel et al., 2007b;Parker and Riches, 1993), but none with unequivocal success. Good broomrape control can be achieved in faba bean by glyphosate at low rates. However, insufficient selectivity was found in lentil (Arjona-Berral et al., 1988). Lentil tolerates pre-and post-emergence treatment of other herbicides suitable for broomrape control, such as imazapic and imazetgapyr (Jurada-Exposito et al., 1997). Imazapic (10gl -1 ) is widely used in SE Anatolia. Phytotoxicity has been observed at higher doses of some herbicides and depends on the level of water stress and lentil cultivar (Henson and Hill, 2001). A number of cultural practices including solarisation, delay sowing, hand weeding, no-tillage, nitrogen fertilization, intercropping, rotations can contribute to seed bank demise. Other strategies such as trap plants, suicidal germination, and activation of systematic acquired resistance, biocontrol or target site herbicide resistance are promising solutions that are being explored but none of them is the sole solution of the problem (Habimana et al., 2014). The only methods currently available for farmers are the use of resistant varieties and chemical control (Rubiales and Fernadez-Aparicio, 2011). Resistance breeding is hampered by the scarcity of proper sources of resistance and of a reliable and practical screening procedure (Fernandez- Aparicio et al., 2007b).
This study aimed to assess the effect of broomrape damage on grain yield, some quality characteristics, marketing price of lentil in the local commodity markets and finally the loss of net income.

Materials and Methods
This study was carried out in the farmer fields in Viransehir location in S. Urfa in the 2018-2019 growing season, wherein broomrape infestations are common. O. crenata Forsk. (white flowering), P. ramosa (pale blue flowering and branched) and P. aegyptica Pers. (blue flowering) were found to be wide-spreading in lentil fields (75,51%) in the Eastern Mediterranean region and Southeastern Anatolia (Bulbul et al., 2009;Temel et al., 2012). O. aegyptica Pers. was prevalent in the Viranşehir region (Uludağ and Demir, 1997;Bayaa et al., 1998).
A preceding crop was wheat in Viransehir. Disharrow + float + drill planting + roller combination was employed for planting management. Two farmer fields with 10 ha each in Viranşehir were planted by a drill with a 120 kg ha -1 seed rate in both fields on the 30 th of October in 2018. A 50 kg ha -1 di ammonium phosphate rate (DAP, 18 and 46% of N and P) was applied at sowing. Annual rainfall was quite satisfactory with 712.6 mm and its distribution throughout the cropping season was also well-balanced. All other necessary agronomical measures were taken for healthy crop production. Chemical weed control for narrow-leaf weeds was employed. However, pest control was not applied. A field trial was carried out under moderate volunteering broomrape infestation. Field plots were assigned at the flowering stage of broomrape and the early pod stage of lentil. One m 2 plots with 0, 5, 10 and 15 broomrape plants surrounded by the strip at the corners built up a block. Three blocks for each cultivar were assigned as shown above (Picture 1). Picture 1. Orobanche plants at flowering and plots surrounded by strips.
A split-plot experimental design was employed. Lentil varieties were placed into main plots and the broomrape infestations (i.e. 0, 5, 10, and 15 plants m -2 ) in the subplots respectively (Table 1).
Subplots were randomly selected taking into account the number of flowering broomrape plants placed in the one m 2 acreage. Numbers of broomrape flowers were counted in each plot at the flowering and pod filling stages of lentil and the assignment of plots was performed. Plots were harvested by hand and threshed by a single plant thresher for weighting grain yield on the 30 th of May in 2019. The highest yield loss for both cultivars was calculated as: HYL% = [1-(mean grain yield of plots with 15 broomrapes/mean grain yield of zero broomrapes)] x 100. Hectolitre and 1000-kernel weights and protein (%) content of lentil grains were also scored through the methods given by Williams et al. (1986).
Seed samples of the experiment with an increasing amount of broomrape damage were presented to randomly chosen 3 grain purchasers in the local commodity market in mid-June in 2019. ANOVA and mean separation were performed for marketing price estimates employing a split-split-plot experimental design with 3 replications. Purchasers, varieties and infestation ratios were placed into main plots, subplots and sub-subplots respectively. Coefficients of correlation among such characteristics were estimated. Regression relations between grain yield, hectolitre weight and 1000-kernel weights vs. broomrape infestations were further investigated (Finlay and Wilkinson, 1963;Eberhard and Russel, 1966). The economic loss (US$ ha -1 ) was calculated as: EL = HYL (%) x mean grain yield of non-damaged grains x mean marketing price of non-damaged grains.
The JMP statistical software was employed for statistical analysis and figures.

Results and Discussion
O. aegyptica Pers. (blue flowering) and O. ramosa (pale blue flowering and branched) were dominating species with a little amount of O. crenata Forsk (white flowering) in Viranşehir in 2018-2019. The sowing time was earlier than that of a common practice. The adopted practice is to plant lentil in late October or early December. The grain yields of lentil crop under various broomrape infestations are given in Table 2.
The analysis of variance (not given here) for grain yield indicated that there were significant differences between broomrape infestation ratios (F=232.27**) and infestation ratios x varieties interaction (F=5.30*), but no difference was found between cultivars (F=17.30, p>0.0532). Table 3 shows the mean differences of significant variables through LSD.
Although being non-significant, Firat-87 seemed to be higher yielding than Yerli Kırmızı. Increasing infestation ratios reduced grain yield significantly. Plots free from broomrape gave the high yield (2033.33 kg ha -1 ), whereas the plots with 15 broomrape plants reduced grain yield to 833.33 kg ha -1 dramatically.   -(833.33 /2033.33)] x 100 = 59%. Grain yield loss seems to be dramatic due to the increasing amount of broomrape infestation.
ANOVA for 1000-kernel weights (not given here) indicated the absence of any significant source of variation. Although being non-significant, there was a slight difference between varietal means in favour of Firat-87. Although being nonsignificant, there were some differences among the means of 1000 KW depending upon infestation ratios in favour of less infestation. ANOVA for hectolitre weights showed that there was not any significant source of variation. Although being nonsignificant, the mean of Firat-87 seemed to be slightly higher than that of Yerli Kırmızı. Although being non-significant, increasing infestation ratios reduced the hectolitre weights slightly. The negative influence of broomrape infestation on lentil quality was discussed by the Australian Department of Agriculture and Food (1999). However, broomrape infestation in our study did not affect any quality characteristics.
The economical loss (EL) for the experiment was approximately = 0.59x 2.033 ton ha -1 x US$ 462.06 ton -1 = US$ 554.22ha -1 Relatively early planting of lentil suffered from broomrape severely (Temel et al., 2012). Volunteering broomrape plants developed very fast and attacked young lentil seedlings. When lentil is planted late into humid soil, plants can escape from severe broomrape attacks and late planting of early maturing type of lentil was recommended by Temel et al. (2012). There were some statistically significant differences among the varieties showing a response to broomrape infestation. Fırat-87 was found to be high-yielding. Yerli Kırmızı (Landrace) was the yield-limiting variety among entries. Late planting of Altın Toprak-98 was recommended for the farmers in the region because of its high-yielding performance and early maturing ability (Temel et al., 2012). Broomrape infestation can reduce grain yield severely as pointed out (Anonymous, 1997). Fifteen broomrapes m -2 reduced grain yield by 59% compared to non-damaged plots. Grain yield reduction was 51.5% in a study carried out in the same region by Ozberk et al. (2016). Regression between grain yield vs. broomrape infestations for both varieties turned out to be significant giving F=74.78** and 76.45** respectively. Regression equations with high coefficients of determinations can be used for yield estimates under various broomrape infestations. Both 1000-kernel weights and hectolitre weights seemed to be slightly decreasing depending on the increasing broomrape infestations as indicated (Ozberk et al., 2016) earlier.
Analysis of variance for marketing price offers indicated that broomrape infestation and replications (purchasers) were found to be non-significant. The presence of broomrapes until 15 per m 2 did not affect negatively on some quality traits and marketing prices. Another study carried out in the same region indicated the absence of any marketing price differences among the grains suffering from the various amounts of broomrape infestation (Ozberk et al., 2016).
Broomrape infestation did not affect any visual quality characteristics such as 1000-kernel weights and hectolitre weight as obtained by Ozberk et al. (2016). Comparing the grain yields of the highest broomrape infested plots versus those of non-damaged plots, the losses showed the importance of broomrape management in the red lentil growing belt of the country. The economic loss was about US$555 ha -1 . Confirming our findings, this was also huge (US$ 396.77 ha -1 ) under 8-9 broomrape m -2 infestations in a similar region (Ozberk et al., 2016). Breeding resistance is the most economic, feasible and environmentally friendly method of control. However, resistance to broomrape is difficult to access due to the scarcity of complex nature and low heritability. Breeding for resistance is a difficult task (Rubiales, 2003). So far, no source of resistance has been available in lentil (Muehlbauer et al., 2006). Nevertheless, Fernandez- Aparicio et al. (2008) have observed a wide range of responses to crenate broomrape resistance under field conditions. Low infection rates seemed to be based on a combination of various escape and resistance mechanisms. Moreover, some in-vitro screening techniques may be used to rank and identify lentil accessions with potential broomrape resistance. There are numbers of cultural practices including delayed sowing, hand weeding, no-tillage, nitrogen fertilization, intercropping, and trap plants such as Brussels sprout, cabbage, broccoli, canola, turnip and crop rotations to contribute to seed bank demise. Taking into account simplicity in application, planting time modifications can be employed as agronomical measures. However, there is a conflict between early planting and late planting. Late planting of early-maturing types of lentil are recommended (Temel et al., 2012;Rubiales and Fernandez-Aparicio, 2011), whereas farmer practice in the region is to plant lentil relatively early for the emergence and rapid vigorous seedling development. Therefore, plant can compete with broomrape development as partially suggested by Silim et al. (1999). Crop rotation, solarisations and the use of the trap plant formerly used to be planted in large scale in the region such as Linum usitatissimum L. are other possible measures (Aksoy and Uygur, 2003). An increase in farmer awareness was also recommended urgently (Ozaslan et al., 2017).

Conclusion
It was concluded that 15% of broomrape infestation resulted in early 60% yield loss with the US$ 555 ha -1 economic loss. It is predicted that 20% or slightly more of broomrape infestation might result in a disaster giving the zero amount of grain at harvest. Thus, immediate agronomical measures given above must be taken in the region and neighboring countries.