Field dodder - How to control it?

Broad geographic distribution and spectrum of hosts make field dodder, 
 Cuscuta campestris, one of the most widespread and most harmful pests among 
 flowering parasitic plants. Field dodder may become a problem in vegetable 
 nurseries (e.g. tomato, sweet pepper and cabbage) or in potato or some other 
 crop grown in plastic greenhouses. However, the most devastating damage comes 
 from field dodder outbreaks in newly-established perennial legume crops 
 (alfalfa, clover, etc.), which are generally the preferred hosts of this 
 parasitic flowering species. Apart from alfalfa and clover, an expansion of 
 field dodder has been observed in recent years in sugar beet, too. Different 
 measures are available for controlling field dodder, from preventive (pure 
 seeding material, tolerant cultivars, etc.), to mechanical removal (mowing 
 and hand weeding) to herbicide treatments. The most successful control of 
 field dodder requires a systematic approach ensured through integrated 
 protection, which contributes to a more effective control of parasitic 
 flowering plants.


INTROdUCTION
Autotrophic f lowering plants constitute the predominant group among weed species but weeds also include some semiparasitic and parasitic flowering plants. Parasitic plants are represented by approximately 4200 species classified in 274 genera, which make a little more than 1% of all flowering plants. Only some 11% of all genera include species that may be considered as parasites of cultivated plants. The worst economic damage in important host crops is caused by species from only four genera: Cuscuta, Arceuthobium, Orobanche and Striga (Nickrent, 2002).
Cuscuta campestris is considered the most widespread Cuscuta species globally. Even though North America is assumed to be its place of origin, the species is cosmopolitan and considerably widespread throughout South America, Europe, Asia, Africa and Australia (Holm et al., 1997). Distribution and frequency of Cuscuta species in anthropogenic habitats in Serbia (i.e. various types of crops and ruderal habitats in urban and rural areas) have been researched by Vrbničanin et al. (2008), and they detected their presence in 25% of the assessed 10x10 km squares on the UTM (Universal Transverse Merkator) grid.
Most of the damage caused by these parasitic flowering plants results from the fact that parasitism is the most acute form of negative interaction between vascular plants in which one of the partners becomes a heterotroph living at the expense of the other, its host.
Plants infested with field dodder gradually weaken, their lush growth dwindles and they have very small vegetative and generative yield (Koskela et al., 2001;Fathoulla & Duhoky, 2008). Damage caused this way may eventually cause total destruction of the host plant. We are therefore focusing in this review on various control options for field dodder, from preventive ones (e.g. mechanical measures or choice of tolerant cultivars) to biological and chemical methods of control.

BIOLOGICAL CHARACTERS OF FIELd dOddER
The genus Cuscuta includes some 200 annual and sporadically perennial non-herbaceous plants that have no roots and parasitize on host stalks. The stem of a field dodder plant is threadlike and twining, it has no leaves or they may only appear as inconspicuous scales. After field dodder seeds have fully matured they fall off and accumulate on the ground. They may germinate during the following season if a suitable host plant is growing nearby or may stay dormant until such conditions have occurred (Swift, 1996). When a seedling touches the stalk or trunk of a host plant it becomes firmly attached to it and twines around it by forming thick growths known as appressoria. Sharp pointed haustoria develop from appressoria that enable the parasite to draw organic and mineral matter from its host. The ability to form specialized organs for absorption, i.e. haustoria, is the chief adaptive character of all higher parasitic plants (Hibberd & Jeschke, 2001). Obligate parasites are unable to develop without assimilates drawn from their host plants because they are either unable to perform photosynthesis (Kujit, 1969;Losner-Goshen et al., 1998) or their photosynthetic capacility is very small (Hibberd & Jeschke, 2001). Even though dodder plants possess a functional photosynthetic apparatus within a ring of cells surrounding vascular tissue (Hibberd & Jeschke, 2001) the amount of organic matter produced there is too small to provide for the plant, so that 99% of the required carbon is still drawn from the host (Jeschke et al., 1994). Holoparasites are believed to use primarily products conducted through the phloem but their haustoria reach into the xylem too for nutrients such as calcium, which is deficient in the phloem. However, field dodder has been reported to get not only organic matter from its host through the phloem but minerals too, such as nitrogen, magnesium and calcium, although they are to be found in greater amounts in the xylem than in the phloem (Hibberd & Jeschke, 2001). Field dodder parasitism interferes with the balance of contents of nitrogen, phosphorus, potassium, organic and inorganic matter in the host plant (e.g. alfalfa or sugar beet) (Sarić-Krsmanović et al., 2013a). It exhausts the host plant, so that it becomes weak, its lushness of growth declines, and fruit and seed maturation become significantly thwarted (Wolswinkel, 1974). Also, host plants change their habit as their axillary buds sometimes become suppressed (Tsivion, 1981), and damage may expand into total plant destruction. Significant changes can be detected in plant morphology and anatomy, so that field dodders cause changes in stalk anatomy (epidermis, cortex, pith or diameter) and leaves (upper epidermis, palisade tissue, spongy tissue, leaf mesophyll, underside epidermis or vascular bundle cells) of host plants Matković et al., 2012). At an appropriate moment during maturation, field dodder plants form inflorescences with abounding hermaphrodite and actinomorphic flowers. The seeds of this parasitic flowering plant germinate on soil surface from May throughout June. Field dodder is a thermophylic species and its optimal temperature for germination is 30˚C (Sarić-Krsmanović et al., 2013b). Its seeds retain vitality in soil over 10 years or more. A single plant is able to form up to 15.000 seeds, and their abundance constitutes the main mode of survival of that parasite in the environment (Benvenuti et al., 2005). Its reproduction may also be vegetative through segmentation of its treadlike stem. Such reproduction mode is frequent in alfalfa and clover crops after harvests and haying, and transfer from infested plots to noninfested fields (Babović, 2003).

dAMAGE CAUSEd BY FIELd dOddER
Apart from an immediate damage caused by reducing the biological yields of plants parasitized by field dodder, indirect forms of damage are also frequently considered: (1) livestock fed on hay (fresh biomass of legumes, primarily alfalfa and clover) containing 50-60% field dodder lose weight, (2) miscarriages are more frequent, (3) indigestion occurs, (4) dodder consumption in bulk feed causes diarrhea, vomiting, palpitation and heavy breathing in rabbits and horses (Movsesyan & Azaryan, 1974), (5) some Cuscuta species carry viruses, thus causing additional difficulties for crop growing and indirectly reducing yields. Besides its role of a vector of diseases, it may also itself be the host of viruses, such as the cucumber mosaic virus or tobacco rattle virus (Marcone et al., 1999).
Its widespread geographic distribution and a wide range of hosts make field dodder one of the most widespread and damaging flowering parasites (Parker & Riches, 1993). Problems with field dodder occur in vegetable nurseries (e.g. tomato, pepper, cabbage) and in greenhouses. Field dodder has also been recognized as a growing problem in sugar beet crops over the past few years (Sarić-Krsmanović & Dobriković, 2012). Lanini (2004) reported an up to 75% yield reduction from tomato infested with field dodder. Several other studies have shown that field dodder is able to reduce carrot yield from 70 to 90% (Bewick et al., 1988). It also causes considerable problems in onion (Allium cepa) crops as its control is difficult because there are no available herbicides with adequate selectivity to protect that crop (Rubin, 1990). Damage is primarily caused through increased volumes of unmarketable bulbs and roots (i.e. their size, form and weight). Cranberry infested with Cuscuta gronovii is known to sustain up to 50% yield loss (Bewick et al., 1988).
Field dodder is able to cause the most intensive damage in newly-formed perennial legume (alfalfa or clover) crops, which are the most frequent targets of dodder parasitism (Dawson et al., 1994). Damage done in these crops consists mainly of reduced fresh biomass yield, which may be upwards of 50%, and significantly reduced seed production by seed alfalfa (Cudney et al., 1992). Dawson (1989) reported a yield loss of 57% in an alfalfa crop artificially infested with C. campestris in Prosser, Washington (USA) over a period of two years. Two years later, potato was sawn in the same location and the crop was totally destroyed by field dodder (Dawson et al., 1994). Mishra (2009) reported some 60% yield reduction in alfalfa infested with C. campestris. Some other legumes, e.g. beans, have shown different levels of sensitivity to dodder parasitism. Bean crops have demonstrated tolerance of the presence of Cuscuta chinesis (Rao & Reddy, 1987), while being sensitive to C. lupuliformis (Liu et al., 1991). Conversely, Cuscuta chinesis has been reported to cause considerable damage to soybean (Li, 1987). Stojanović and Mijatović (1973) reported a yield reduction of around 80% in alfalfa infested with C. campestris, and some 20% in red clover. Furthermore, Stojšin et al. (1992) recorded major losses in sugar beet crops in Serbia, estimating them at around 40%, while sugar content decreased between 1.3 and 2.6%. In Khirghistan, C. campestris has been reported to cause a significant reduction in sugar beet yield, around 4 t/ha, and sugar content to 1.5-1.9% (Belyaeva et al., 1978). Serious problems have also been reported in sugar beet crops in Slovakia, where an average yield loss of some 37% was reported in the 2002-2004 period, while sugar content reduction was around 12% (Tóth et al., 2006).
Ornamentals make another group of frequent hosts of this parasitic flowering plant, which rarely destroys them totally but the weakness caused by parasitism creates threats from other harmful organisms, primarily insects and various pathogens. Significant damage has been reported lately on Capsicum frutescens (hot pepper) in Pakistan, where the crop has high economic value because it is used both for diet and medical purposes (Mukhtar et al., 2011).

CONTROL OPTIONS
Based on the importance of field dodder and damage that it is able to cause, it has been categorized as a quarantine plant parasite in many countries, and in Serbia too (IA List, 2010), making its suppression mandatory throughout the country. Attention should primarily focus on field crops. Control of field dodder should commence as soon as initial points of infestation have been observed, and completed before dodder plants begin to flower and set seeds. Once its seeds have fallen on the ground the species becomes a permanent threat to crops. Various options for control of field dodder are available, beginning with preventive steps (by using pure seeding material or tolerant cultivars), to physical removal (by mowing or hand weeding) to herbicide treatements.

PREVENTIVE CONTROL OF FIELd dOddER
Preventive control is one of the most important and fundamental activities in any field dodder control strategy, which focuses primarily on prevention of plot infestation by: (1) cleaning all nearby plots; (2) cleaning field margins; (3) cleaning waste grounds; (4) destroying weeds parasitized by field dodder; (5) maintaining irrigation canals dodder-free; (6) spreading rotted manure; (7) hand weeding dodder plants in small areas, taking good care of the removed plants because dodder seedlings are able to survive only a few days without a host, while fully developed plants removed with their hosts are able to retain freshness up to a couple of weeks; (8) checking on potentially infestable crops at 15 days intervals to detect infestation in an early stage and take adequate control measures; (9) longterm crop rotation; once the presence of field dodder seeds in soil has been detected, such plots should not be used for cultivation of known dodder hosts for a minimum of 4-5 years. Crop rotation is an important preventive measure even though it may be difficult to find an adequate replacement for some crops and so avoid dodder parasitism in that new crop (Parker, 1991). Cereals are considered suitable rotation crops as they have not been observed to host Cuscuta species (Dawson, 1987;Dawson et al., 1994).
Postponement of sawing or replanting is also considered an important preventive measure. Lanini (2004) found that later replanting of older tomato plantlets made it difficult for dodder plants to attach to them because stalk tissue of such plants had already lignified. However, this measure is often considered a poor choice because it delays yield. Also, early crop sowing in combination with irrigation enables faster development of the cultivated plants, while field dodders will not germinate at low temperatures. Fast crop growth and its greater density make dodder germination more difficult because it requires high temperatures, as well as good irradiation (Dawson et al., 1994).
Differences in the tolerance of host plants to various Cuscuta species have been reported but they have not been studied in detail. Al-Menoufi and Ashton, (1991) detected different levels of tolerance of four wild Lycopersicon species to C. pentagona. Similar data were collected by Löffler et al. (1995) in a study of relationships between Cuscuta reflexa and as many as 30 varieties of tomato, which showed their significant level of tolerance to the parasite. The examined tomato cultivars were found to undergo changes in epidermis, hypodermis and collenchyma, forming necrotic tissue around points of haustoria penetration and thus preventing its further progress. Ihl and Miersch (1996) observed a similar level of tolerance of 22 tomato cultivars to four Cuscuta species: C. reflexa, C. japonica, C. odorata and C. europaea. All those tomato cultivars reacted with hypersensitiveness of epidermal cells on their stalks and tissue necrotization, which stopped haustoria penetration. Necrosis of the upper cell layer was accompanied by increased peroxidase activity, which was a further obstacle to haustoria penetration into the conducting tissue of the host. However, different levels of tolerance of some tomato cultivars greatly depend on the virulence of different Cuscuta populations. Goldwasser et al. (2001) and Lanini (2004) confirmed different tolerance levels of 33 commercial tomato cultivars to a highly virulent population of C. pentagona. So far, six commercial tomato cultivars (Heinz 9492, Heinz 9553, Heinz 9992, Heinz 9888, Heinz 1100 and Campbells CXD 233) have been confirmed tolerant to several species of the genus Cuscuta. Some of the species manage to survive on their tomato hosts without causing them significant damage. The cultivars had been created to be primarily tolerant to bacterial cancer (Clavibacter michiganensis subs. michiganesis), which may have also created their tolerance to field dodder (Goldwasser et al., 2001;Lanini, 2004). Parker (1991) tried to use certain phytopathogenic fungi, bacteria and insects for biological control of several Cuscuta species. Bewick et al. (1987) found several phytopathogenic fungi, including Fusarium tricinctum and Alternaria spp., to cause some damage to C. gronovii, while A. alternata and Geotrichum candidum were harmful to C. pentagona. Besides, Li (1987) reported that a conidial suspension of Colletotrichum gloeosporioides could be used for selective control of the species C. chinensis and C. australis in soybean crops. Bewick et al., (2000) used Alternaria destruens to control C. gronovii in fields of cranberry (Vaccinium macrocarpon) and carrot (Daucus carota), and reduced it up to 90%. However, the results of similar efforts to control C. pentagona in the same crops were not nearly as successful in the warm and dry climate of California (Lanini, 2004). Božić (2009) and

CHEMICAL CONTROL OF FIELd dOddER
As a result of haustoria penetration and the formation of a closed host-parasite association it is believed that only strongly selective herbicides are effective enough in destroying the parasite without hurting the host (Fer, 1984). Studies have mostly been focused on chemical methods of field dodder control (Dawson, 1984(Dawson, , 1987Parker, 1991;Parker & Riches, 1993). Some researchers have reported better results of herbicide treatments before the parasite has attached to its hosts (Cudney et al., 1992;Dawson, 1990a;Orloff & Cudney, 1987). Herbicide treatments prior to dodder attachment are conducted to avoid such attachment and so prevent even the least damage (Parker, 1991). Dinitroaniline herbicides have been used for preventive control of field dodder in alfalfa crops (Orloff & Cudney, 1987). Pendimethalin, one of such herbicides, has been found far more effective than trifluralin because its effect is more durable. But trifluralin may also be used as a selective herbicide for control of C. indecora and C. pentagona in alfalfa crops. It is used in granular formulation that stays close to soil surface in which dodder seeds are expected to germinate. Liquid formulation of trifluralin has not produced such good results in controlling these species in tomato. Pendimenthalin may also be used for selective control of field dodder in carrot, onion and alfalfa (Orloff & Cudney, 1987). Pendimenthalin is less transportable than trifluralin but rainfall and irrigation certainly facilitate its faster incorporation and activity in soil (Parker & Riches, 1993). Foschi and Rapparini (1977) used ethofumesate to control field dodder in sugar beet. As the selection of herbicides available for control of field dodder in sugar beet is very restricted, soil herbicides are often used, but practice has revealed their rather poor effects on field dodder. Conversely, propyzamide has been identified as a sound solution for field dodder control in sugar beet, depending on infestation intensity (Sarić-Krsmanović & Dobriković, 2012). Orloff and Cudney (1987) conducted similar research and both studies showed rather weak effects of that herbicide. The low water potential of field dodder is assumed to restrict movement of herbicides through the xylem, which is another reason why soil herbicides are less effective against this parasitic plant (Fer, 1984). Fer (1984) found that xylem-conducted compounds move and become accumulated mostly in organs of the host plants with higher water potential (transpiration) and may so harm the host plant more than the parasite. Liu and Fer (1990) found that the weakly transportable pendimenthalin herbicide applied in beans was not moving fast enough along transpiration pathway to control field dodder plants, while its foliar application resulted in its nearly 60%accumulation in parasite tissue.
Treatments with post-emergence herbicides, which are translocated through the host phloem, enable their selective uptake by dodder plants owing to the parasite's ability to draw nourishment from the host phloem by transfers of solutions that occur as a result of different water potentials of cell sap in the host and the parasite (Fer, 1984;Nir et al., 1996;Shlevin & Golan, 1982). Herbicides conducted through the phloem should selectively accumulate in the parasite plant because of its stronger uptake (Nir et al., 1996). Liu and Fer (1990) reported that foliar application of glyphosate led to its 26-fold higher accumulation in the apical part of field dodder plants than in the root and young leaves of their hosts. Bewick et al. (1991) used 14 C-labelled glyphosate in carrot infested with C. pentagona and found that significantly greater amounts were accumulated in the parasite tissue than in any part of the host plant. Dawson (1990b) reported similar good results after applying glyphosate in alfalfa, and Mishra et al. (2004) after treatment of black gram [Vigna mungo (L.) Hepper]. Besides, glyphosate has been found effective in controlling Cuscuta monogyna Vahl. on the woody species Punica granatum L. (Bewick et al., 1988). Sarić-Krsmanović et al. (2015) found that glyphosate applied at the rates of 288 and 360 g a.i. ha significantly reduced field dodder in alfalfa crop. Shawn et al. (2008) conducted a two-year study in which all application rates (140-1,120 g a.i. ha) had high effectiveness of >84% in controlling field dodder on ornamental plants. In some other crops, however, even low amounts of glyphosate are able to harm the host (Orloff & Cudney, 1987), which prevents adequate control of the parasite (Frolisek, 1987).
Several herbicides classified as ALS inhibitors have proved themselves effective in controlling field dodder. Post-emergence treatment with imazethapyr is able to reduce significantly the number of dodder seedlings in alfalfa (Cudney & Lanini, 2000). Rimsulfuron applied in tomato crops also controls field dodder (Mullen et al., 1998). Furthermore, imazethapyr treatment in an infested carrot crop has been found to cause less damage than its application in non-infested crop, which again points at the potentials of exploiting the low translocation rates of non-selective herbicides for selective control of parasite weeds (Nir et al., 1996). However, Sarić-Krsmanović et al. (2015) found imazethapyr to have a weak effect on field dodder heavily infesting alfalfa as 78-95% of dodder plants remained after treatment (imazethapyr, 150 g a.i. ha).
The fact that carotenoid pigment lends field dodder stalks their orange colour and its role as an auxiliary pigment is to absorb light and transfer it to chlorophyll, thus protecting it from oxidation, was used by Weinberg et al. (2003) in studying the effect of herbicides that prevent carotenoid biosynthesis in C. campestris. β-carotene is considered to have a significant role in maintaining membrane amyloplasts, and its decrease therefore results in amyloplast destruction and decrease in starch contents (Weinberg et al., 2003). Flurochloridone caused bleeching effects merely two days after application but failed to inhibit stem elongation, and a full pigment recovery from the application of this herbicide occurred after six days. In contrast, sulcotrione and mesotrione slowed down the recovery (Weinberg et al., 2003) but it occurred nevertheless.
Introduction of transgenic crops that are tolerant to phloem-transported broad-spectrum herbicides has inspired some researchers (Nadler-Hasser & Rubin, 2003;Nadler-Hasser et al., 2004) to try to use them for control of field dodder. However, Nadler-Hasser and  found that field dodder was not reduced by glyphosate when it was applied to a transgenic sugar beet crop. Sulfometuron had the same effect in a tomato crop tolerant to that herbicide. Similar data have been reported after control trials of C. campestris in glyphosate-tolerant tobacco (Nadler-Hasser et al., 2004). Cudney et al. (1992), Cudney and Lanini (2000), and Sarić-Krsmanović et al. (2015) also examined the effects of non-selective contact herbicides, such as paraquat and diquat, in controlling field dodder in alfalfa and red clover. Control results were good but the host crops were also greatly affected, so that their use is meaningful only in small areas of infestation.

CONCLUSION
Successful control of field dodder requires a systematic approach of the integrated protection program that begins with dodder monitoring in crops, as well as ruderal areas, and includes adequate crop rotation, planned growing of crops that are not suitable hosts to field dodder, a variety of preventive measures and physical removal, the use of tolerant cultivars and biological agents, as well as treatments with herbicides when the problem cannot be solved any other way.