Alectra vogelii (yellow witchweed)

A. vogelii is an annual parasitic weed of legume crops, particularly cowpea and groundnut, in semi-arid areas of East, West, Central and Southern Africa. It is closely associated with cultivation, is occasionally found associated with weeds of fallows but rarely in natural vegetation. Copious seed production and a long-lived seed-bank allow the rapid build up of infestations when susceptible crop cultivars are planted. Tiny seeds are easily spread by wind, surface water flow or in crop seed. The genus Alectra is on the USDA Federal Noxious Weed list. Despite the similar life cycle to Striga species which are listed, and potential for crop damage, A. vogelii does not appear on Noxious weed lists in Australia. An assessment of its global invasive potential is given by Mohamed et al. (2006).

Engler (1922) split the species into A. angustifolia, A. merkeri and A. scharensis. However, in his taxonomic revision of the genus, Melchior (1941) considered these all to be characteristic of A. vogelii on the basis of the specimen collected by Vogel in Guinea in 1843. All previous and subsequent major floras for West Africa (Hutchinson and Dalziel, 1963) and south-eastern Africa (Philcox, 1998) have maintained the name as A. vogelii. Although these accounts include the genus in the family Scrophulariaceae, a sequence analysis of three plastid genes suggested that it should be placed in the Orobanchaceae along with other closely related parasitic genera (Olmstead et al., 2001). No morphological or anatomical evidence for this reclassification has however been advanced.

As flowering specimens are very leafy and with a similar habit to many free-living plants, people who are not familiar with root hemi-parasites are unlikely to recognize that A. vogelii is indeed parasitic. Below ground, bright orange stems are attached to host roots by a spherical haustorium up to 2 cm in diameter. This is composed of a mass of host and parasite tissue and the orange adventitious roots of the parasite. Plants grow to 30-45 cm tall, often as a single stem but sometimes branching from near soil level. The stems and leaves, which can be 1.5 to 3.5 cm long by 0.3 to 1.5 cm wide, are conspicuously hairy. Leaf shape, particularly the nature and extent of toothing along the edge of the lamina, varies considerably. In parts of West Africa, leaf margins are almost entire, in central and southern Africa they may have two to five widely spaced teeth along each edge while in Kenya plants with five or six sharp teeth, each up to 3 mm long, have been collected. Flowers appear singly on a short stem in the axils of upper leaves or bracts. Up to 10 flowers may open on one day. The flower buds are enclosed in a densely hairy calyx whose five lobes each have a triangular tip with an obtuse apex. The tubular corolla is formed of five petals fused towards the base, so that the flower is bell-shaped when open. The corolla is 0.6 to 1 cm in diameter and somewhat longer than the calyx. The petals are pale yellow and may or may not have three deep red veins. Both types of flowers can be found in a group of plants. The anthers and filaments are glabrous. The flowers wither and remain covering the developing globose seed capsule which swells to approximately 5 mm in diameter at maturity. The dust-like seeds have a complex structure. An outer cell layer of the testa is modified into a cone or a 'trumpet-like' structure about 1 mm long within which the 'kernel' of the seed, measuring about 0.15 mm by 0.25 mm, is suspended. The surface of the seed coat is covered in indentations.

A. vogelii is distributed throughout semi-arid areas of tropical and sub-tropical Africa. In the Nigerian savannahs it can be found in cowpea crops which are also attacked by Striga gesnerioides, and it has been reported as the major parasite of the crop in the northern Guinea savannah (Lagoke, 1989). Elsewhere in West Africa, infestations tend to be more localized, as in southern Mali. A. vogelii replaces S. gesnerioides as an important constraint to cowpea production in East, Central and particularly Southern Africa.

A. vogelii has long been recognized as a constraint to cowpea production, in semi-arid area of sub-Saharan Africa, particularly in East and Southern Africa, mentioned in the 1920s in Kenya and the mid-1960s in Botswana (Parker and Riches, 1993). The species is assumed to have an origin in West Africa and to have spread with human migrations and along trade routes with cowpea cultivation but no records exist on its first appearance in particular areas. It is often present at low densities in stands of traditional cowpea land-races but builds up rapidly to become a problem when a susceptible exotic cultivar is introduced as occurred in Botswana from the late 1950s. There is no indication that the species is spreading although greater attention from development workers in communities where cowpea is produced for household food security has highlighted the distribution and importance of the species in the past 30-40 years.

Although A. vogelii is already widespread in semi-arid areas of Africa, further spread is possible as seed contaminating grain legume shipments to markets or on legume planting seed sold commercially or in samples distributed throughout sub-Saharan Africa for trials by research organizations. This should be prevented by undertaking seed multiplication on uninfested fields and careful inspection of the crop. The main danger in Africa would be to introduce biotypes with differential host specificity from one area to another. The accidental introduction of the related Striga asiatica, a noxious parasitic weed of maize and other cereals, into the USA in the 1950s (Parker and Riches, 1993) demonstrates that long-distance spread of the tiny seeds of these root parasites is possible. A. vogelii is already prohibited as a noxious weed in the USA (USDA-APHIS, 2003).

The reticulated surface of the minute seeds trap pockets of air when they float on water, making the seed buoyant and easily dispersed at least for short distances in rainwater run-off. The trumpet-like structure of the outer seed coat makes the seeds aerodynamically suited to being wind-blown even in the lightest breeze, and windy conditions are common in the dry season in regions where A. vogelii is found. Man is a dispersal agent through the harvesting of legume seed pods from infested stands. Seeds of the parasite may contaminate grain legume seeds during threshing and be transported to markets or neighbouring farms during local sales.

Cowpea is the major crop host of A. vogelii throughout its range (Parker and Riches, 1993). Bambara, groundnuts, common bean, soyabean, mung bean, and tepary are also common hosts and there have been occasional reports of infestation of chickpea and runner bean. Pigeon pea is the only widely grown grain legume which is not parasitized. Although A. vogelii can attack the crops listed there is clear geographic variation in the host range in different regions of Africa. Host range tests (Riches et al., 1992), indicate that populations from Mali, Nigeria and Cameroon can attack groundnut and cowpea. Samples from eastern Botswana and northern areas of Northern Province, South Africa attack mung bean in addition to cowpea and groundnut. Populations sampled from Kenya, Malawi and eastern areas of Northern Province, South Africa, parasitize bambara as well as crops which are susceptible elsewhere. No association has been observed between morphological variation, largely in leaf shape, and host preference. Many other legumes are hosts including species such as lab lab and velvet bean which are often introduced as fodder or green manure crops in infested areas. A. vogelii has a wide host range and has been occasionally recorded as parasitic on non-legume weeds including Acanthospermum hispidum and Vernonia poskeana (Compositae), Euphorbia (Euphorbiaceae) and Hibiscus (Malvaceae) species in addition to common legume weeds including Indigofera and Tephrosia species.

A. vogelii has a similar distribution to A. picta, with which it is easily confused in the field. A. picta has been observed parasitizing cowpea in northern Cameroon, eastern Hararghe, Ethiopia and in Malawi (Parker and Riches, 1993). The presence of so-called 'beards' or hairs on the stamen filaments of A. picta compared to the hairless filaments of A. vogelii is the character used to maintain these as separate species (Philcox, 1990). The leaves of A. picta have an entire margin or one small tooth on either edge of the lamina and so can be distinguished in the vegetative state from A. vogelii in eastern, central and southern Africa where this species has obviously toothed leaves as well as glabrous filaments. However, in Cameroon and West Africa, leaves of the two species are similar. Both species are known from the same areas of Cameroon and Malawi and in Malawi both have been observed growing in the same row of groundnuts. As A. picta has a similar host range to West African populations of A. vogelii, parasitizing cowpea and groundnut but not bambara or mung bean (Riches et al., 1992), and in view of the morphological similarities, there must be some doubt as to whether these are distinct species.

A. sessiliflora is another leafy member of the genus found in natural vegetation throughout the range of A. vogelii. It also occurs in Madagascar, Mauritius to India, Myanmar, China and the Philippines. The host range is almost entirely on weeds or natural vegetation, especially the Compositae (Parker, 1988). A. sessiliflora only has hairs on the nerves and margins on the calyx whereas in A. vogelii and A. picta the calyx is covered evenly with short hairs. Furthermore, A. sessiliflora tends to have sessile leaves which are more sharply-toothed and pointed than those of A. vogelii. A. orobanchoides Benth. (= A. kirkii Benth.), a third species associated with crops in Africa, is easily distinguished by undeveloped scale-like leaves. This species is occasionally found growing on tobacco and sunflower in southern Africa. A. fluminensis is a South American species of local importance as a parasite of sugarcane in Venezuela. It grows up to 1 m tall.

A. vogelii is always associated with the cultivation of leguminous crops, on which it is parasitic, in semi-arid savannah areas of sub-Saharan Africa. Reports of the species in association with non-crop legumes and occasionally non-legumes always involve weeds on fallow or cropped arable land. It has not been reported as a component of natural vegetation.

Genetics

The chromosome number (2n) is 38 (Parker and Riches, 1993). The extent of genetic variation within or between populations is not known.

Reproductive Biology

Controlled experiments have shown that A. vogelii can set seed as a result of either self- or cross-pollination. However, field observations demonstrate that the anthers will only release pollen when stimulated to do so by foraging insects (Riches, 1989; Parker and Riches, 1989). Pollen-feeding flies in the genera Cosmia, Ischiodon, and Rhyncomya and various bees including Amegilla and Lasioglossum species release a cloud of powdery pollen as they forage over the anthers onto the adjacent large stigma to effect self-pollination. As bees carry loads of pollen as they forage throughout a flowering stand of the parasite, it is likely that cross-pollination also results from insect activity. The relative importance of self- or cross- pollination has not been studied. Parker and Riches (1993) have reported that seeds may remain viable in the soil for up to 12 years. Each A. vogelii plant may produce 400,000 to 600,000 seeds (Botha, 1948; Visser, 1978).

Physiology and Phenology

A. vogelii is an obligate root parasite and seed germination follows exposure to chemicals in the root exudate of a potential host plant. The seed has no after-ripening requirement. Germination will occur within 5 days of adding a suitable stimulant to dry seed at 28-30°C (Visser and Johnson, 1982; Riches, 1989). Prolonged periods of imbibition of the seed in water, in the absence of a stimulant, does not induce a 'wet dormancy' characteristic of many parasites in the related genus Striga (Botha, 1948). Four substances that stimulate A. vogelii seed germination have been identified (Herb et al., 1987), including one with a structural similarity to the cytokinin group of plant growth hormones. A stimulant termed alectrol, isolated from cowpea root exudates (Muller et al., 1992) is chemically similar to the Striga germination stimulant strigol isolated from cotton roots. Synthetic analogues of strigol, including GR7 and GR24, are effective stimulators of the germination of A. vogelii as well as the Striga species that infest cereal crops in sub-Saharan Africa (Visser and Johnson, 1982).

The radicle of A. vogelii needs to penetrate a compatible host root within 8-10 days of germination to survive. Growth towards the root is a chemotropic response to a concentration gradient of host root exudate (Visser, 1978). The parasite grows within the host until contact is made with xylem vessels and phloem sieve tube elements of the host stele. About 12 days after germination, the parasite has penetrated the host and the parasite stem begins to elongate following the differentiation of the first leaves. The parasite stimulates a proliferation of host lateral roots in the region around penetration and formation of the haustorium. Shoots emerge above ground about 4 weeks after the parasite radicle has penetrated a cowpea root and first flowers are produced some 2 weeks later. The leaves contain around 18% of the chlorophyll content found in sunflower so photosynthetic activity is consequently low with carbon dioxide assimilation at only 21% of the rate found in sunflower (Harpe et al., 1979).

Environmental Requirements

As A. vogelii is largely dependent on annual cropping, environmental requirements mirror those of its major hosts cowpea, bambara, groundnut and soybean in sub-Saharan Africa. By and large these are found in semi-arid areas with a short growing season of 4 to 6 months, below 1500 m altitude. The parasite is most commonly found in areas of mono-modal rainfall with a long dry season as in Botswana or the Guinea savannah of West Africa, but it is also a pest in bimodal rainfall areas as in north-west and coastal Tanzania. Although crops are not produced during the cold dry season in the range of the parasite, frost at the end of the growing season will kill host plants surviving in crop residue on residual moisture and will prevent further seed production by A. vogelii. Host crops are largely associated with free-draining sands and sandy-loams.

Some herbivorous insects and fungal diseases have been reported from A. vogelii but their role in the natural regulation of parasite populations has not been quantified. Larvae of the moth Stenoptiloides taprobanes feed on the flowers preventing seed production on predated flowers (Parker and Riches, 1993). From East Africa, Greathead and Milner (1971) have reported both Ophiomyia strigalis attacking roots and Platyptilia sp. attacking flowers of A. vogelii. However, only a small proportion of plants are attacked so the overall effect on seed production is probably not significant. At some sites in Botswana, up to 40% of plants fail to produce seed due to a fungal die-back following infection of the stem by Fusarium species (Riches, 1989) including F. oxysporum and F. solani.

A. vogelii is a serious constraint to the production of grain legumes, particularly cowpea, bambara, groundnut and soybean in the semi-arid savannahs of sub-Saharan Africa. Before parasite emergence, aboveground affected cowpea plants may appear wilted. Delayed flowering, a reduced number of flowers and pods all contribute to yield loss. The extent of yield loss depends on the susceptibility of the cultivar with greatest losses reported for introduced lines rather than landrace types (Parker and Riches, 1993).

Most information on the economic impact of A. vogelii comes from East and Southern Africa. Yield losses of 20% were reported from Kenya in the 1920s with total crop loss in the 1980s in Embu District (Bagnall-Oakeley et al., 1991). In Botswana in 1979/80 un-infested fields of the cultivar Blackeye, introduced from the USA, produced an average grain yield of 602 kg/ha while in parasite infested fields less than 100 kg/ha was harvested (Riches, 1989). Losses in groundnut of 15% have been recorded due to the parasite in Nigeria (Salako, 1984), and yield reduction in bambara in South Africa of 30-50% has been observed (Beck, 1987). Late sown crops of soyabean may be completely destroyed by the parasite in northern Nigeria (Lagoke, 1989). A. vogelii is also a constraint to common bean production in the Blantyre Shire Highlands of Malawi (Riches, 2001).

In Tanzania, A. vogelii is common in Mwanza, Shinyanga, Dodoma, Ismani and Ruvuma regions with yield losses of up to 50% (Mbwaga et al., 2000). The parasite is common in Lilongwe, Dowa and districts in central Malawi, the lower lying, drier areas of the southern region, and the Blantyre/Shire Highlands (Mainjeni, 1999; Riches and Shaxson, 1993). Introduced cowpeas are often very susceptible.

Cowpea is an inexpensive, high quality source of protein of major importance to the nutrition of poor rural households in sub-humid and semi-arid areas of sub-Saharan Africa (Singh et al., 2003) where improving food security and household income has proved difficult. Studies from these areas show a high incidence of poverty and associated problems such as malnutrition among under-5s (e.g. for Tanzania; World Bank, 2000; UNICEF, 2007). The nutritive value of cowpea grain and leaves (eaten as spinach) is high with crude protein contents ranging from 22 to 30% of dry weight (Bressani, 1985). A. vogelii infestation, through limiting yields, particularly of improved cultivars with a high yield potential, reduces the availability of pulse and leaf to families in semi-arid areas where diets are dominated by starchy foods such as millet, sorghum, maize and cassava and vegetables are in poor supply.

No uses of the plant have been reported. It will only grow in association with a host and is of no ornamental value.

Cultural Control

Two options, catch and trap-cropping, are available for reducing the size of the A. vogelii seed bank in the soil. Catch-crops are susceptible species which are ploughed in or harvested after parasite attachment but before emergence and seed production. A catch-crop of a cultivar of cowpea suitable for use as fodder has been recommended in South Africa (Hattingh, 1954). This would be cut and the roots destroyed by ploughing when about two months old and when A. vogelii was emerging. In a season of good rainfall, a quick-maturing crop of sunflower could then be grown with cowpea planted again in the following season. Trap-crops produce the Alectra germination stimulant in their root exudates but are not susceptible to attack by the parasite seedlings. In Botswana, grain or fodder cultivars of pearl millet and bambara, which is not attacked by the local biotype of the parasite, are potent stimulators of A. vogelii germination. These can be used in a rotation to cause suicidal germination of the parasite and hence reduce the number of seed in the soil (Parker and Riches, 1993).

Improved cowpea cultivars which combine resistance to A. vogelii, the related parasitic weed Striga gesnerioides, and several insect pests and fungal diseases have been developed in West Africa. These include the cultivars IT90K-76-6 and IT90K-82-2 which have been released for commercial production in Nigeria (Singh, 2000). These are not, however, resistant to biotypes of A. vogelii from southern Africa (Riches, 2001). The Botswana landrace accession B359 has been shown to be resistant to samples of the parasite from Botswana, Malawi and Kenya, so could be used as a parent for breeding improved cultivars for East and southern Africa (Riches et al., 1992; Riches, 2001). Fite (2009) reports on resistant landraces from Botswana, and finds that cultivars with thicker stems are negatively correlated with Alectra infection. Omoigui et al. (2012) identify some cowpea breeding lines with high resistance to both Striga  and Alectra infestation.

Potentially useful levels of resistance have also been demonstrated in germplasm of bambara (Riches et al., 1992) and cultivars of soyabean (Kureh and Alabi, 2003) but multi-location testing is needed to confirm the value of these lines in the field.

Karanja et al. (2012) suggest that application of farmyard manure may reduce the effect of Alectra parasitism on cowpea crops. Kwaga et al. (2010) report reduced incidence of Alectra on groundnuts when N fertilizer is applied.

Physical/Mechanical Control

Hand pulling and destruction of emerged stems before flowering may be useful where infestations are limited in extent, to prevent seed production and an expansion of the area infested. However, Beck (1987) found that hand pulling did not directly improve the yield of an infested bambara crop and this is likely to be the same for other susceptible species, as the majority of damage occurs before the parasite emerges above ground. Prompt ploughing of crop residues after harvest will prevent continued seed production as host plants continue to grow on residual moisture.

Biological Control

No research has been reported on the development of biological control agents for A. vogelii.

Chemical Control

A. vogelii is predominantly a pest of crops grown by resource-poor small-holder farmers who rarely have the finance to access herbicides. Little attention has therefore been given to the development of chemical control. The potential for controlling the weed by treating cowpea seed with the herbicide imazaquin before planting has been demonstrated but this practice has not been commercialized (Berner et al., 1994). Magani and Lagoke (2009) report that farmers can reduce cowpea infection by A. vogelii when preemergence herbicide mixtures containing pree (metazachlor + antidote) are applied, followed by post-emergence application of imazaquin at 0.18 kg a.i/ha.

IPM Programmes

Integrated control should be built around the use of resistant crop cultivars if possible, or choice of the least susceptible cultivar that is currently available. Timely destruction of legume crop residues is important to prevent parasite seed production after harvest and trap-crops should be included in the rotation to reduce the soil seed bank. Hand-pulling should be carried out on lightly infested areas, particularly in fields which have not previously had a history of infestation.