DOI: 10.1111/wre.12129
Rhamphicarpa fistulosa, a widespread facultative
hemi-parasitic weed, threatening rice production in
Africa
J RODENBURG*, J J MORAWETZ† & L BASTIAANS‡
*East and Southern Africa, Africa Rice Center, Dar es Salaam, Tanzania, †Rancho Santa Ana Botanic Garden, Claremont, CA, USA, and
‡Crop and Weed Ecology Group, Centre for Crop Systems Analysis, Wageningen University, Wageningen, The Netherlands
Received 20 May 2014
Revised version accepted 17 September 2014
Subject Editor: Maurizio Vurro, CNR, Bari, Italy
Summary
Rhamphicarpa fistulosa is a facultative hemi-parasitic
plant of the Orobanchaceae family, adapted to wet
soils. Apart from tropical Australia, it is only found
in sub-Saharan Africa, where it is considered a minor
weed in cereal crops such as rice. Due to this status,
the species has received only sporadic attention.
Recent field observations and encounters with rice
farmers in several African countries showed that
R. fistulosa is, however, a more serious and increasing production constraint than previously thought.
Results from a systematic literature review and a global herbarium study support this. The species has a
broad distribution over Africa (at least 35 countries
from Madagascar to Senegal and from Sudan to
South Africa) and a wide range in altitude (0–
2150 m a.s.l.) and environment (waterlogged swamps
to moist free-draining uplands). Rhamphicarpa fistulosa is relatively independent and persistent because
of the presumably wide host range, the facultative
nature of its parasitism and its prolific seed (estimated 100 000 seeds m 2 under moderate infestation
levels). Finally, R. fistulosa causes severe yield losses
(average 60%) and high regional annual economic
losses (estimated US $175 million), while effective
control options are scant and awareness of the species among important R&D stakeholders is almost
absent. An integrated approach is advocated to assist
the rice sector to reduce current R. fistulosa-inflicted
losses and to prevent further spread of the species
into new areas.
Keywords: rice vampire weed, inland valley, rain-fed
lowland, parasitic plant, integrated weed management,
subsistence farming, sub-Saharan Africa.
RODENBURG J, MORAWETZ JJ & BASTIAANS L (2015). Rhamphicarpa fistulosa, a widespread facultative hemi-parasitic weed, threatening rice production in Africa. Weed Research 55, 118–131.
Introduction
Rhamphicarpa fistulosa (Hochst.) Benth. (Orobanchaceae) is an annual, facultative hemi-parasitic forb species (Hansen, 1975; Ouedraogo et al., 1999). Although
much less well known than other weedy members of
Orobanchaceae, such as Striga Lour. spp., Orobanche
L. spp. and Phelipanche Pomel spp., it is a widespread
and common feature in the natural vegetation of
ephemeral wetlands (e.g. Hansen, 1975; Cisse et al.,
1996; Deil, 2005; M€
uller & Deil, 2005; M€
uller, 2007),
as well as in agro-ecosystems of tropical Africa, including cropping systems characterised by dryer soils
(Ouedraogo et al., 1999; Gworgwor et al., 2001; Rodenburg et al., 2011). The species is increasingly
encountered and perceived as a noxious weed in rice.
Correspondence: J Rodenburg, Africa Rice Center (AfricaRice), East and Southern Africa, P.O. Box 33581, Dar es Salaam, Tanzania. Tel: &
Fax: +
( 255) 222780768; E-mail: j.rodenburg@cgiar.org
© 2014 European Weed Research Society 55, 118–131
Rhamphicarpa fistulosa 119
Rice farmers and agricultural extension agents lack
knowledge on effective management strategies for this
species. This is mainly a result of the low awareness of
its existence and consequently the low priority it has
so far received for research and development (Schut
et al., 2014). Indeed, many knowledge gaps exist with
respect to R. fistulosa. There is an urgent need to
understand just how important the species is in terms
of its distribution, invasiveness and agronomic and
economic impacts. Secondly, effective management
strategies should be developed that prevent the species’
spread and reduce crop damage. Knowing the ecological and biological characteristics of the plant is of
utmost importance for the development of such strategies. While researchers, mainly botanists, have studied
and reported on R. fistulosa since 1835, when it was
first described and named, the information is scattered
and far from complete. A structured and co-ordinated
approach is advocated to complete the missing information and increase our understanding of this species.
To this end, we have reviewed all publicly available
publications and herbarium specimens of this species.
The objectives were to provide an overview of the current knowledge and understanding of the species’ distribution, biology, ecology, invasiveness, agronomic
and economic importance and management and to
identify and prioritise research questions. The overall
aim of this review was to alert decision and policy
makers and stakeholders of the emerging problem
caused by R. fistulosa and to prioritise and guide
research and development efforts aimed (i) at the control of this species where it has already turned into a
weed and (ii) at the prevention of spread into new
areas.
What do we know about the plant species
R. fistulosa?
Taxonomy, nomenclature and similarities to other
species
Rhamphicarpa fistulosa is an angiosperm species of the
Lamiales order, Orobanchaceae family (formerly
Scrophulariaceae; Olmstead et al., 2001) and the genus
Rhamphicarpa (Bentham, 1835; Hochstetter, 1841; Bentham, 1846; Engler, 1895; Hansen, 1975; Philcox, 1990;
Mielcarek, 1996; Fischer, 2004; Table 1). Its phylogenetic position is not yet completely confirmed, but the
species R. fistulosa has been placed under the tropical
clade of Orobanchaceae previously reported by Morawetz et al. (2010), with Fischer et al. (2012) showing
its closest relatives being the genera Sieversandreas Eb.
Fisch., Bardotia Eb. Fisch. Sch€
aferh. & Kai M€
ull. and
Randamaea Benth. The species R. fistulosa has a num© 2014 European Weed Research Society 55, 118–131
ber of local names in many of the countries where it
occurs as a weed in rice (see Table 1). Based on the
species’ parasitic nature and the most common host
crop species, rice vampire weed is proposed as the
common name of R. fistulosa.
Plants are erect and slender, simple-stemmed and
(mostly) glabrous, with smooth needle-like pale green
leaves, in opposite arrangement (Fig. 1A and B), and
can reach up to 120 cm height, depending on locality
(Philcox, 1990). The species is adapted to semi-aquatic
environments, with large (air) spaces between the cortical cells of the root aerenchyma to facilitate air flow
under submerged conditions (Neumann et al., 1997;
Ouedraogo et al., 1999).
Mature plants are branched and may turn reddish
(Fig. 1C). Flowers are white, cream, pale pink or pale
blue (the white form is most common in Africa)
(Fig. 1D) with long tubes (25–30 mm) that are straight
or slightly curved (Hansen, 1975; Fig. 1A and D). The
fruits are asymmetrical and neatly beaked (Fig. 1A
and B), about the size of a small pea, that is 6–15 mm
long and 4–7 mm broad, containing 100–250 dark
brown seeds. Seeds are oval shaped, 0.2 9 0.55 mm,
and the outer seed coat forms a reticulate network
covered by prominent ridges (Fig. 1A; e.g. Mielcarek,
1996; Ouedraogo et al., 1999) and weigh about
0.011 mg (Rodenburg et al., 2011). For complete
botanical descriptions, see Hansen (1975) and Ouedraogo et al. (1999).
Bentham (1835) was the first to describe a species
within this genus, that is Rhamphicarpa longiflora
Benth. Independently from this work, Hochstetter
(1841) named the genus Macrosiphon and described
two African species, M. fistulosus Hochst. and
M. elongatus Hochst. These are currently considered
synonyms of Rhamphicarpa fistulosa and R. elongata
(Hochst.) O.J. Hansen respectively (Hansen, 1975). In
total, 41 different names of species and subspecies (or
varieties) have been given to plants presumed to
belong to Rhamphicarpa, but many of them are no
longer accepted. For instance, Hooker (1884) and van
Steenis (1970) considered the African, Australian and
Indian species to be different. The Australian plants
were named R. australiensis Steen., but as van Steenis
did not compare this species to the African or Caucasian species, this name was not widely acknowledged.
In the literature prior to Staner’s (1938) revision, many
species that are currently considered to be part of the
genus Cycnium were classified as Rhamphicarpa; For
example, the hemi-parasitic Cycnium veronicifolium
(Vatke) Engl. used to be called Rhamphicarpa veronicifolia Vatke (Fuggles-Couchman, 1935; Parker &
Riches, 1993). The closely related genera Rhamphicarpa
and Cycnium are distinguished based on the form of
120 J Rodenburg et al.
Table 1 Taxonomy, scientific, common and local names of Rhamphicarpa fistulosa
Scientific name
Rhamphicarpa fistulosa
Authors
Common name
Family
Tribe
Order
Class
Synonyms
Hochstetter (1841), Bentham (1835, 1846), Engler (1895)
Rice vampire weed
Orobanchaceae (formerly: Scrophulariaceae)
Buchnereae (formerly Gerardieae)
Lamiales
Angiospermae – Dicotyledons
Macrosiphon elongatus Hochst.
Rhamphicarpa longiflora (Indian species most related to R. fistulosa) Benth.
Macrosiphon fistulosus (synonym of R. longiflora) Hochst.
Rhamphicarpa australiensis Steenis
Tutari (R. longiflora)
– India – Maharashtra state (Marathi)
Vernacular
names
Grassland trumpet or trumpet flower
(R. longiflora)
Kayongo
Otcha, Do, Corico, Efri
Mbosyo
Ntengo ya nchele nchele
Mulungi
Angamay
Mogogatau
^
Loho Soukoh/Soukoh lo
– India (English)
–
–
–
–
–
–
–
–
Uganda – Namutumba District (Lusoga)
Districts (Idaatcha)
Benin – Dassa, Glazoue
Tanzania – Kyela District (Nyakusa)
Tanzania – Mbinga District (Nyasa)
Tanzania – Ifakara (Kisajala)
Madagascar – Mid West (Malagasy)
Zambia – North (Tswana)
Cote d’Ivoire – North: Korhogo/Boundiali (Dioula/
Senoufo)
Sources: Hochstetter (1841), Bentham (1835, 1846), Engler (1895), von Wettstein (1891), Steenis (1970), Hansen (1975), Ouedraogo et al.
(1999), l’Herbier de Parc Botanique et Zoologique de Tsimbazaza, Antananarivo, Madagascar, Herbarium of the Department of Botany, University of Dar es Salaam, Museum National d’Histoire Naturelle, Paris, France (SONNERAT).
the capsules and the presence of a beak on their capsules; that is, oblique ovoid capsules with beaks
(Rhamphicarpa) compared with straight oblong capsules without a beak (Cycnium) (Staner, 1938). In fact,
the genus name Rhamphicarpa is a combination from
the Greek words for ‘beak’ or ‘bill’ and ‘fruit’.
Another distinctive feature is the stamen structure; that
is stamens arising at two levels in the corolla tube with
the style never exceeding the lower pair of stamens
(Cycnium) compared with stamens equal in length with
the style exceeding the stamens (Rhamphicarpa) (Philcox, 1990; Fischer, 1999; Leistner, 2005). Rhamphicarpa fistulosa can be confounded with Cycnium recurvum
(Oliv.) Engl. (previously named Rhamphicarpa recurva
Oliv. and R. tenuisecta Standl.), which has a similar
appearance and overlapping distribution in parts of
north-east and south-east Africa. However, the tube
of the corolla of C. recurvum is about a third of that
of R. fistulosa. Moreover, C. recurvum has a distinctly
different habitat, favouring dry conditions (Mielcarek,
1996). There is, however, still no conclusive evidence
that Cycnium and Rhamphicarpa are really separate
genera. A recent molecular phylogenetic study, the first
of this type to include Rhamphicarpa, seems to indicate
a much closer lineage with the Madagascan genera
Radamaea/Sieversandreas than with Cycnium (Fischer
et al., 2012). Further phylogenetic work will be
necessary to definitively determine the closest relatives
of Rhamphicarpa.
There are five other species accepted within Rhamphicarpa: R. longiflora Wight ex. Benth., R. elongata
(Hochst) O.J. Hansen, R. brevipedicellata O.J. Hansen,
R. capillacea A. Raynal and R. medwedewii Albov. The
latter species is only found in the Caucasus. The species
R. fistulosa is most often confused with R. longiflora,
but they differ in distribution; that is, R. longiflora is
only found in India. These two species can be distinguished by the form of the beak of their capsules: R. fistulosa has a straight beak, while the Indian R. longiflora
has an oblique beak (Bentham, 1846). Hansen (1975)
concluded that R. fistulosa is the correct name for the
species occurring in New Guinea, Australia, Madagascar and Africa, while R. longiflora is the Indian species
of this genus. This is still the currently accepted taxonomic division (Philcox, 1990; Mielcarek, 1996).
In Central Africa, R. fistulosa can be confounded
with R. capillacea, which also has long white flowers
and favours similar growth conditions (Raynal, 1970).
Rhamphicarpa capillacea can be distinguished from the
other Rhamphicarpa species by the leaves (entire for
R. capillacea compared with pinnatisect for the others)
and capsules (isodiametric for R. capillacea compared
with variable and never isodiametric for the others)
(Raynal, 1970; Hansen, 1975).
© 2014 European Weed Research Society 55, 118–131
Rhamphicarpa fistulosa 121
A
B
C
Fig. 1 (A) Drawing of Rhamphicarpa fistulosa, adapted from Hansen (1975),
showing habit (a), flower (b), capsule (c)
and seed (d); (B) R. fistulosa seed capsules, (C) close-up of the flower head with
flowers and capsules at different stages
and with reddish stem; (D) R. fistulosa
flower during daytime. Photographs were
taken by J Rodenburg.
Finally, R. fistulosa can be confounded with the
Striga spp. that have an overlapping host range
(mainly Striga hermonthica (Delile) Benth., S. asiatica
(L.) Kuntze or S. aspera (Willd.) Benth.). The morphological differences between the species are obvious (e.g.
Parker & Riches, 1993), but due to their parasitic nature and similarities in host crop ranges and geographic
distribution, local names given by farmers are often
the same for R. fistulosa and Striga spp. (e.g. ‘Kayongo’ in Uganda, ‘Otcha’ and ‘Do’ in Benin; Table 1).
Rhamphicarpa fistulosa is sometimes even referred to as
‘the Striga of rice’, even though both R. fistulosa and
Striga spp. parasitise rice. An important difference is
that Striga spp. are usually found on rice grown in the
free-draining uplands, whereas R. fistulosa mainly
parasitises rice in the water-logged lowlands and
hydromorphic zones, sometimes within the same
upland–lowland continuum (Kabiri et al., 2015).
A facultative root hemi-parasite
Rhamphicarpa fistulosa roots develop haustoria like
other parasitic plants such as Striga spp. and Orobanche spp. (Parker & Riches, 1993; Press & Graves,
1995). While Striga species develop terminal and
© 2014 European Weed Research Society 55, 118–131
D
lateral haustoria, R. fistulosa, like other facultative
parasites such as Rhinanthus minor L. (Seel et al.,
1993; Cameron & Seel, 2007) and Buchnera hispida
Buch.–Ham. Ex. D. Don, (e.g. Neumann et al., 1997,
1999), only develops lateral haustoria that bridge the
parasite and host root xylem (Kuijt, 1969; Neumann
et al., 1998, 1999). About three to four weeks after
sowing of the host plant, upon contact between the
parasite and the host root, the parasite starts to
develop haustoria. The haustorium initiation starts
with the development of tiny hairs around the area of
outgrowth, which sometimes facilitate the attachment
of the parasite with the host root (Neumann et al.,
1998). If the host root and the parasite root are parallel to each other, the parasite root can develop multiple haustoria. Without a host in its vicinity, the
parasite does not develop any haustoria, indicating
that some morphogenic host root factors are involved
in the host detection of the parasite. Upon establishment of a xylem-to-xylem connection, the parasite can
extract host metabolites, nutrients and water from its
host (e.g. Aly, 2013). In some cases, phenolic substances or lignins can be observed on the host roots
where the parasite attempts to penetrate, indicating the
existence of a host plant defence reaction (Neumann
122 J Rodenburg et al.
et al., 1999). Rhamphicarpa fistulosa uses the C3 pathway for CO2 assimilation (Press et al., 1987), but plants
are pale green (both stem and leaves), which suggests a
low chlorophyll content and consequently suboptimal
CO2 assimilation levels, explaining the species’ need for
host metabolites. The biomass accumulated by a parasitising R. fistulosa plant is usually much smaller than the
biomass lost by the affected host plant (Rodenburg
et al., 2011). This would point to a phytotoxic mechanism, but the existence of such a pathological effect is
not yet confirmed (Rodenburg et al., 2010).
The host range of R. fistulosa has not yet been fully
established. Apart from cereal crops such as maize,
millet and rice (Bouriquet, 1933; Kuijt, 1969; Cisse
et al., 1996; Ouedraogo et al., 1999), it has been
reported to parasitise groundnut (Arachis hypogaea L.;
Bouriquet, 1933) and cowpea (Vigna unguiculata (L.)
Walp.), although the latter report concerned R. veronicifolia Vatke (= Cycnium veronicifolium (Vatke)
Engl.) rather than R. fistulosa (Fuggles-Couchman,
1935). Supposedly it can also parasitise wild grasses
(Poaceae) and members of the Cyperaceae, Leguminosae and Labiatae families (Bouriquet, 1933). Although
other facultative hemi-parasites such as Rhinanthus
minor are able to parasitise both grasses and legumes
(Cameron & Seel, 2007), parasitic plant species typically parasitise either monocotyledons or dicotyledons;
hence, these reports need to be confirmed.
Reproduction and seed biology
Flowers are white and fragrant, only open at dusk and
usually last only one night, after which they fall off
(Cisse et al., 1996). Plants growing without a host
develop fewer flowers (often just one or very few) than
plants having successfully established a parasitic relationship with a suitable host (Ouedraogo et al., 1999).
The reproductive biology of R. fistulosa is unclear.
Some reports mention cross-pollination by night moths
(Parker & Riches, 1993; Cisse et al., 1996; Ouedraogo
et al., 1999), perhaps mainly due to the shape of the
corolla that is compatible with hawk-moth pollination
(e.g. Fischer et al., 2012) and the fact that the flowers
only open between sunset and sunrise. However, viable
seeds have been produced in the absence of such insects
in controlled screen house environments (A van Ast,
pers. comm.). The species may produce well over 1000
small seeds per plant. As densities above 100 plants per
m2 are not unusual (N’cho et al., 2014), seed production may easily exceed 100 000 seeds per m2.
Little is known about seed longevity under natural
conditions, but according to Gbehounou and Assigbe
(2004), seeds are short-lived (approximately 1 year).
Seeds of R. fistulosa have a dormancy period of six
months and require water and daylight for germination
(Ouedraogo et al., 1999). Contrary to other parasitic
Orobanchaceae, seeds of R. fistulosa do not require
pre-conditioning for germination (A van Ast, pers.
comm.). Moreover, in contrast to obligate parasitic
plants (e.g. Striga spp.), the seeds of the facultative
hemi-parasitic R. fistulosa do not need a host-derived
stimulant for germination (Ouedraogo et al., 1999;
Gbehounou & Assigbe, 2004). Germination occurs
within about 4 days, when the conditions are favourable. Two to three days after germination, the green
cotyledons emerge, after which the seedling starts to
develop leaves. Rhamphicarpa fistulosa usually has a
low initial growth rate (J Rodenburg, pers. obs.).
Flowering and maturity times seem to vary with
growing conditions. Ouedraogo et al. (1999) reported
initiation of flowering around 140 days after sowing
(DAS) in trials in Burkina Faso, but an earlier onset
of flowering (around 70–100 DAS) has been observed
in trials in Benin and Tanzania (J Rodenburg, pers.
obs.). Plants of R. fistulosa can continue growth and
reproduction beyond the harvest of the crop, provided
that there is enough residual soil moisture.
Where and under what conditions can we
find R. fistulosa?
Biotic and abiotic environment
Rhamphicarpa fistulosa thrives in wet and semi-aquatic
environments in forest and savannah zones (e.g. Cisse
et al., 1996). It can grow in peaty soils over rock substratum, on or between rocks in shallow, slow running
streams, but more frequently in grassy swamps, temporary or permanently flooded areas such as inland valley swamps and poorly drained rain-fed lowland rice
fields (Hansen, 1975; Philcox, 1990; Ouedraogo et al.,
1999). In areas where rice, the most common host of
R. fistulosa, is grown along the upland–lowland continuum, the weed is only found in the lower, seasonally
flooded zones (Kabiri et al., 2015), although recently,
we have observed it on higher parts as well (J Rodenburg, pers. obs.). Soils favouring R. fistulosa are generally poor in N, P and K with relatively high silt
content (Ouedraogo et al., 1999; Kabiri et al., 2015),
which would imply a high degree of salinity tolerance.
The exact range of salinity tolerated needs to be
confirmed.
Fungi (i.e. Fusarium spp., Sclerotium rolfsii) and
bacteria (i.e. Stenotrophomonas maltophilia, Bacillus
pumilus, B. megaterium) have been observed as pathogenic to R. fistulosa (Sikirou et al., 2002a). The species
is also attacked by beetles and caterpillars. The
Nymphalid caterpillar Junonia spp. has frequently been
© 2014 European Weed Research Society 55, 118–131
Rhamphicarpa fistulosa 123
observed on R. fistulosa plants and is able to feed on
all the above-ground plant tissue (J Rodenburg, pers.
obs.). The Coleoptera (beetle) Smicronyx spp. (Curculionidae) has also been observed to cause foliar damage
to R. fistulosa plants and to lay eggs in the seed capsules (Sikirou et al., 2002a). The larvae of these beetles
feed on the immature seeds in the capsule and make
the capsule look swollen (J Rodenburg, pers. obs.).
Rhamphicarpa fistulosa has been observed to co-occur
with other parasitic weeds, such as Alectra vogelii
Benth., Striga asiatica, S. aspera and S. hermonthica in
Guinea (Cisse et al., 1996), Striga aspera in Burkina
Faso (Salle et al., 1994), Striga asiatica in Tanzania
(Johnson et al., 1998; Kayeke et al., 2010; Kabiri et al.,
2015) and Madagascar (M Cissoko & A P Andrianaivo,
pers. comm.), and S. hermonthica in Mali, Burkina Faso
(Salle et al., 1994) and Uganda (J Rodenburg, pers.
obs.). Rhamphicarpa fistulosa is, however, rarely
observed with any of these species in the same crop, due
to its distinct environmental niche (Kabiri et al., 2015).
The species has been indicated as characteristic of
the West African class of mud vegetation: Rhamphicarpo fistulosae-Hygrophiletea senegalensis (Deil, 2005;
M€
uller & Deil, 2005). Observed associated wild plant
or weed species are: Parahyparrhenia annua (Hack.) W.
D. Clayton, Sacciolepis microcorra Mez., Panicum spp.
or wild rice (Oryza spp.) in Senegal, Burkina Faso and
Mali (Ouedraogo et al., 1999) and Ammania auriculata
Willd., Oryza longistaminata A. Chev. & Roehr., Scleria vogelii C. B. Clarke, Fimbristylis littoralis Gaudich.
and Mariscus longibracteatus Cherm. in a field survey
in southern Tanzania (Kabiri et al., 2015). Whether or
not any of these plants are also parasitised by R. fistulosa is not known.
Geographic distribution
The genus Rhamphicarpa is spread over four subareas:
(i) sub-Saharan Africa and Madagascar, (ii) India, (iii)
New Guinea and tropical Australia and (iv) the Caucasus. It is not clear yet how the genus could have spread
to such discontinuous and remote places. It was
hypothesised by Hansen (1975) that the genus Rhamphicarpa originated in Africa and that R. fistulosa represents the ancestral stock, as this species is the most
widely distributed and the only taxon that is found in
more than one subarea. From Africa, the genus may
have spread to other areas, while subsequent environmental changes (e.g. in climate) may have caused a
break-up of the original distribution to the currently
observed discontinuous subareas.
Rhamphicarpa fistulosa is a very widespread species
in tropical Africa (Staner, 1938; M€
uller, 2007).
Combining a literature study with a search in national
© 2014 European Weed Research Society 55, 118–131
and international herbaria and our own field observations, we retrieved 392 observations, 378 of which can
be traced back to geo-coordinates and 348 of which
seemed to be unique individual observations/specimens. They are collected from 35 countries (Table 2),
and the distribution of the species’ observations is
shown in Fig. 2. From two countries, the Gambia and
Egypt, we only found a reference in the literature (i.e.
Mielcarek, 1996), but no actual herbarium specimen or
concrete observation with a name or geo-reference to
the location. Liberia, Sierra Leone, Equatorial Guinea,
Eritrea, Somalia and Comoros are the most remarkable absentees of the list of countries where R. fistulosa
was observed, as these countries are located within the
species’ distribution zone. Apart from the possibility
that this species does indeed not occur in these countries, the absence of any herbarium record may simply
be a symptom of an incomplete national flora inventory or a weak national research infrastructure, which
may be a result of recent turbulent histories, characterised by political instability and armed conflicts. The
altitude of collections or observations ranged from 2
to 1750 m a.s.l. (average: 536 m), the latitude ranged
from 28.72 to 19.25 degrees, and the longitude ranged from 16.85 to 49.97 degrees (Fig. 2). Previously,
R. fistulosa distribution in Africa was assumed to be
restricted to sub-Saharan regions, below 17°N, but our
herbarium and literature search provided indications
that the species can be found in more northern parts
of Africa, as well. Outside Africa, it is reported in New
Guinea and Australia (USDA, 2013), notably the
northern tropical areas of Queensland (Martin, 2000).
Means of spread
Rhamphicarpa fistulosa seeds are minute and can
adhere to crop seeds harvested from infested fields; if
these seeds are then marketed, they can be introduced
to previously uninfested fields when they are sown.
Other likely means of introduction are through flood
water, as R. fistulosa is mostly found along streams or
in temporary flooded areas, and by wild or domesticated animals, for example free-roaming cattle in
infested fields. The latter is a commonly observed a
feature in the agricultural systems where R. fistulosa
constitutes a weed problem (J Rodenburg, pers. obs.).
Seeds are transported in the fur or hooves of the animals or ingested by animals feeding on crop residues
at one place and deposited in their droppings in
another place. Such means of dispersal is believed to
be over relatively short distances, that is the typical
distances these cattle cover. Although no published
studies are available on seed dispersal for R. fistulosa,
the above-mentioned processes have been reported as
124 J Rodenburg et al.
Table 2 Rain-fed rice area, yields, total production and Rhamphicarpa fistulosa-inflicted economic losses in African countries where
R. fistulosa was reported, sorted in decreasing order of magnitude
Country
Total area
of rain-fed
lowlands rice
systems (ha)*
Average estimated
yield from rain-fed
lowlands (t ha 1)†
Estimated milled
rice production
from rain-fed
lowlands (tonnes)‡
Estimated minimum
annual economic
loss caused by
R. fistulosa (US $)§
Estimated maximum
annual economic
loss caused by
R. fistulosa (US $)§
Nigeria
Tanzania
Madagascar
Cote d’Ivoire
Guinea
Mali
Ghana
Mozambique
Uganda
Burkina Faso
Guinea-Bissau
Chad
Cameroon
Senegal
Malawi
Togo
Benin
Gambia
DRC
Zambia
Burundi
Angola
Niger
Ethiopia
Sudan
Congo
CAR
South Africa
Kenya
Gabon
Zimbabwe
Total
1 032 935
677 806
322 688
314 863
381 756
134 851
129 533
73 954
72 109
61 743
47 521
37 734
19 635
43 948
28 338
27 876
23 552
25 231
28 021
11 775
7778
6036
4727
2811
1438
1008
2731
572
414
258
145
3 523 787
3.02
1.89
1.71
1.61
1.10
2.85
1.16
1.89
1.89
1.71
1.89
1.89
3.2
1.22
1.89
1.89
1.83
1.28
0.88
1.89
1.89
1.89
1.89
1.89
1.89
1.89
0.53
1.89
1.29
1.89
1.89
1.79
1 871 678
768 632
331 078
304 158
251 95
230 595
90 155
83 864
81 772
63 348
53 889
42 790
37 699
32 170
32 135
31 611
25 860
19 377
14 795
13 353
8820
6845
5360
3188
1631
1143
868
649
320
293
164
4 410 201
17
7
3
2
2
2
123
50
21
20
16
15
5
5
5
4
3
2
2
2
2
2
1
1
293 049
101 643
058 937
810 212
327 931
130 545
832 971
774 845
755 515
585 296
497 896
395 354
348 315
297 229
296 909
292 068
238 930
179 034
136 697
123 371
81 493
63 242
49 527
29 452
15 066
10 561
8024
5993
2961
2703
1519
40 747 288
521
726
849
072
628
218
949
534
396
180
556
823
487
123
120
086
706
278
976
881
582
451
353
210
107
75
57
42
21
19
10
291 052
778
023
551
945
082
177
795
611
533
685
403
958
966
061
775
200
642
816
405
224
094
726
762
371
618
437
314
808
147
308
852
067
*Estimates from Diagne et al. (2013a).
†Estimates for 18 countries derived from Diagne et al. (2013a); where national yield figures are not provided, the average yield from the
18 countries (1.89 t ha 1) was used.
‡rice area multiplied by paddy yield per area and a paddy to milled rice conversion factor of 0.6.
§Milled rice production multiplied by the estimated proportion of R. fistulosa-infested lowlands (22%), the estimated proportion of
infested fields in infested lowlands (72%), the estimated minimum or maximum R. fistulosa-inflicted yield loss in these infested fields (14
and 100%, respectively) and the most current world rice price (June 2014: US $416.64 per tonne). Based on the average yield loss
(60%), the annual economic loss would be $175 million.
possible contamination pathways for other parasitic
weeds (Jacobsohn et al., 1987; Berner et al., 1994).
What is the impact of R. fistulosa on rice
in Africa?
Agronomic impact
In north-eastern Nigeria (Adamawa, Borno, Jigawa,
Bauchi, Gombe and Yobe states), R. fistulosa occurred
in 48% of the 65 surveyed locations (each sampling
area was 1 km2, comprising both farmland and natural
vegetation) and was classified as ‘abundant’ (Gworgwor et al., 2001). In neighbouring Benin, an estimated
22% of the inland valleys where rice is grown were
infested by R. fistulosa (Rodenburg et al., 2011), and
in another survey in Benin, R. fistulosa was found in
72% of the rice fields in an infested inland valley
(N’cho et al., 2014). When R. fistulosa invades a rice
crop, resulting yield losses are generally high. The
weed will parasitise the rice, removing metabolites,
water and nutrients from it and presumably exerting a
negative effect on its hormone regulatory system. The
result is stunted growth of rice and reduced grain pro© 2014 European Weed Research Society 55, 118–131
Rhamphicarpa fistulosa 125
Fig. 2 Distribution of Rhamphicarpa fistulosa in Africa, based on the literature
(see References), national and international herbaria (see Acknowledgements)
and field observations of the authors and
co-workers. Locations where R. fistulosa
has been observed or herbarium specimen
have been collected are indicated by black
dots; national paddy production (tonnes)
estimates from rain-fed lowland rice
(derived from area and yield figures provided by Diagne et al., 2013a), which may
be impacted by R. fistulosa, are indicated
by shading (see legend).
duction. In R. fistulosa-infested rice fields, yield losses
can be as high as 100%, as observed in Benin (Sikirou
et al., 2002a; Gbehounou & Assigbe, 2003) and in
Tanzania (Kayeke et al., 2010). The effect of R. fistulosa is also obvious from some of the local names it
received from farmers, for example ‘Efri’ meaning ‘killing’ (Rodenburg et al., 2011), ‘Otcha’ referring to
‘viper’ (poisonous snake) and ‘Do’ meaning ‘crop
killer’ (Table 1; Gbehounou & Assigbe, 2003). Pot
experiments showed a range of 14–78% R. fistulosainflicted grain losses, depending on rice variety and
infestation level, while in infested fields in Benin, rice
farmers estimated the average yield losses at 60%
(Rodenburg et al., 2011). This average is much higher
than estimated yield losses caused by non-parasitic
weeds. For comparison, in a large survey held among
rice farmers from 21 African countries, farmers growing rice in rain-fed lowlands who indicated weeds to be
a problem, estimated weed-inflicted yield losses in rainfed lowland rice around 36%, with a maximum average estimate of 43% in Kenya and 40% in Cote d’Ivoire (Diagne et al., 2013b).
Economic impact
Of the 35 countries where the species is found, at least
31 have rainfed lowland rice production systems,
which, based on the most recent and accurate
© 2014 European Weed Research Society 55, 118–131
estimations (see Diagne et al., 2013a; data on Sudan
and South Sudan are combined) annually produce
about 7.35 M tonnes of paddy (4.41 M tonnes of
milled rice), worth around US $1.84 billion. If R. fistulosa can be found in 22% of the rice grown inland
valleys, and in 72% of the rice fields in such valleys,
and given an average R. fistulosa-inflicted yield loss of
60% (ranging from 14% to 100%), the current annual
economic losses in sub-Saharan Africa are estimated at
US $175 million (with a range from US $41 to 291
million; see Table 2). This is 9.5% of the total estimated value of the regional rain-fed lowland rice production. This estimate will become more accurate,
once additional data are available.
Social impact
Infestation by R. fistulosa can be considered a poorman’s problem. The parasitic weed is primarily problematic on marginal arable land, that is on low fertility
and poorly drained soils, where water cannot be controlled (e.g. N’cho et al., 2014). These are the typical
crop production conditions of resource-poor subsistence farmers, with a high proportion of female farmers (N’cho et al., 2014; Rodenburg et al., 2014). The
weed has clear negative economic impacts and requires
the farmer to invest valuable time for weeding (S.
N’cho, pers. comm.). Weeding is often performed by
126 J Rodenburg et al.
women and children and consumes time that could
otherwise be invested in family welfare and education
(Ogwuike et al., 2014). Sometimes heavily infested
fields are abandoned by the farmer (e.g. Rodenburg
et al., 2011).
Little is known about the economic, social or environmental value of R. fistulosa. The species has been
observed locally (in central Benin) being used as an
insect repellent. Fresh plants were burned in a portable
stove to produce smoke that was believed to repel (biting) insects such as mosquitoes (J. Rodenburg, pers.
obs.). The plant was also reported to have medicinal
uses in Machipi (near Ifakara), Kilombero District,
Tanzania (EAH, 2013).
How can we stop the future spread of
R. fistulosa and reduce current damage?
Prevention
As with other parasitic weeds of the Orobanchaceae
family, the spread of R. fistulosa via their minute seeds
can be prevented through basic phytosanitary measures. This means that any possible vectors that move
seeds from an infested area should be controlled as
much as possible (e.g. Rubiales et al., 2009; Goldwasser & Rodenburg, 2013). Farm implements should be
cleaned before using them in another field. Cattle
movement between contaminated and clean fields
should be avoided. Fields should be bunded to prevent
seed movement from one field to another in water following uncontrolled floods and crop seeds should be
cleaned before sowing. To prevent a seedbank build-up
in a given field in a contaminated area, the crop should
be regularly weeded (at least before flowering), so that
weeds are removed from the field, both during the season and between seasons during any fallow period.
Control
The main weed management practices by rice farmers
in Benin, Cote d’Ivoire and Tanzania with parasitic
weed infested rice fields (including R. fistulosa and
Striga spp.) are, in decreasing order of frequency: hand
weeding, hand-hoe weeding, soil fertility management,
herbicide use, water control, use of clean seeds, transplanting and the use of resistant or tolerant rice varieties (S. N’cho pers. comm.).
Rhamphicarpa fistulosa can be controlled with the
post-emergence herbicide 2,4-D (Gbehounou & Assigbe, 2003). Fertiliser has a proven suppressive effect
on R. fistulosa and a positive effect on rice yields of
R. fistulosa-infected plants (Sikirou et al., 2002b;
Rodenburg et al., 2011). Resource-poor rice farmers
could use rice husks, which are often freely available,
as it may reduce negative effects of R. fistulosa infestation on yield (Kayeke et al., 2013). Genetic variation
in resistance and tolerance levels (Rodenburg et al.,
2011), as well as in weed competitiveness (Rodenburg
et al., 2009), was observed among adapted lowland
rice cultivars, and these could be useful in R. fistulosainfested rice fields. For resource-poor farmers, the
availability of improved rice varieties may, however,
be limited. It is also hypothesised that improved water
management, enabling either drainage or continuous
flooding, can reduce R. fistulosa abundance (Parker &
Riches, 1993; Parker, 2012). Permanently flooded conditions, starting at the early stages of the crop, will
contribute to reduced R. fistulosa plant numbers (van
‘t Klooster, 2011). Indeed, R. fistulosa has never been
reported in irrigated rice systems where water is fully
controlled. As R. fistulosa is particularly problematic
in direct seeded rice (Johnson et al., 1998), transplanting is also likely to have a positive effect on rice performance in infested fields (Gbehounou & Assigbe,
2003). It will give the crop a time advantage over the
weed, thereby rendering it more competitive. It has
the additional advantage of facilitating hand weeding,
the spot application of post-emergence herbicides or the
use of a rotary weeder (e.g. Rodenburg & Johnson,
2009). Timing of planting is also reported to be important (Langeloo, 2013; Rodenburg et al., 2013). However, whether or not early or late sowing is
advantageous most probably depends on the local
environmental conditions, in particular the hydrology
and rainfall distribution. Exact relationships between
environmental conditions, timing and parasitism
should therefore be further investigated. An integrated
management strategy against R. fistulosa, combining
any of the above measures, is generally considered the
most effective and sustainable solution (e.g. Salle et al.,
2000; Kayeke et al., 2010; Goldwasser & Rodenburg,
2013).
Discussion
Rhamphicarpa fistulosa: an increasing problem
Rhamphicarpa fistulosa is a widespread and rather
common species of natural wetland vegetation in
Africa (e.g. Deil, 2005; M€
uller & Deil, 2005; M€
uller,
2007). Salle et al. (1994) observed the species to occur
more frequently in natural vegetation than in crops.
Indeed, for parasitic plants in general, the natural geographical range is usually much larger than their geographical range as a weed (Raynal Roques, 1994). This
also seems to be the case for R. fistulosa. From the
aforementioned herbarium study, many of the
© 2014 European Weed Research Society 55, 118–131
Rhamphicarpa fistulosa 127
specimens were collected from national parks and nature reserves or otherwise uncultivated areas. From
only 10% of the specimens or observations, we are
sure that the plants were found in a rice field. We estimate that of the remaining 90% of specimens for
which it was not indicated whether it was found in a
rice crop, about 50% were collected from locations
with at least a close vicinity to rice production sites
and about 40% was likely not close to a rain-fed rice
production area.
We hypothesise that when the natural habitats of
R. fistulosa are turned into agricultural production
sites, with a suitable host grown as a monoculture in a
high density, the spontaneously occurring population
of the species can rapidly increase, transforming the
species into an agricultural pest (Bouriquet, 1933; ,
Akoegninou et al., 1999; Gbehounou & Assigbe,
2003). The only major staple crop that can be grown
across the range of environments where R. fistulosa is
observed, that is from hydromorphic to waterlogged
soils, is rice. Rice is an increasingly important crop in
sub-Saharan Africa. To keep pace with the increasing
regional rice consumption, about 30 million tons more
rice will be needed by 2035 (Seck et al., 2012). Part of
the increase in production will likely come from expansion into areas previously unused for agriculture. Lowlying areas, such as inland valleys, with a relatively
favourable hydrology and soil fertility, constitute highpotential areas for rice production and are likely to be
increasingly exploited for that purpose (Rodenburg
et al., 2014). Intensification of rice production in these
ecosystems may be threatened by infestations of R. fistulosa (Johnson et al., 1998). Given its widespread distribution, the species is poised to become an even more
serious parasitic weed throughout the continent.
We assume, based on the descriptions of its habitat
(Hansen, 1975) and our own observations in the field,
that R. fistulosa will in particular invade rain-fed lowland rice growing environments. However, the species
was shown to have a relatively broad ecological niche
(Kabiri et al., 2015), and we have recently observed it
in the undulating landscape of Namutumba District
(Ivukula village) in Uganda on the top of a hill in a
free-draining upland rice field. In the same district, it
has been found in maize fields as well. Ouedraogo
et al. (1999) also reported this species in agro-ecosystems other than rain-fed lowlands. Hence, R. fistulosa
seems to have a reasonably high degree of ecological
plasticity.
Rhamphicarpa fistulosa remains a relatively
unknown species among local extension and research
(Schut et al., 2014) and therefore often goes unnoticed
(as we observed in Benin, Cote d’Ivoire, Madagascar,
Senegal, Tanzania and Uganda). The species is also
© 2014 European Weed Research Society 55, 118–131
easily overlooked because the flowers are only opening
at sunset (Cisse et al., 1996). The actual extent of the
problem of R. fistulosa in rain-fed lowland rice in subSaharan Africa is therefore expected to be largely
underestimated. Recent observations in West Africa
indicate the species is spreading. Rodenburg et al.
(2011) observed an increase in the number of infested
inland valleys growing rice over a period of about
10 years. In Cote d’Ivoire, farmers indicated an
observed general increase of the species in the period
2008–2012 (S N’cho, pers. comm.). In Senegal in 2008,
R. fistulosa was observed in a rice field in the Casamance, south of the Gambia (J Rodenburg, pers.
obs.), where it had not been observed previously during annual surveys from 1985 to 1996 (Ouedraogo
et al., 1999). For the farmer of the aforementioned
highly infested upland rice field in Ivukula, Namutumba District, Uganda, R. fistulosa was a completely
new species three years ago when he observed the first
invasive individuals. Similarly in Madagascar (Tsiroanomandidy, Bongolava region), farmers indicated
new infestations of R. fistulosa in their rice fields during recent years (M Cissoko and A P Andrianaivo,
pers. comm.).
Future research topics
Since its description by Bentham in 1835, the taxonomy, biology, ecology and agronomic importance of
Rhamphicarpa fistulosa has been only infrequently
studied. The species therefore remains relatively
unknown and many knowledge gaps still need to be
filled. Increased awareness and knowledge is required
for the development and implementation of control
strategies to prevent the species from becoming a more
important constraint to food production in sub-Saharan Africa. Ten important research topics are listed
below:
Within the domain of invasive plant ecology and
environmental studies, (i) the invasiveness of R. fistulosa needs to be studied to ascertain whether the distribution is increasing, stable or decreasing. Furthermore,
(ii) the main distribution mechanisms and the history
of the spread of the genus over the discontinuous
subareas would need to be clarified. Related to that,
(iii) the altitude and environmental plasticity need to
be confirmed, as well as the soil chemical ranges of the
R. fistulosa habitat, with special focus on salinity and
acidity tolerances. These all seem to be important
parameters to infer the likely spread of the species.
Next, within the economic science domain, (iv) our
best-bet economic loss estimate of US $175 million per
year should be revised using updated figures on
R. fistulosa incidences and yield losses in rain-fed rice
128 J Rodenburg et al.
systems per country with local rice prices and using
solid spatial and economic models. This is important
for priority setting of research and developments
efforts, as well as for raising awareness of the problem.
Within the domain of taxonomy, plant physiology and
crop sciences, (v) the host–parasite and damage mechanisms need to be elucidated, as it remains unclear
whether this can purely be defined as a sink-source
relation or whether R. fistulosa negatively affects the
host plant hormone balance and through that, the host
metabolism and growth, as with Striga spp. Another
fundamental issue, (vi) the distinction between Cycnium and Rhamphicarpa, requires further study, probably
using molecular analyses. Next, (vii) the parasitic nature, the biology and ecology of other species of the
genus Cycnium and Rhamphicarpa should be investigated, as other species from these families could potentially emerge as important parasitic weeds as well,
(viii) the host range of R. fistulosa (and other parasitic
species of Rhamphicarpa and Cycnium) needs to be
confirmed, as it will determine whether crop rotations,
inter- or relay cropping are useful control methods,
and which species should then be used. Related to
that, (xi) feasible control strategies for rice farmers
need to be further investigated and developed. In particular, the timing of crop and weeding operations and
soil fertility management seems to be promising avenues to explore further. Another potentially interesting
control option is the use of resistant or tolerant host
crop varieties. To explore and use this option (x) the
host resistance and tolerance mechanisms and responsible genes need to be identified and possibly transferred to adapted cultivars.
Conclusions
Rhamphicarpa fistulosa (rice vampire weed) is a widespread facultative hemi-parasitic weed, threatening rice
production in Africa. Based on a literature and herbarium study, we conclude that R. fistulosa is an important rice production constraint in some areas,
particularly in subsistence rice production systems, and
poses a strong threat for rice production in other areas
in Africa. The species has a broad distribution over
tropical Africa, occurring in at least 35 countries geographically spread from eastern Madagascar to western
Senegal and from Sudan to South Africa. In addition
to the wide geographic range, R. fistulosa has been
observed at widely varying altitudes, from sea level to
an estimated 1750 m a.s.l., and under a range of ecological conditions, from waterlogged swamps to
(moist) free-draining uplands. Combined with a presumably wide host range, the facultative nature of its
parasitism and prolific seed production, the plant has a
putative high degree of ecological plasticity. While the
weed has very significant effects on rice productivity
when present, farmers and even extension services are
generally unaware of effective and affordable control
options. Despite the wide distribution and severe economic consequences (an estimated annual loss of US
$175 million), awareness of the species among research,
extension and development stakeholders is largely
lacking.
A systematic and integrated approach is advocated
to assist farmers and other stakeholders in affected
areas to reduce current losses due to this parasitic
weed and to prevent future spread into other areas.
Important knowledge gaps concerning the species’ taxonomy, biology, ecology, parasitic nature, invasiveness
and economic impact need to be filled. This will enable
informed development of effective integrated control
and prevention strategies and form the necessary bedrock for increasing the awareness among a wider range
of stakeholders and actors within research, development, education and policy domains.
Acknowledgements
The authors gratefully acknowledge the assistance of
the following herbaria (and curators): Kew Royal
Botanic Gardens (David J. Goyder); South African
National Biodiversity Institute (Brenda Daly); Missouri Botanical Garden (George Schatz, Pete Lowry,
James C. Solomon), MBG’s TROPICOS database;
Museum National d’Histoire Naturelle (SONNERAT);
l’Herbier de Parc Botanique et Zoologique de Tsimbazaza, Antananarivo, Madagascar (Solo Rapanarivo, Frank Rakotonasolo); l’Herbier du DBEV,
Universite d’Antananarivo (Cathy Madiomanana, Verohanitra Rafidison); National Herbarium of Rwanda
(Minani Vedaste); Herbarium of the Department of
Botany, University of Dar es Salaam (Frank Mbago);
East African Herbarium, National Museums of Kenya
(Itambo Barnabas Malombe); as well as technical
assistance from Runyambo Irakiza, Derek Makokha,
Mamadou Cissoko (AfricaRice) and Alain Paul Andrianaivo (FOFIFA). Sander Zwart and Justin Djagba
(AfricaRice) are kindly acknowledged for their assistance in the production of the distribution map. We
also thank Lytton John Musselman (Old Dominion
University) for sharing valuable information with us
and Aad van Ast (Wageningen University) for proofreading our manuscript. This study forms part of the
PARASITE project, funded by the Integrated Programmes Scheme of the Netherlands Organisation for
Scientific Research – Science for Global Development
(NWO-WOTRO; grant number W 01.65.327.00).
Additional support is provided by the CGIAR
© 2014 European Weed Research Society 55, 118–131
Rhamphicarpa fistulosa 129
Research Program on Climate Change, Agriculture
and Food Security (CCAFS) and the National Science
Foundation (DEB1119801 to JJM).
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