Biology and Management of Cuscuta in Crops W.T. Lanini1 and M. Kogan2

LITERATURE REVIEW

Biology and Management of Cuscuta in Crops

W.T. Lanini1 and M. Kogan2 1Department of Plant Science University of California, Davis One Shields Ave, Davis, CA 95616 2Facultad de Agronomía e Ingeniería Forestal Pontificia Universidad Católica de Chile Casilla 306-22, Santiago, Chile

Abstract

W.T. Lanini and M. Kogan. Biology and management of Cuscuta in crops. Cuscuta is a stem and leaf parasite that infects many broadleaf crops, ornamentals and weeds and a few monocot crops. It lives entirely on the host plant, thus reducing the growth and yield of the host. Preventing infestations by planting crop seed free of Cuscuta seed, rotating to non-host crops, delaying crop planting until fall for sugarbeet (Beta vulgaris), use of resistant varieties or large transplants, and preemergence herbicides have all been shown to be successful in certain crops. Once Cuscuta attaches to a crop, some yield loss will occur, regardless of the method of control, and selective control becomes very difficult. Post attachment control often requires killing or severely injuring the host plant to avoid spread of Cuscuta to surrounding plants. However, several herbicides have been shown to selectively suppress attached Cuscuta, but complete control is rarely obtained. Cuscuta attached to genetically modified, herbicide resistant crops, have not been successfully killed by treatment with herbicide in all cases, indicating that these crops will only be a partial solution to the problem. Cuscuta control will require an integrated approach conducted over a period of many years.

Key Words: Cuscuta, dodder, parasitic plant, resistance, weed management. Cien. Inv. Agr. 32(3): 127-141. 2005

INTRODUCCTION as important in Chilean crops. Dodder is a nonspecific parasite that attacks, sometimes The genera Cuscuta (known as dodder) are simultaneously a wide range of host species obligate parasitic plants with approximately including many cultivated plant species and 170 different species distributed throughout dicotyledonous weeds, but not grasses or the world (Holm et al., 1997). Most of the monocotyledonous weeds (Table 1; Dawson 170 species are found primarily in the et al., 1994). Similarly, the same crop may Americas from Canada to Chile of which 7 serve as a host of several dodder species or 8 are known in Chile (Navas, 1979). (Cudney and Lanini, 2000). The dodder Kogan (1992) recognized C. chilensis, C. seedling coils around the host stem and racemosa var. chiliana and C. campestris leaves, penetrates their tissue and vascular

Received on 16 March 2005; Accepted on 29 April 2005 1 Corresponding author: W.T. Lanini,[email protected] 128 CIENCIA E INVESTIGACION AGRARIA system via haustoria, and exploits the host throughout the warm seasons. In addition, by withdrawing photosynthates and water the nature of attachment and association (Figure 1). Thus, the vigor of the host is between host and parasite requires a highly lowered and crop production is dramatically selective herbicide to destroy the parasite reduced. Once a seedbank is established, without crop damage (Fer, 1984). This article control is extremely difficult, as dodder seeds reviews the life cycle, distribution and the can remain viable in soil for 20 years or control measures currently used for control more, and continue to germinate and emerge of dodder in crops.

A

B C Figure 1. Dodder, Cuscuta sp, common obligate parasitic plants. A. Onion field heavily infested with dodder; B. Dodder haustoria (arrow) penetrating tomato stems; C. Dodder wraping (arrow) arrow around tomato stems. VOL 32 N°3 SEPTEMBER - DECEMBER 2005. 129

Table 1. Crops, ornamental plants, and common weeds susceptible to dodder (Cuscuta spp.) infestation. Latin name Common name Crops Monocotyledonous Allium cepa Onion Allium sativum Garlic Dicotyledonous Asparagus officinalis Asparagus Beta vulgaris Sugarbeet Capsicum annuum Pepper Carthamus tinctorius Safflower Citrus spp. Citrus Cucumis melo Melon Cucumis sativus Cucumber Daucus carota Carrot Ipomoea batatas Sweet potato Lycopersicon esculentum Tomato Punica granatum Pomegranate Solanum melongena Eggplant Solanum tuberosum Potato Ornamental Monocotyledonous Impatiens spp. Impatiens Chrysanthemum spp. Chrysanthemum Ipomoea spp. Morningglory Dicotyledonous Satureja hortensis Summer savory Coleus blumei Coleus Geranium spp. Geranium Dahlia merckii Dahlia Parthenocissus quinquefolia Virginia-creeper Campsis radicans Trumpet-vine Hedera helix English ivy Petunia inflata Petunia Foeniculum vulgare Fennel Mentha spp. Mint Origanum majorana Marjoram Catharanthus roseus Periwinkle Weeds Monocotyledonous Solanum nigrum Black nightshade Portulaca oleracea Common purslane Amaranthus blitoides Prostrate pigweed Dicotyledonous Bilderdykia convolvulus Wild buckwheat Convolvulus arvensis Field bindweed Salsola tragus Russian thistle Chenopodium album Lambsquarters

DODDER LIFE CYCLE 1987). Favorable soil temperatures for dodder germination and emergence are in Cuscuta seeds germinate independently the range of 15 to 38°C, with an optimum of the presence of host plants (Dawson, around 30°C (Hutchison and Ashton, 130 CIENCIA E INVESTIGACION AGRARIA

1979), which corresponds with the disappear completely (Wolswinkel, 1984). prevailing temperatures during the spring As the dodder plants grow, support is and summer. Because of the seed size (1 maintained by continually reattaching to to 2 mm in diameter), emergence is limited the host. Dodder plants grow about 7 cm to the upper 1 to 1.5 cm of soil. Germi- per day and one plant can cover 3 m2 in a nating seeds will emerge as rootless and growing season. When other suitable hosts long yellow-orange thread-like leafless are nearby, dodder extends and attaches stems, which can grow to 2.5 to 7 cm in to their stems, spreading from one host to height. After germination, the dodder another, often forming a dense vegetative seedling circumnutates in a counter mat of intertwined stems. Flowering can clockwise direction in search of a host occur from late spring through fall, stem or other objects to wind around. It is depending on the species and date of possible that light or humidity may emergence, however seed set is highest in influence growth toward a host plant. the late summer and fall. In a field study These rootless seedlings will generally of dodder (C. pentagona) developing on only attach to hosts that are within a processing tomato, the first dodder flowers distance of 2.5 to 5 cm. Cuscuta seedlings were observed at 51 days after initial possess a rudimentary autotrophic system, attachment and the first viable seeds were containing only a small amount of observed at 60 days after attachment. First chlorophyll (Table 2) and other accessory flowering of dodder was observed to pigments (Dinelli et al., 1993). However, initiate near the point of initial attachment the autotropic system is insufficient to and later flowering progressed out away support growth. Thus, if no suitable host from this point. Once seeds are shed to is found within 3 to 5 days, the seedling the soil they can remain dormant, yet will die. Soon after the connection between viable, in the soil for 10 to 30 or more the parasite and host is established, the years, depending on the species and dodder seedling loses its soil connection environmental conditions. and lives entirely from photosynthates and water extracted from the host plant (Parker Table 2. Content of chlorophyll a and b in and Riches, 1993). Dodder adheres to the Cuscuta campestris, Convolvulus arvensis and host with a cementing layer of pectin and Beta vulgaris. develops haustoria within a few days due Species Organ Chlorophyll a + b to thigmotropic responses and chemical (mgág-1)1 recognition of the host plants (Press et al., B. vulgaris Leaves 3.91 ± 0.31 1990). The haustoria, single-cell hyphae, C. arvensis Leaves 2.54 ± 0.21 elongates within the host tissue and meets C. campestris Stems 0.28 ± 0.02 the vascular bundles, where they From: Dinelli et al., 1993. differentiate into xylem and phloem 1Based on dry matter measurements. ±Standard elements. This highly efficient absorption deviation system allows the parasite to divert resources - water, amino acids and Economical Importance and geographical assimilates - from the host into the parasite distribution (Dorr, 1987). It has been shown that when The wide geographical distribution of Cuscuta and developing seeds from the dodders (Table 3) and their wide range of host plant fruit compete for assimilates, hosts, make them amongst the most the sink activity of dodder is much stronger damaging parasites worldwide (Parker and while the sink activity of the fruit can Riches, 1993). Studies have shown that VOL 32 N°3 SEPTEMBER - DECEMBER 2005. 131 field dodder (C. pentagona) infestation production by more that 50% (Cudney et reduced tomato (Lycopersicumal., 1992). Where present in harvested esculentum) yield by 50 to 75% (Table 4; alfalfa, its moist stems will not allow the Lanini, 2004). It was shown that field hay to cure properly resulting in moldy, dodder infestation reduced carrot (Daucus unmarketable hay. Other legume crops carota) yield by 70 to 90% (Bewick et al., vary in their sensitivity to dodders. Bean 1988). Dodder is also considered a (Phaseolus spp.) was reported as resistant troublesome weed in onion (Allium cepa). to China dodder (C. chinensis) (Rao and Rubin (1990) stated that onion fields Reddy, 1987) and to field dodder in India heavily infested with dodder should be (Nemli, 1987), but sensitive to C. destroyed, as there is no selective herbicide lupuliformis in France (Liu et al., 1991). to control it available for this crop. In On the other hand, China dodder is a carrots or onions infested with dodder, the noxious weed in soybean (Glycine max) roots or bulbs, respectively, fail to reach in China (Li, 1987). Ornamental shrubs, a marketable size. When multiple dodder trees and groundcovers are often infested plants attack the same host (tomato) plant, with dodder (Table 1). Dodder infestations death of the host often occurs. Alfalfa are readily apparent along roadsides in (Medicago sativa) and clover (Trifolium weeds, shrubs and trees. Host plants are pratense) are the most common crops rarely killed by dodder infestation. The infested by dodder (Dawson et al., 1994). weakened state of the infected plants does Although dodder does not generally kill predispose them to loss from other alfalfa, it weakens the crop, reduces stand maladies (disease, insect, and nematode and can reduce yield of forage and seed invasions).

Table 3. The main Cuscuta species invading crops and their geographical distribution. Species Distribution Comments C. pentagona Worldwide The most important Cuscuta species, attacking a wide (C. campestris) range of species, including vegetables, fruits, ornamentals and woody plants. It is reported as a weed in 25 crops in 55 countries. C. epithymum Worldwide This is a serious weed problem in Europe and Asia, on clovers, other forage legumes and carrot. C. europaea Europe and North America A serious weed in Europe, but also found in USA. C. gronovii North America This species typically is found in wet places and along water courses. It has a wide host range, attacking cranberry, other crops and shrubs. C. indecora North and South America This is an important species primarily found attacking alfalfa. C. planiflora Asia, Europe, and A widespread species having a wide host range, North America including alfalfa and clovers. C. reflexa Asia A serious weed problem in woody perennials. C. suaveolens South America, Native to South America, but now found worldwide, Europe and Africa primarily attacking alfalfa 132 CIENCIA E INVESTIGACION AGRARIA

Table 4. Tomato fruit yield relative to the level of dodder infestation (% cover at harvest) at Davis, California. Dodder cover 1991 1992 at harvest reds greens rots reds greens rots (%) tonáha-1 tonáha-1 80 to 100 36.3 7.0 0.0 22.9 1.1 0.7 60 to 80 60.7 5.3 0.0 39.5 1.6 1.8 40 to 60 66.7 10.5 0.0 73.4 3.1 2.0 20 to 40 58.0 10.0 0.3 93.6 3.4 3.6 1 to 20 68.7 13.2 0.1 95.4 5.2 2.7 0 73.3 14.3 0.2 93.4 7.4 1.6

DODDER CONTROL certified free of dodder seed. To prevent new dodder infestations, clean equipment Dodder prevention can be achieved by after working in a dodder infested field, prior avoidance, and control by mechanical means to moving to another field. Similarly, do not or hand removal, resistant varieties, and allow animals feeding in a dodder infested herbicides. None of these methods work field to move to a dodder free field, as dodder 100% of the time, but all offer some tools seed are known to survive passage through for managing this parasitic weed. Another the digestive system of many domestic complicating factor is that several dodder animals (Gaertner, 1950). Many broadleaf species are often involved. Dodder weeds have been observed to host dodder populations have also been observed to vary (Table 1; Ashton and Santana, 1976). Hence, in virulence and susceptibility to herbicide proper weed control in and around cultivated treatment. Thus, an integrated approach to areas will prevent dodder from parasitizing managing dodder will be needed. weeds and would reduce the potential for dodder seed production and dispersal. SANITATION Fluctuations in soil moisture and Avoidance and prevention are the most temperature near the surface may initiate effective and most economical methods to dormancy breaking of superficially buried reduce dodder infestations (Parker and dodder seed (Hutchison and Ashton 1979). Riches, 1993). Dodder seeds are likely spread These authors observed dodder emergence by man, through seed international to begin in March and to cease in early to commerce, movement of equipment, and in mid-May (early spring to late spring) in the the mud on tires and shoes (Cudney and central valley of California (N 38°33, W Lanini, 2000). Planting contaminated seed 121¼47), despite temperatures in the can lead to severe infestations (Parker and optimum range for germination and Riches, 1993). C. pentagona has beenemergence (Hutchison and Ashton 1980). distributed worldwide as a contaminant of Parker and Riches (1993) observed a flush alfalfa seed, as both dodder and alfalfa seeds of dodder seed germination often occurs are very similar in appearance. Dodder seed early in the spring season and they attributed has also been spread as a contaminant of this to dodder seed losing their dormancy flax, linseed, and niger seed (Parker and during the cold winter months. Additionally, Riches, 1993). Thus, avoid using seed from the major flush of dodder emergence often fields where dodder is present or use seed occurs close to the time of crop emergence, VOL 32 N°3 SEPTEMBER - DECEMBER 2005. 133 indicating that field preparation, crop Table 5. Number of dodder attachments to seeding and irrigation or rainfall may also selected tomato varieties when scarified dodder be involved in germination, perhaps by was seeded into pots when tomato reached the scarification of the seed coat or leaching 1 leaf stage or 3 leaf stage. of chemicals out of the seed coat. Delayed Tomato variety Dodder attachments planting can reduce dodder infestation, but 1 leaf 3 leaf that is not always practical due to marketing Campbell CXD 233 3 2 considerations for certain crops. In direct Heinz 1100 0 0 seeded crops, the use of transplants may Heinz 9492 0 2 allow a later planting without sacrificing Halley 3155 4 5 early market delivery. Larger transplanted SVR 024 1 0312 2 3 tomatoes have also been observed to be Campbell CXD 234 5 0 more resistant to dodder attachment (Table Heinz 1400 4 2 5), as older stems may become more SVR 024 2 0662 3 0 lignified (Lanini, 2004). Early seeding of SVR 024 2 0664 1 0 the crop in spring might delay infestation SVR 024 2 0665 3 2 due to low temperatures, which together 4863N 4 0 with a delayed irrigation can prolong the AB 2 3 2 APT 410 4 1 period before dodder emerges (Dawson, Campbell CXD 179 4 0 1987). These means will allow the Campbell CXD 222 4 0 development of dense crop foliage that will ENP 113 5 0 suppress dodder's initial light dependent Heinz 0830 3 0 growth. Heinz 2501 3 0 Heinz 2601 2 2 Crop rotation can be an effective method Heinz 8892 4 1 to reduce dodder infestations. However, the HMX 3859 5 0 large weed and crop host range makes it Heinz 9663 0 0 difficult to avoid this pest by crop rotation Heinz 9665 0 0 and thus, careful crop selection is essential Heinz 9780 2 0 (Parker, 1991). Dodder is often observed Heinz 9888 0 0 coiling around grasses, but cannot form Heinz 9997 2 0 haustoria connections and will die unless Average 2.69 0.85 a suitable host is found. Thus, growing cereals or other grass crops (which are not Due to the absence of roots, dodder parasitized by most dodder species) seedlings (before attachment to the crop) continuously for several years, may facilitate are easy to control by shallow cultivation the exhaustion of dodder seed bank in the (Parker and Riches, 1993). In addition, soil (Dawson, 1987). Lanini (2004) found tillage may hasten drying the soil surface, that growing wheat followed by corn in a thus preventing further dodder germination field heavily infested with C. pentagona and emergence. Tillage can be employed reduced the number of dodder plants in crops grown in rows, which allow infesting tomato by 90%. Thus, two years cultivation such as sugar beet and alfalfa of growing a non-host crop was effective grown for seed production. However, the in reducing the population. Of course these tillage only controls the dodder growing grass crops must be well weeded, as dodder between the rows and not in the rows. Deep can easily develop and set seed on broadleaf tillage with implements that invert the soil weeds in these crops. can greatly reduce emergence of recently 134 CIENCIA E INVESTIGACION AGRARIA shed seed (Parker and Riches, 1993), but RESISTANCE may bring previously deep buried seed to the soil surface. In cranberry, burying C. Although not much effort has been made gronovii seed with 2.5 cm of sand reduced to assess variety differences to dodder infestation, indicating emergence was attachment or damage, some resistance has primarily in the superficial soil layer been observed among sensitive crops. (Sandler et al., 1997). Late season tillage Different levels of resistance to C. may facilitate the distribution of vegetative pentagona were observed within four wild twigs of dodder from an infested row to Lycopersicon species (Al-Menoufi and other plants, and should be avoided. Dodder Ashton, 1991). Incompatible interactions often spreads beyond the typical crop row between Cuscuta species and by late season and tillage can break off resistant/tolerant tomato plants have been vegetative pieces of dodder which can attach reported by Loffler et al., (1995). They to non-infected plants if they end up in described incompatible interactions between close proximity to these plants. 30 tomato varieties and C. reflexa. This resistance was characterized by enlargement Removal by hand crews, of the crop with of epidermis, hypodermis and collenchyma dodder attached, remains a viable but of tomato cells, necrotic tissue developing expensive option, when infestations are around the pre-haustoria and hardening of small patches. When infestations are cell walls adjacent to the necrotic tissue, extensive, hand removal is prohibitively preventing haustoria formation. Ihl and expensive, not to mention the loss in the Miersch (1996) observed a similar crop stand. If done, hand removal should resistance phenomenon in 22 tomato be done when dodder is first detected to varieties and four wild tomato species to prevent spread and seed production. In a four Cuscuta species: C. reflexa, C. trial area, farm workers were observed to japonica, C. odorata and C. europaea. In remove approximately 90% of the attached all cases, no functional haustoria were dodder (Lanini, 2004). The remaining 10% formed due to hypersensitive response of was generally missed, because it was too external cell layers of the tomato stems or small to be easily detected. If a hand crew petioles after pre-haustoria contact. The can be sent back through a field about 15 layer of dead tomato cells prevented to 21 days after the first hand weeding, the intrusion of initial haustoria, followed by remaining dodder plants can be removed an increase in peroxidase activity. prior to any dodder seed production. Dodder Nevertheless, there are contradicting reports can reattach to a new host if left in close of resistance of tomato to field dodder. proximity to living crop plants, but if the Nemli (1987) found resistance to C. plants that are removed are moved six or pentagona (C. campestris) in all five tomato more inches from the remaining crop plants, varieties tested, however, Ashton and the dodder will not be able to reach a new Santana (1976), Hutchison and Ashton host. Dodder seedlings can only survive a (1980) and Nir et al., (1996) reported that few days without a host, however dodder all commercial tomato varieties were stems which are attached to a host plant, seriously attacked by C. pentagona. These have been known to survive for several contradictions may be due to variation in weeks after being removed from the host, the tomato varieties used in the studies or before drying. These twigs are able to attach variation in C. pentagona populations. to a new host plant and rapidly produce Recently, Miranda-Sazo (2003) observed haustoria (Dawson, 1984). different levels of virulence among several VOL 32 N°3 SEPTEMBER - DECEMBER 2005. 135 populations of C. pentagona, perhaps dry climate and the different dodder species partially explaining the contradictions in (Lanini, 2004). Difficulty in culturing and the reports on resistant tomato varieties. In efficacy under field conditions has limited an examination of 33 commercial tomato the use and commercialization of fungi. varieties, sensitivity to a highly virulent C. Solarization has also been tested and found pentagona population varied considerably to not be effective, as dodder has a hard (Goldwasser et al., 2001; Lanini, 2004). seed coat. Thus far, six commercially available tomato varieties have been identified as dodder CHEMICAL CONTROL resistant Ð Heinz 9492, Heinz 9553, Heinz 9992, Heinz 9888, Heinz 1100, and The use of herbicides to control dodder has Campbells CXD 233. Some dodder plants been intensively studied worldwide. are able to attach and survive on these Treatments may be divided according to varieties, but generally, tomato yields are the timing of application; applications made not reduced and dodder seed production is prior to attachment to the host or very low or non-existent. The Heinz applications made after attachment. varieties were originally developed to be bacterial canker (Clavibacter michiganensis Dodder control prior to attachment subs. michiganesis) resistant, and thus, the This approach attempts to control dodder mechanism of disease resistance could be before it attaches to the host and eliminate what prevents dodder growth. any possible damage (Parker, 1991). Fumigants, such as methyl bromide, or BIOLOGICAL CONTROL metam sodium controls many weeds prior to vegetable planting, but species with a The potential of using insects and pathogens hard seed coat, such as C. pentagona, are for dodder control has been reviewed not affected (Lanini, 2004). However, (Parker, 1991). In spite of the optimism, Ashton and Santana (1976) reported some there is still much research to be done before success in controlling dodder ahead of any commercial biological agent for dodder transplanting tobacco. However, since control can be released (Bewick et al., transplants were used, it is difficult to 1987). Several fungi have been found that determine if the fumigant was effective or damage dodder, including Fusarium if the transplants were too large for dodder tricinctum and Alternaria spp. which attack to successfully attach. swamp dodder (C. gronovii) and A. alternata and Geotrichum candidum which There are many preemergence (PRE) both attack field dodder (C. pentagona). herbicides that have been shown to affect Additionally, researchers in China have germinating dodder seedlings. These found that a conidia suspension of herbicides are applied to the soil either Colletotrichum gloeosporioides has before seeding or before emergence of the provided selective control of C. chinensis crop. When these herbicides are used, and C. australis in soybeans. In field tests dodder seeds germinate but initial growth with Alternaria destruens, Bewick et al., is reduced and attachment to the host fails. (2000) reduced C. gronovii attack by 90% Chloropropham (CIPC), a carbamate in cranberry (Vaccinium macrocarpon) and herbicide, was the first soil-applied carrot (Daucus carota), but it was notherbicide used for dodder control in various effective against C. pentagona under crops (Lee and Timmons, 1956). California conditions, possibly due to the Chloropropham is no longer used, however, 136 CIENCIA E INVESTIGACION AGRARIA pronamide, a benzamide herbicide, is now Pendimethalin is also recommended for used to prevent dodder attachment in alfalfa, selective dodder control in carrot, onions, sugarbeet, cranberry (Bewick et al., 1989) and alfalfa (Orloff and Cudney, 1987). and onion (Rubin, 1990). It is typically Pendimethalin is less volatile than trifluralin used at 1-2 kgáha-1, of active ingredient (a.i.) and thus incorporation is not necessary, but and its persistence is longer than overhead irrigation or rainfall improves chloropropham. Pronamide is also used in activity (Parker and Riches, 1993). sugarbeets in Chile as a sequential application for control of dodder, with 1 Various herbicides including ethofumesate -1 kgáha applied at cotyledon to first true leaf at 2.2 kgáha-1 (a.i.), were also reported to sugarbeets and a second and possibly a control dodder selectively in sugarbeet third application at the same rate at 20 day (Orloff and Cudney, 1987). Ethofumesate intervals. DCPA applied at 7 to 14 kgáha-1 can be used both pre and postemergence, (a.i.), provides selective dodder control in and is selective in sugarbeet at rates of 0.25 carrot (Shlevin and Golan, 1982), to 2.0 kgáha-1 (a.i.), (Foschi and Rapparini, ornamentals, and onion. Unlike 1977). Dichlobenil is used to prevent dodder chloropropham and pronamide, DCPA is growth in ornamentals and blueberries. non-volatile and presumably acts on dodder Thiazopyr (thiazole herbicide), which is by direct contact (Bayer et al., 1965). currently recomended in tree and vine crops, has been shown to stunt dodder seedlings Dinitroaniline herbicides have been and prevent attachment to host crops, such examined for their effectiveness to control as alfalfa. Following thiazopyr treatment, dodder in alfalfa (Orloff and Cudney, 1987). field dodder seedling emergence is delayed, Although they differ in their persistence of and seedling length is reduced, while width dodder control, all dinitroanilines reduced is increased. The seedlings are not able to dodder infestation. Pendimethalin and circumnutate normally and attachment to prodiamine were more effective than a host does not occur. trifluralin and controlled dodder for a longer period of time. Prodiamine, applied at high Post-attachment dodder control rate (2.6 kgáha-1 (a.i.)), is the longest lasting Parker (1991) stated that post-attachment of the dinitroaniline herbicides, but its control of a parasite is very important in persistence restricts its use only to order to reduce its seed production and further ornamental and non-crop areas. Trifluralin, spread, although irreversible damage was at fairly high rates (22.5 kgáha-1 of the TR- already done. Rapid eradication of dodder 10 granular formulation), is also used for patches should be done when first detected selective dodder (C. indecora and C.in the field before they have a chance to pentagona) control in alfalfa. Trifluralin is produce seeds. In alfalfa, Cudney et al. surface applied in a granular formulation (1992) suggested spraying both host and in alfalfa, which concentrates the herbicide parasite, with a contact herbicide, such as near the surface where dodder seed paraquat or by searing with a flame-throwing germinates. Using the liquid formulation torch or hand burner. In infected alfalfa for of trifluralin has not been successful in hay, flail mowing or burning can be effective controlling field dodder in tomatoes and (Orloff and Cudney, 1987). In tomatoes or other crops, as trifluralin on or near the soil other row crops with new or small surface degrades rapidly, and thus the infestations, hand roguing host plants with shallow germination depth and lack of roots attached dodder while they are small, before permits dodder to escape control. many plants are infected can be a reasonable VOL 32 N°3 SEPTEMBER - DECEMBER 2005. 137 practice. Patches should be marked with a carrot plants infected with swamp dodder flag or other method, and examine the fields accumulated in the parasite tissue more than again two or three weeks later to insure all in any part of the host plant. Along this line, dodder was removed. Diquat, a contact studies have been conducted using phloem- herbicide, has been used for dodder control mobile herbicides, such as glyphosate, for in alfalfa and clovers (Gimesi, 1966). Diquat selective post-attachment control of dodder application following forage harvest limits in alfalfa (Liu and Fer, 1990; Dawson, the crop foliage that is damaged, since both 1989a). No damage to alfalfa was observed crop and dodder are desiccated by this following treatment with low doses of treatment. Paraquat is used in a similar way glyphosate (75 to 150 gáha-1(a.i.) when both, to diquat, but generally alfalfa is less tolerant, parasite and host, were still vegetative and and thus its use is typically limited to spot vigorously growing (Dawson, 1989b). treatment of small patches (Cudney and Similarly, glyphosate at 400 gáha-1(a.i.) Lanini, 2000). applied late in the life cycle of carrot when swamp dodder was in full flower, The nature of attachment and association satisfactorily controlled the parasite and between host and parasite requires a highly increased carrot root yield (Bewick et al., selective herbicide to destroy the attached 1988). Unfortunately, host crops can be dodder without crop damage. injured by glyphosate treatment (Orloff and Postemergence applications of herbicides Cudney, 1987) and the parasite may not be such as ethofumesate, pronamide, and adequately controlled (Frolisek, 1987). pendimethalin can suppress the parasite, but dodder generally recovers (Orloff and Several acetolactate synthase (ALS) Cudney, 1987). It was suggested that the inhibiting herbicides have been shown to low transpiration rate of dodder may limit control or suppress dodder. When imazaquin movement of xylem mobile, soil applied is applied to dodder-infected soybean and herbicides into the parasite, and thus, should mung beans plants, the herbicide not be used for dodder control (Fer, 1984). accumulates in the apical part of the dodder The author argued that xylem-mobile stem (Liu et al., 1991). It has also been compounds move and accumulate mostly shown that imazethapyr and thiazopyr in the host organs with high transpiration (thiazole herbicide) applied to carrot plants rate and may damage the host more than infested with dodder were less damaging the parasite. As expected, Liu and Fer (1990) than when applied to non-infested carrot, found that pendimethalin, an 'ambimobile' indicating the potential of using low rates herbicide, applied to mung beans of non-selective herbicides for selective (Phaseolus aureus) roots does not move to control of parasitic weeds (Nir et al., 1996). the attached dodder via the transpiration Possibly the herbicide accumulates stream. However, when pendimethalin was selectively in the dodder due to it strong sink applied to one leaf, 56% of the herbicide activity. Imazethapyr at 100-150 gáha-1 (a.i.) was accumulated in the parasite. applied preemergence reduces dodder infestations in seedling alfalfa and A phloem-mobile herbicide applied suppression of more established dodder broadcast to the host plant should stems (Cudney and Lanini, 2000). accumulate selectively in the parasite Rimsulfuron applied at 35 gáha-1 (a.i.) because of its stronger sink (Nir et al., suppresses dodder in tomatoes, particularly 1996). Bewick et al., (1991) reported that when split applications are used (Mullen 14C-labeled glyphosate foliar applied to et al., 1998). Further studies have shown 138 CIENCIA E INVESTIGACION AGRARIA that treatments made soon after dodder to non-host crops for several years may be attachment were more effective than required. Once a host crop is planted again, applications made after dodder became well treatments must be made to contain escaped established. However, the season-long plants. control achieved by the best rimsulfuron treatments was only about 50% and differed RESUMEN substantially in different fields, possibly indicating dodder population differences La cúscuta (Cuscuta spp.) es un parásito (Lanini, 2004). Sulfosulfuron applied at 20 foliar y de los tallos, que infecta muchos to 50 gáha-1 (a.i.) was shown to be very cultivos de hoja ancha, ornamentales y effective at controlling attached dodder in malezas y sólo algunos cultivos direct seeded tomatoes, with excellent monocotiledóneas. Vive completamente en selectivity (Eizenberg et al., 2003), however, la planta hospedera, reduciendo el it is only registered for use in wheat in the crecimiento y los rendimientos. La USA. prevención por medio de rotación de cultivos con especies no hospederas, Introduction of transgenic crops resistant retrasando la fecha de siembra hasta el to phloem-mobile broad-spectrum otoño en el caso de la remolacha azucarera herbicides to selectively control parasitic (Beta vulgaris), uso de cultivares resistentes weeds was suggested for dodder control y el uso de herbicidas de pre emergencia, (Rubin, 1991). However, Nadler-Hasser han demostrado ser útiles en ciertos cultivos. and Rubin (2003) found that dodder Una vez que la cúscuta ataca el cultivos, growing on transgenic glyphosate resistant se registrarán pérdidas de rendimiento, sugarbeet was not controlled when treated independientemente del método de control with glyphosate (1.08 kgáha-1(a.i)), nor when aplicado, siendo en estas circunstancias, sulfometuron resistant tomatoes were muy difícil disponer de métodos selectivos. treated with sulfometuron (22.5 gáha-1 (a.i.)). El control luego de la fijación de la cúscuta Dodder may be obtaining amino acids from a la planta a menudo requiere de la the resistant host plant and thus are able to destrucción o de daños muy severos en la survive these treatments. Since dodder, in planta hospedera para evitar la dispersión a sense, is just another stem on the host de la cúscuta a las plantas vecinas. Sin plant, we believe that some crop injury may embargo, existen varios herbicidas que han be necessary to achieve dodder control with demostrado selectividad permitiendo herbicides. Thus, rates higher than are detener el ataque de cúscuta, pero rara vez currently registered for use may be needed, se obtienen un total control. La cúscuta regardless of the herbicide used. adherida a plantas modificadas genéticamente, en cultivos resistentes a CONCLUSIONS herbicidas, no ha sido exitosamente controlada con tratamientos herbicidas, The most successful control of dodder indicando que estos cultivos permiten una involves a systematic approach whereby solución parcial al problema. El control de several methods of control are used together. la cúscuta requiere de una estrategia de Effective management requires control of control integrado aplicada por varios años. any new populations, prevention of seed production and monitoring in subsequent Palabras clave: Cabello de ángel, Cuscuta, years to insure complete control. Where plantas parásitas, resistencia, manejo more extensive infestations exist, rotation de maleza. VOL 32 N°3 SEPTEMBER - DECEMBER 2005. 139

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