Rhamphicarpa fistulosa, a parasitic weed threatening rain-fed lowland rice production in sub-Saharan Africa – A case study from Benin

Crop Protection 30 (2011) 1306e1314

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Rhamphicarpa fistulosa, a parasitic weed threatening rain-fed lowland rice production in sub-Saharan Africa e A case study from Benin Jonne Rodenburg a, *, Norliette Zossou-Kouderin b, Gualbert Gbèhounou c, Adam Ahanchede b, Amadou Touré d, Gerald Kyalo a, Paul Kiepe a a

Africa Rice Center (AfricaRice), East and Southern Africa Rice Program (ESARP), P.O. Box 33581, Dar es Salaam, Tanzania Faculté des Sciences Agronomiques, Université d’Abomey-Calavi, 01 BP 526 Cotonou, Benin FAO, Plant Production and Protection Division, Viale delle Terme di Caracalla 00153 Rome, Italy d Africa Rice Center (AfricaRice), 01 BP 2031 Cotonou, Benin b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 9 November 2010 Received in revised form 27 June 2011 Accepted 27 June 2011

Expansion of the facultative parasitic plant Rhamphicarpa fistulosa as a weed of rain-fed lowland rice was studied in 2007 on a national level (Benin) by repeating a survey from 1998. Wider species’ distribution was investigated in 2008. Current and potential impact and management strategies were investigated through farmer surveys and pot experiments. Out of 36 cultivated inland valleys visited across Benin, eight were found to be infested with Rhamphicarpa. Out of nine inland valleys inspected in 1998, Rhamphicarpa was found in five in 2007, compared with only three in 1998. Farmers estimated Rhamphicarpa-inflicted yield losses could exceed 60% and indicated that heavily infested fields are abandoned. In a pot experiment with a wide infestation range, the popular cultivar Gambiaka, combining resistance with sensitivity, showed a mean relative yield loss (RYL) of 63%. Parasitic Rhamphicarpa biomass (PRB), the difference between the above-ground biomass produced with and without a host, was suggested as indicator for infection level of this facultative parasite and hence as a practical measure for host resistance. Genetic variation in resistance and tolerance levels was observed among rice cultivars, but fertilizer applications significantly reduced parasite numbers, biomass and effects, cancelling out such genotypic differences. Depending on the tolerance level of the cultivars, the PRB only accounted for 3.7 e38.8% of the average parasite-inflicted host biomass reductions, indicating phytotoxic effects of Rhamphicarpa infection. R. fistulosa is an apparently increasing constraint to rain-fed lowland rice in Benin, threatening rice production in the wider region. The use of resistant and tolerant cultivars, combined with fertilizer applications could reduce Rhamphicarpa infections and mitigate negative effects on rice yields. Ó 2011 Elsevier Ltd. All rights reserved.

Keywords: Parasitic plants Inland valleys Subsistence farming Integrated weed management

1. Introduction The annual forb Rhamphicarpa fistulosa (Hochst.) Benth. (syn. Macrosiphon fistulosus Hochst.) of the Orobanchaceae family, henceforward referred to as Rhamphicarpa, is a parasitic weed of cereal crops in tropical Africa (Ouédraogo et al., 1999). Rhamphicarpa parasitizes the host through a haustorium bridging parasite and host root xylem (Neumann et al., 1998). Although the most widely affected crop is (lowland) rice, it can cause significant yield reductions in millet, sorghum and maize too (Cissé et al., 1996; Kuijt, 1969; Ouédraogo et al., 1999). It is however not clear

* Corresponding author. Tel./fax: þ255 222780768. E-mail address: [email protected] (J. Rodenburg). 0261-2194/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2011.06.007

whether host damage is caused merely by extraction of host assimilates and water or also by additional pathological or phytotoxic mechanisms (Rodenburg et al., 2010). Rhamphicarpa is a facultative hemi-parasite and as such not dependent on the presence of a host to complete the life cycle, although the parasite supposedly obtains a reproduction advantage from parasitizing a suitable host plant (e.g. Ouédraogo et al., 1999). R. fistulosa occurs from the far east (Madagascar) to the far west (Senegal) of the continent (GBIF, 2010). It is a wide-spread wetland species, both in crops and in natural vegetation, throughout West and Central Africa (Muller, 2007) where it has been observed in Benin (Gbèhounou and Assigbé, 2003), Senegal, Burkina Faso, Mali (e.g. Ouédraogo et al., 1999), Sierra Leone (Gledhill, 1970), Guinea (Cissé et al., 1996) and Congo (both DRC and Congo-Brazaville; Staner, 1938). It has also been observed in East and Southern

J. Rodenburg et al. / Crop Protection 30 (2011) 1306e1314

Africa, e.g. in Uganda (Jackson and Gartlan, 1965), Tanzania (Kayeke et al., 2010), Zimbabwe (Johnson et al., 1998), Madagascar (Bouriquet, 1933) and South Africa (Kuijt, 1969). In the early nineties of last century, Rhamphicarpa was still considered a parasitic weed of minor importance but one that was predicted to become a major problem in the future (Raynal Roques, 1994). Rhamphicarpa is adapted to seasonally wet, water-logged locations with open vegetation types (Hansen, 1975) and is therefore mainly found in hydromorphic zones and unimproved rain-fed lowland rice fields (inland valleys) (Rodenburg et al., 2010). These environments generally have a high production potential and are of strategic importance for future rice production in tropical Africa (e.g. Sakurai, 2006). Rice is the only major crop that can be grown here during the wet season due to its unique adaptation to waterlogged conditions (e.g. Andriesse and Fresco, 1991). Moreover, in terms of surface area, inland valleys constitute a huge and largely unexploited, potential for food production (e.g. Balasubramanian et al., 2007). In tropical Africa the total inland-valley area is estimated at 130 M ha (AfricaRice, 2008). Over the past three decades rice has increased in SSA by 105% in area and 170% in production (FAO, 2010). This increase is in part the result from inland-valley developments and in part from recent technological breakthroughs, such as the development of adapted and high yielding rice cultivars (e.g. Dalton and Guei, 2003). New Rice for Africa (NERICA) cultivars, for instance, have recently been developed for rain-fed lowlands and are gaining popularity (Balasubramanian et al., 2007). Some of these lowland NERICA cultivars proved to have superior weed competitiveness (Rodenburg et al., 2009) and could likewise play a role in the management of the parasitic weed Rhamphicarpa. Experiences with Striga spp. have shown that cultivar choice (e.g. Harahap et al., 1993; Johnson et al., 1997) and soil fertility management (e.g. Adagba et al., 2002; Riches et al., 2005) are essential components of an integrated parasitic weed management approach. Rhamphicarpa distribution in rain-fed lowland rice in Benin was evaluated in 1998 by Gbèhounou and Assigbé (2003). Availability of these data offers a unique opportunity to investigate whether the species is of increasing importance as a pest for rain-fed lowland rice. With a high density of inland valleys (205,000 ha; 2.8% of total land area) combined with an increasing population pressure (population growth rate 1990e2008: 3.3%; UNICEF, 2010) and a near five-fold increase in area under rice (ten-fold increase in production) between 1988 and 2008 (FAO, 2010), Benin represents an emerging rice producing country where part of the expansion is to be expected from inland-valley development, making it a suitable case-study area. The objectives of this study were to 1) investigate whether the Rhamphicarpa-infested rain-fed lowland rice area is expanding, using Benin as a case study, 2) assess the potential impact of Rhamphicarpa on rice yield and 3) explore cultivar and fertilizer effects on the parasiteehost relation and the importance of host presence for the performance of the facultative parasite. To this end, the abovementioned survey by Gbèhounou and Assigbé (2003), carried out in 1998, was repeated in 2007 and complementary farmer surveys and inland-valley inspections are combined with pot experiments, with infestation density, cultivar and fertilizer as factors.

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two cultivated inland valleys were randomly selected in each of the two districts where Rhamphicarpa was observed and reported previously (Dassa-Zoumé and Glazoué, in central Benin) and one in each of five districts with no prior report on Rhamphicarpa presence (Boukoumbé, Ouaké, Gogounou, Kandi and Karimama in the north). With help from the local extension offices, all rice farmers from those nine inland valleys were questioned about the presence of Rhamphicarpa and the location of their rice fields. Their responses were crossed-checked with a field visit. The survey period was chosen to take place in the second-half of the cropping season to increase the probability to see Rhamphicarpa in the field. Inland valleys were marked as ‘infested’ whenever a single Rhamphicarpa plant in any field was observed in the rice crop, although everywhere where Rhamphicarpa was observed it was abundant and never limited to just a few plants. During the 2007 cropping season, presence/absence of Rhamphicarpa was inspected in the same nine inland valleys as in 1998 as well as in 12 new inland valleys. These 21 inland valleys were located in seven districts: Ouaké (1 inland valley), Boukoumbé (4), Kandi (4), Gogounou (2) and Karimama (1) in the north and DassaZoumè (5) and Glazoué (4) in central Benin. The 12 new inland valleys were selected the same way as the first nine in 1998. In 2008, all the 21 inland valleys were revisited for confirmation and a random sample of an additional 15 inland valleys, stretching from 6170 N to 11430 , was checked to get an idea of the current spread in rain-fed lowland rice in the remaining parts of the country. Of the additional inland valleys 11 were located in the north e districts of Banikoara (3), Malanville (1), Matéri (3), Tanguiéta (3) and Bembèrèkè (1) e three in the centre e Bantè (3) e and one in the south e Grand-Popo (1). In total 36 inland valleys have been inspected in this study. The total number of inland valleys in Benin is estimated at 694, of which 251 are found in the 14 districts visited in this study (Source: Direction du Génie Rural, Cellule Bas-Fonds, Benin, June 2002). 2.2. Farmer survey Semi-structured, open interviews were held in 2007 with 90 rice farmers from two villages in the district of Dassa-Zoumè (Loulè 1, Loulè 2) and one village in the district of Glazoué (SokpontaBaatè) in the department of Collines (central Benin). They represent the three villages that were both located in the most important rain-fed lowland rice area of Benin (department of Collines) and that were already reported to be infested with Rhamphicarpa in 1998. A relatively long experience with rain-fed lowland rice production and Rhamphicarpa problems was expected to result in the most reliable and valuable farmer perceptions (e.g. yield loss estimates, management options). The farmers (57% women) were asked if they knew Rhamphicarpa and if they had this weed in their inland-valley rice fields. The remaining questionnaire was carried out with the rice farmers that responded affirmative to this question. Information was collected about the period Rhamphicarpa was first observed, farmers’ estimations on Rhamphicarpa-inflicted yield losses, local names of Rhamphicarpa, rice cultivars grown as well as their seed sources and farmers’ management response to Rhamphicarpa infestation. 2.3. Pot experiment 1: host  fertilizer

2. Material and methods 2.1. Inland-valley inspection During the 1998 cropping season, inland valleys grown with rice were first inspected for the presence of Rhamphicarpa. In important and representative rain-fed lowland rice-growing areas in Benin,

In 2007 a pot experiment was conducted to test host (presence and genotype) and fertilizer effects on Rhamphicarpa and rice performance. It comprised a splitesplit-plot design with seven lowland rice cultivars and one “no-host” treatment on the plot level, two Rhamphicarpa infestation levels on the sub-plot level and three fertilizer treatments (including a “no-fertilizer” control) on

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the subesub-plot level. Cultivars tested were NERICA-L-20, -32, -39 and -43, their genetic parents Oryza glaberrima TOG5681 and Oryza sativa (subspecies indica) IR64, and a popular local check Gambiaka. Cultivars NERICA-L-20, -32 and -43 were selected for their strong weed competitiveness under high weed infestation while NERICAL-39 was selected as a weak weed competitive check; TOG5681 is also highly weed suppressive while IR64 is a weak weed competitor (Rodenburg et al., 2009). Gambiaka is a traditional cultivar of the O. sativa species, subspecies indica, widely grown in West Africa (e.g. Becker and Diallo, 1996) and the most common cultivar in the Rhamphicarpa-infested inland valleys of central Benin. Rhamphicarpa infestation levels were: 1) 5 mg Rhamphicarpa seed pot1, equivalent to approximately 6267 seeds m2 (1000-seed weight of Rhamphicarpa was assessed at 11.3 mg), and 2) a Rhamphicarpa-free control. For Rhamphicarpa infestation, the upper 2 cm of soil of each pot was moved to a container, thoroughly mixed with Rhamphicarpa seed and subsequently returned to the pots. Fertilizer treatments were: 1) no-fertilizer (‘Zero’), 2) 100 kg NePeK (15:15:15) ha1 and 37.5 kg urea ha1 (‘Low’) and 3) 200 kg NePeK (15:15:15) ha1 and 75 kg urea ha1 (‘High’). With urea [(NH2)2CO] containing 46.7% nitrogen, this comes down to an equivalent of 1) 0 kg Ne0 kg Pe0 kg K ha1, 2) 32.5 kg Ne15 kg Pe15 kg K ha1 and 3) 65 kg Ne30 kg Pe30 kg K ha1. 2.4. Pot experiment 2: infestation density A second pot experiment was conducted in 2007 with the local popular rice cultivar Gambiaka to establish effects of Rhamphicarpa soil infestation density on numbers and biomass of the parasite (henceforward referred to as ‘infection’) and the effect of infestation and infection level on relative grain yield and straw biomass losses of the host plant (‘relative host damage’). A randomized block design was used with ten different Rhamphicarpa infestation levels and five replicates. For Rhamphicarpa infestation 0.0, 2.5, 5.0, 7.5, 10.0, 12.5, 25.0, 37.5, 50.0 and 62.5 mg of Rhamphicarpa seed were mixed through the upper 2 cm of soil in each pot, resulting in densities ranging from an equivalent of 0 to approximately 78,342 seeds m2. Pots were fertilized at a rate equivalent to 100 kg NePeK (15:15:15) ha1 and 37.5 kg urea ha1 (equivalent to 32.5 kg Ne15 kg Pe15 kg P ha1).

Rhamphicarpa plants from each individual pot were counted and sampled at rice maturity (105 DAS in experiment 2 and 110 DAS in experiment 1) and dried for 72 h at 75  C to assess above-ground biomass dry weight. At maturity, rice tiller numbers were counted per pot and plant height was measured from the soil surface to the tip of the tallest panicle. Weight of total rice grain yield was assessed from each individual pot and corrected to 14% grain moisture content using a moisture metre (Shin Heung Industry Co. of Oga Electric Co. Ltd., Japan; model SH-6D). Rice kernel weight was assessed by weighing 100 grains per sample derived from an individual pot. Cases with less than 100 grains per pot (4 from experiment 1 and 3 from experiment 2) have been disregarded. Rice stem and leaves harvested at rice maturity were dried for 72 h at 75  C and weighed to assess rice straw dry weights. 2.7. Data analysis and calculations Data analyses were carried out with Genstat 9th Edition, Release 9.1, SP1 (Genstat, 2007). Data derived from the pot experiments were subjected to ANOVA followed by a comparison of means using the least significant difference (LSD). To meet the assumptions of ANOVA, numbers of emerged Rhamphicarpa plants and capsule numbers were square-root transformed ([X þ c]0.5; where X is the original observation and c ¼ 0.5), prior to analyses, following procedures recommended by Sokal and Rohlf (1995). Non-linear regression was carried out using Genstat 9th Edition, to construct a model describing the relationship between relative yield loss (RYL) and Rhamphicarpa infection. Relative losses in rice grain yield (RYL), expressed in percentage (%) were calculated as follows:

RYL ¼

  YC  YR  100 YC

(1)

where YC represents the Rhamphicarpa-free rice grain weights and YR represents the Rhamphicarpa-affected rice grain weights. For the calculations of relative straw dry weight losses, grain weights were replaced by straw weights. 3. Results

2.5. Soil volume, origin and composition

3.1. Spread and distribution of Rhamphicarpa in Benin

For both experiments, 15 L pots were used with a diameter of 0.29 m at the rim and 0.23 at the bottom and 0.28 m height. Each pot was filled up to 3 cm below the rim (hence approx. soil volume: 13 L; pot surface area: 706 cm2) with a soil mixture of one unit of fine gravel and seven units of soils of an irrigated lowland rice scheme in Deve (6 450 N and 1370 E; altitude: around 19 m a.s.l.). The soil of this site (Deve) is characterized as a vertic-Eutric Gleysol with 29:30:41 (%) of sand:silt:clay composition (0e20 cm) and moderate acidity (pH-H2O: 6.0), soil organic carbon (15 g kg1), total nitrogen (1.55 g kg1) and extractable P (12 mg kg1) levels (Rodenburg et al., 2009). For both pot trials, the soil was kept at saturation level throughout the duration of the experiments, while rain caused temporary submergence to a maximum depth of 3 cm (height soil surface to the rim of the pot) and for a maximum time span of 7 continuous days.

In 2007 and 2008, eight of the 36 cultivated inland valleys visited (22%), three in the north and five in the centre, were found to be infested with Rhamphicarpa (Fig. 1): Boukoumbé (Atakora), Lèma, Loulè 1 and Loulè 2 (Dassa-Zoumè), Ouaké (Donga), Baatè/ Sokponta and Gomè (Glazoué) and Sonsoro (Kandi). Of the nine inland valleys inspected in 1998, Rhamphicarpa was found in five in 2007, compared with only three in 1998. Rice in the inland valley of Gomè (District of Glazoué, Department of Collines in the centre) and Ouaké (District of Ouaké, Department of Donga in the north) were found to be newly infested with Rhamphicarpa in the period between 1998 and 2007. In 2008, Rhamphicarpa was also observed for the first time in the inland valleys of Sonsoro, in the district of Kandi, and Lèma, in the district of Dassa, but both sites were not previously surveyed. 3.2. Farmers’ perceptions and practices

2.6. Experimental observations and measurements Rhamphicarpa plants were counted at 105 days after sowing (DAS) in experiment 2 and at 2-week intervals until 110 DAS in experiment 1. Moreover, Rhamphicarpa seed capsules were collected regularly in experiment 1 and counted at completion. All

Of the 90 farmers surveyed in the villages Loulè 1, Loulè 2 (District Dassa-Zoumè) and Sokponta-Baatè (District Glazoué), 87 encountered Rhamphicarpa in their fields. The remaining three farmers knew the species but did not have it in their field. A majority of 59% of the 87 affected farmers recalled the first

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Fig. 1. Map of the Republic of Benin, West Africa; districts where rice-grown inland valleys are evaluated for the presence of Rhamphicarpa are indicated in dark (both 1998 and 2008) and light (2008) grey; new Rhamphicarpa infestations (period 1998e2007) are indicated by a black star.

infestations in the period 1994e1998. The second largest group (23%) of farmers recalled being confronted with the parasitic weed for the first time after that period while only 5% recalled having seen it prior to 1994, and13% did not remember when Rhamphicarpa was first observed. Local names (language: Idaatcha) for Rhamphicarpa were “otcha” (meaning: death), “corico” (meaning: weed) and “efri” (meaning: killing). Of the rice farmers that were growing rice in the inland valley at the time of the survey (total 66), 83% grew rice cultivar Gambiaka, 12% used IR64, 9% NERICA (exact line number not known) and one farmer also grew TOG5681. Some farmers grew more than one cultivar in the same field, explaining

why these numbers, if added up, surpass 100%. Rice seed of these cultivars is primarily purchased at the local market (65%) but farmers also use seed derived from their own previous crop (32.5%) or from other farmers (2.5%). All but one of the rice farmers with Rhamphicarpa in their field estimated yield losses caused by this parasitic weed to surpass 60%. As a result of high Rhamphicarpa infestation levels, 27 affected farmers indicated that they have abandoned Rhamphicarpa-infested fields in the past. The only control method farmers used was hand- or hoe-weeding and one farmer indicated that the use of large amounts of fertilizer would contribute to reductions in Rhamphicarpa infestation levels.

J. Rodenburg et al. / Crop Protection 30 (2011) 1306e1314

3.3. Rhamphicarpa infestation density effects In Fig. 2, a three-quadrant representation of the relationship between Rhamphicarpa infestation level (mg of Rhamphicarpa seed per pot), Rhamphicarpa infection level (number or above-ground biomass of Rhamphicarpa plants) and Rhamphicarpa-inflicted relative host damage (relative grain yield and straw weight loss) is shown for rice cultivar Gambiaka. The upper-left quadrant (quadrant II) represents the relationship between Rhamphicarpa infestation level and relative host damage, the lower-right quadrant (quadrant IV) represents the relationship between Rhamphicarpa infestation level and infection level and the upper-right quadrant (quadrant I) represents the relationship between infection level and relative host damage. There were significant (P < 0.001; F ¼ 5.03), almost linear, increases in numbers of Rhamphicarpa plants with increasing infestation levels at 105 DAS (Fig. 2; quadrant IV). However, differences in above-ground Rhamphicarpa biomass at 105 DAS did not differ significantly between infestation levels. This relation showed a steep initial increase in Rhamphicarpa biomass until an optimum, followed by a gentle decline thereafter (quadrant IV). All but the lowest infestation level of Rhamphicarpa caused highly significant (P < 0.001; F ¼ 9.76) reductions in rice grain yield compared with un-infested controls. With increasing infestation densities Rhamphicarpa-inflicted relative yield loss quickly reaches a ceiling around 70e75% (mean: 63%; median: 68%) with no clear further increment at higher infestation levels (quadrant II). Rice biomass dry weight was also significantly (P < 0.01; F ¼ 3.79) affected but showed a more gradual decline with increasing Rhamphicarpa infestation levels (quadrant II); the first significant reduction in biomass, compared to parasite-free control plants, was

100 %

II

Infestation level

60 plants ( ) 20 g( )

Infection level

Infestation level

62.5 mg seeds

Relative host damage

I

IV 62.5 mg seeds Fig. 2. Three-quadrant representation of the relations between Rhamphicarpa infestation level (ranging from 2.5 to 62.5 mg seeds equivalent to 3133e78,342 seeds m2), Rhamphicarpa infection levels (expressed in numbers of emerged plants per pot at 105 DAS [B], ranging from 2.7 to 45.7, and above-ground plant biomass per pot at 105 DAS [:], ranging from 6.9 to 13.1 g) and Rhamphicarpa-inflicted relative host damage. Relative host damage is expressed as relative grain yield loss (RYL; ranging from 12.1 to 75.8%) in quadrant I (upper-right) and as RYL (), and as relative straw (stem and leaf) dry weight loss (þ; ranging from 5.8 to 59.4%) in quadrant II (upper-left). Data presented are derived from rice cultivar Gambiaka.

observed at the fourth infestation level (10 mg of seed, approx. 10,900 seeds m2) with no significant decrease thereafter. Quadrant I shows that the steep initial RYL increase followed by an apparent evening out thereafter is observed in spite of a wide range of achieved infection levels in terms of above-ground plant numbers. 3.4. Host and fertilizer effects on Rhamphicarpa Experiment 1 (host  fertilizer) and experiment 2 (infestation density) showed comparable means for the two common treatments (rice cultivar Gambiaka at fertilizer rates equivalent to 32.5 kg Ne15 kg Pe15 kg K ha1 and Rhamphicarpa infestation levels of 0 and 5.0 mg seeds per pot or 6267 seeds m2). Rhamphicarpa-free yield was 42.0 g per pot in experiment 1 and 33.4 g in experiment 2; the Rhamphicarpa-infested rice grain yields were 14.4 and 13.5 g per pot, respectively resulting in Rhamphicarpainflicted relative yield losses of 66 and 60%. Rhamphicarpa numbers of 8.4 in experiment 1 compared to 7.9 in experiment 2, were associated with parasitic biomass of 10.5 and 10.4 g per pot, respectively. At 110 DAS, the factor host (presence and genotype) had a significant (P < 0.001; F ¼ 11.2) effect on above-ground Rhamphicarpa biomass production but not on the number of Rhamphicarpa plants or the number of seed capsules formed. Significant effects on parasite numbers were also not observed in the period prior to 110 DAS (not shown). Fertilizer application, on the other hand, significantly (P < 0.001) reduced Rhamphicarpa plant numbers (F ¼ 36.78) and above-ground biomass (F ¼ 127.5), but not seed capsule numbers. There was also a highly significant (P < 0.001; F ¼ 9.64) host  fertilizer effect on above-ground Rhamphicarpa biomass at 110 days. Across rice cultivars Rhamphicarpa plant numbers were reduced from 66 DAS onwards by the application of fertilizer (Fig. 3). Compared to the control treatment (no-fertilizer), application of fertilizer resulted in a near 50% reduction of Rhamphicarpa numbers at a rate equivalent to 32.5 kg Ne15 kg Pe15 kg K ha1, and a near 70% reduction at double that rate, at 110 DAS. Across fertilizer levels, the presence of a host (rice) resulted in an increase of 34e111% of Rhamphicarpa biomass production, depending on the rice cultivar (Table 1). Overall, Rhamphicarpa plants parasitizing on NERICA-L-20, -39 and -43 accumulated significantly (P < 0.001)

Number of emerged Rhamphicarpa plants

1310

25

20

15

10

5

0 38

52

66

80

94

110

Days after sowing Fig. 3. Effect of fertilizer application on the number of emerged Rhamphicarpa plants (averaged over all seven rice cultivars) at a 2-week interval starting at 38 DAS. Fertilizer levels are: no-fertilizer (‘Zero’; C) and applications equivalent to 32.5 kg Ne15 kg Pe15 kg K ha1 (‘Low’; ,) and 65 kg Ne30 kg Pe30 kg K ha1 (‘High’; :). Differences between Rhamphicarpa plant numbers per treatment are significant (P < 0.001) at 66 DAS and thereafter.

J. Rodenburg et al. / Crop Protection 30 (2011) 1306e1314

Fertilizer application level

Mean (H)

‘Zero’

‘Low’

‘High’

Gambiaka IR64 NERICA-L-20 NERICA-L-32 NERICA-L-39 NERICA-L-43 TOG5681 No host

10.85 13.6 23.65 13.63 24.68 21.00 9.57 10.83

10.40 10.53 15.43 10.55 11.80 15.25 11.42 5.13

6.00 6.72 3.85 6.78 3.85 4.13 9.52 4.40

Mean (F)

15.98

11.31

5.66

9.08 10.28 14.31 10.32 13.44 13.46 10.17 6.79

H-effect (P < 0.001; F ¼ 11.2): SED ¼ 1.092; LSD ¼ 2.27; df ¼ 35. F-effect (P < 0.001; F ¼ 127.5): SED ¼ 0.645; LSD ¼ 1.283; df ¼ 80. H  F-effect (P < 0.001; F ¼ 9.64): SED ¼ 1.847; LSD ¼ 3.659; df ¼ 114; SED (within a host treatment) ¼ 1.824; LSD (within a host treatment) ¼ 3.63; df ¼ 80.

more biomass than plants parasitizing on the other cultivars. Between the two extremes, NERICA-L-20 (highest) and Gambiaka (lowest), the difference in parasite biomass dry weights was nearly 58%. However, fertilizer level had a significant effect on the ranking of cultivars based on Rhamphicarpa biomass. In absence of fertilizer, TOG5681 had the lowest, and NERICA-20 and -39 the highest Rhamphicarpa biomass. However the inverse was observed at the ‘High’ fertilizer level. At the ‘Low’ fertilizer level, Rhamphicarpa biomass production was significantly (P < 0.001) reduced (by 30%) compared to the no-fertilizer control. Doubling this rate (‘High’) significantly reduced above-ground parasite biomass compared to the ‘Low’ fertilizer level, resulting in a 65% reduction compared to the no-fertilizer control. For all host treatments, except TOG5681, the ‘High’ fertilizer application significantly (P < 0.001) reduced Rhamphicarpa biomass production compared to the no-fertilizer control. This reduction of Rhamphicarpa biomass was most pronounced (80e84%) for the cultivars with the highest parasite biomass in the no-fertilizer control situation (NERICA-L-20, -39 and -43).

3.5. Infestation effects on rice as a function of cultivar and fertilizer level Infestation by Rhamphicarpa (5.0 mg seed per pot or 6267 seeds m2) had a significant (P < 0.01; F ¼ 29.88) effect on rice grain yields and highly significant (P < 0.001) effects on tiller number (F ¼ 82.42) and straw (stem and leaf) biomass production (F ¼ 81.32) but not on kernel weight and plant height. Across parasite-free and parasite-infested conditions, the range of cultivars showed highly significant (P < 0.001) differences in rice grain yield (F ¼ 13.80), 1000-kernel dry weight (F ¼ 12.25), tiller number (F ¼ 6.58), height (F ¼ 27.16) and straw dry biomass (F ¼ 37.71). Fertilizer application showed significant (P < 0.001) positive effects on rice grain yield (F ¼ 97.79), tiller number (F ¼ 14.63), plant height (33.70) and straw biomass (F ¼ 190.07) but not on kernel weight. Significant infestation  cultivar effects were observed on rice grain yields (P < 0.05; F ¼ 2.33), 1000-kernel weight (P < 0.01; F ¼ 3.63), and straw biomass (P < 0.001; F ¼ 5.61). The interaction between Rhamphicarpa infestation and fertilizer was highly significant for tiller number only (P < 0.001; F ¼ 54.10). Under parasite-free conditions highest grain yields were obtained from IR64 followed by NERICA-L-20 and -32. Significant lower parasite-free yields were obtained from NERICA-L-39 and

50

Rice grain yield (g pot-1)

Host

60

40 30 20 10 0

Rice straw dry weights (g pot-1)

Table 1 Fertilizer (F), host (H) and F  H interaction effects on above-ground Rhamphicarpa biomass (g pot1) at 110 DAS. Fertilizer treatment factors: no-fertilizer (‘Zero’) and applications equivalent to 32.5 kg Ne15 kg Pe15 kg K ha1 (‘Low’) and 65 kg Ne30 kg Pe30 kg K ha1 (‘High’). Host treatment factors: rice cultivars Gambiaka, IR64, NERICA-L-20, -32, -39, and -43, and TOG5681 and a ‘no-host’ treatment.

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120 100 80 60 40 20 0

Fig. 4. Rhamphicarpa infestation  cultivar interaction effects on rice grain yields (g pot1) at 14% grain moisture content (top) and rice straw dry weight (g pot1), composed of stem and leaf dry weights (bottom). Cultivars are Gambiaka, IR64, NERICA-L-20, -32, -39, and -43 and TOG5681. Rhamphicarpa-free plants are represented by white bars, Rhamphicarpa-infested ones by grey bars. Error bars indicate standard errors of means (SE). LSDgrain (I  C; within levels of I): 9.345; LSDgrain (I  C; between levels of I): 9.754; LSDstraw (I  C; within levels of I): 5.495; LSDstraw (I  C; between levels of I): 5.416. Data represent means across fertilizer levels.

TOG5681 (Fig. 4). Under Rhamphicarpa-infested conditions, IR64 and NERICA-L-32 obtained significant higher grain yields than NERICA-L-20 and -39, Gambiaka and TOG5681. Only two cultivars, NERICA-L-32 and -39, did not show significant Rhamphicarpainflicted grain yield reductions. Their relative yield losses (16 and 14%, respectively) were much smaller than those of IR64 (25%), NERICA-L-43 (28%), NERICA-L-20 (42%), TOG5681 (46%) and the popularly grown Gambiaka (60%). All cultivars showed significantly (P < 0.001) reduced straw biomass production when grown in Rhamphicarpa-infested soil (Fig. 4). Rhamphicarpa-inflicted relative losses of straw biomass were 17, 20, 20 and 23% for NERICA-L-43, -32 and -39 and IR64, and 36, 37 and 40% for Gambiaka, NERICA-L-20, and TOG5681, respectively. 4. Discussion 4.1. Spread and impact The current study suggests that the importance of Rhamphicarpa as a weed of lowland rice has increased. Nine years after the first investigation by Gbèhounou and Assigbé (2003), carried out in 1998 the same nine inland valleys were revisited. In 1998, three inland valleys were infested; nine years later five. The infestation of the inland valley observed in Ouaké in 2007, denotes the first

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observation of Rhamphicarpa in the department of Donga. The 2008 observation from the district of Kandi represents the first record of Rhamphicarpa in Alibori, the most northern department of Benin. It was however not observed in the same inland valley surveyed in 1998 and consequently it is uncertain if this results from a recent invasion. Rhamphicarpa has been found in 5 of the 14 districts, and 8 of 36 inland valleys visited across the country. The actual distribution of the species in Benin could be more wide-spread as the sample of this study only included 18% of all districts of which, on average, only 14.3% of the inland valleys were visited (5.2% of the total number of valleys in Benin). Moreover, only inland valleys that are used for rice production are considered. The species however also occurs in natural vegetation. In fact, Rhamphicarpa is common in wet savannahs and characterizes a West African class of mud vegetation, the R. fistulosa-Hygrophiletea senegalensis (e.g. Müller and Deil, 2005). Adaptation to crops can occur when the crop is introduced in the preferred ecological range. With the expansion of rice production in the seasonally flooded lowlands (Balasubramanian et al., 2007; Sakurai, 2006), where Rhamphicarpa naturally occurs, and following continuous mono-cropping and exchange of seeds between farmers, the species can develop from an occasional weed into a true pest (Raynal Roques, 1994). The possibility of the existence of Rhamphicarpa prior to the years of study, as part of the natural vegetation cannot be completely ruled out. However, the current study showed that the importance of the species as a pest to lowland rice is indeed increasing. The means of dissemination of this species is still unknown. The more frequently studied parasitic weed species Striga spp. seem to spread through marketing and transport of contaminated crop seeds and, to a lesser extent, by movement of cattle (Berner et al., 1994). Interviews with rice farmers from the infested rain-fed lowlands in the current study indicated that the majority (65%) of the seed is indeed purchased from the local markets. Such informal seed systems are common in Africa but lack the institutional oversight and quality control (e.g. Balasubramanian et al., 2007; Richards et al., 2009) necessary to prevent spread of diseases and pests through seed. Rhamphicarpa primarily thrives on seasonally flooded soils (Hansen, 1975) and is rarely observed in irrigated rice fields where a permanent water level can be maintained. Hence, if rice production expansion is envisaged by putting new inland valleys into production, the prevalence of the species can increase, if improvements in water management (e.g. drainage, irrigation, field levelling, bunding) are not taken into account. Farmer interviews confirm that the species is a serious local constraint to rain-fed rice production in Benin. This is obvious from the meaning of the local names (e.g. death, killing), the high estimated yield losses and cases where farmers decided to abandon their field due to high infestation levels. The high yield losses (>60%) caused by Rhamphicarpa infestation, as estimated by rice farmers of central Benin, are confirmed by the pot experiments with the most popular cultivar (Gambiaka). Already at relative low infestation densities grain yield losses (at plant level) exceeded 60%. However, maximum relative yield losses for Gambiaka typically seem to stabilize between 60 and 80% and rarely reach complete failure. 4.2. Parasite  host interactions, resistance and tolerance Host presence had a significant effect on Rhamphicarpa biomass. A significant increase in seed capsule numbers due to host presence, as previously suggested by Ouédraogo et al. (1999), was not observed here. It should be investigated further if the capsules formed by independent plants are indeed smaller and contain fewer seeds compared to capsules of parasitizing individuals as these authors had hypothesized.

Rhamphicarpa infestation significantly reduced rice grain yield and rice straw biomass in both pot experiments similar to earlier reported effects of Striga (Striga asiatica and Striga hermonthica) on rice (e.g. Cechin and Press, 1994; Johnson et al., 1997). Resistant crop genotypes have fewer parasitic infections, while tolerant genotypes show less parasite-inflicted biomass or yield losses when exposed to similar levels of infections compared to other genotypes of the same crop species (e.g. Rodenburg et al., 2005). For the assessment of both resistance and tolerance, quantitative information on the infection level is essential (Rodenburg et al., 2006). With obligate parasitic weeds such as Striga spp. the number of above-ground parasites provides reliable information on the infection level and can be used to assess resistance and, in turn, tolerance (e.g. Haussmann et al., 2000; Rodenburg et al., 2005). However, for a facultative parasitic weed such as Rhamphicarpa, the use of above-ground parasite numbers is less suitable as a measure for infection. Presence of a Rhamphicarpa plant alone does not necessarily mean that it parasitizes on a host plant. The only way to quantify Rhamphicarpa infection levels would be to count Rhamphicarpa connections on the host root systems. However, this requires washing of root systems which is laborious and can also only be done when host plants are grown in pots. Moreover, as host connections of Rhamphicarpa plants are fragile and can easily break during the operation, the reliability of the data is not guaranteed. An alternative assessment of resistance would be the use of root observation chambers (rhizotrons), similar to the ones used for Striga research (e.g. Gurney et al., 2006). An in situ alternative is however required to assess expression of resistance in the field. Ouédraogo et al. (1999) previously indicated that parasitizing Rhamphicarpa plants accumulate more biomass than plants that grow independently. Results presented in the current study confirm this and also show that cultivars differ significantly in the amount of Rhamphicarpa biomass they support. A suitable field measure for Rhamphicarpa infection rate, that could be used to screen for resistance, could therefore be based on above-ground parasite biomass dry weights. The most reliable information would be obtained with a design that includes non-crop spaces adjacent to each genotype under consideration. The difference between the above-ground Rhamphicarpa biomass produced underneath a crop genotype and the biomass produced without a host can then be used as a measure for infection rate and hence resistance level. When the screening lines represent a wide range of plant types, the effect of cultivar differences in weed suppressive ability should however also be considered. If this measure, henceforward referred to as ‘parasitic Rhamphicarpa biomass’ (PRB), is used across fertilizer application levels the most resistant cultivars in the current study were (in decreasing order) Gambiaka, TOG5681, IR64 and NERICA-L-32. The remaining three NERICA-L cultivars (-20, -39 and -43) supported significant higher PRB and could therefore be considered susceptible. Tolerance, in turn, could be assessed by correcting the (relative) grain yield loss of a specific genotype by the aforementioned infection rate (PRB). Such correction would however require the relation between (relative) yield loss and infection rate to be known (Rodenburg et al., 2006). The three-quadrant figure presented in the current study suggested this relation to be exponential (asymptotic), similar to the sorghum yield e Striga biomass relation found by Gurney et al. (1999). Through non-linear regression based on mean RYL and mean PRB per infestation level, observed with rice cultivar Gambiaka, the following model was generated:

RYL ¼ RYLmax  ðRYLmax Þ  RPRB

(2)

where RYLmax represents the estimated maximum relative yield loss (73.2%), R is a constant (0.2074). This model could explain 99%

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of the observed variation in mean RYL (Fig. 5; P < 0.001). Parasitic Rhamphicarpa biomass (PRB) was assessed as the difference between an estimated constant and the observed biomass at each infestation level. This constant was derived from the no-host treatment in the host  fertilizer experiment at an infestation level of 6267 seeds m2 (across fertilizer rates) under the assumption, confirmed in this study, that infestation level has no significant effect on Rhamphicarpa biomass production. Negative values of RYL (3 cases) were removed. In the same graph (Fig. 5) mean RYL per mean PRB (at 6267 Rhamphicarpa seeds m2) for the other six cultivars is indicated. This shows that, although for the other cultivars the RYL-infection relation could not be modelled, all cultivars have lower RYL at comparable infection levels as Gambiaka and could thus be considered more tolerant. Based on this representation, the cultivars NERICA-L-32, and NERICA-L-39 showed a higher tolerance level than their two genetic parents (IR64 and TOG5681). NERICA-L-39 showed to be the most tolerant rice cultivar. The observed losses in host biomass and yield largely outweigh the associated parasitic Rhamphicarpa biomass (PRB). Across fertilizer levels, RPB could explain only 38.8% of the observed total above-ground rice biomass loss (including stem, leaf and grain) of the most tolerant cultivar, NERICA-L-39 in experiment 1. For the most sensitive cultivar, RPB comprised only 3.7% of the total aboveground host biomass loss. Analogous to inferences on the Strigasorghum association by Press and Stewart (1987) it could therefore be concluded that Rhamphicarpa does not merely act as a sink for its host plant but also has additional negative effects on the host. These additional effects could be caused by interspecific competition (cropeweed competition) and by what is sometimes referred to as a phytotoxic reaction. Weak weed competitors such as IR64 and NERICA-L-39 do not clearly suffer more Rhamphicarpa-inflicted damage than weed competitive cultivars (e.g. TOG5681, NERICA-L-20, -32 and -43), hence similar to host effects of obligate parasitic plants (Rank et al., 2004), phytotoxicity seems an important additional cause for the observed Rhamphicarpa-inflicted host effect.

Relative yield loss (%)

100 75 50 25 0 0

2 4 6 Parasitic Rhamphicarpa biomass (g)

8

Fig. 5. Observed (:) and fitted (continuous line; P < 0.001, F ¼ 2249.14) relation between parasitic Rhamphicarpa biomass (g) at harvest (105 DAS) and relative rice yield loss (%; with maximum RYL indicated by a dashed line) for cultivar Gambiaka at a range of infestation levels (0e62.5 mg seed per pot, equivalent to 0e78,342 seeds m2; data derived from infestation density experiment), compared to observations on a wider range of rice cultivars (IR64 [], TOG5681 [,], NERICA-L-20 [C], -32 [þ], -39 [-], and -43 [B]) at a Rhamphicarpa seed infestation level of 5.0 mg seed per pot (6267 seeds m2; data derived from host  fertilizer experiment, averaged over fertilizer application levels). The data point of Gambiaka (Δ) from the host  fertilizer experiment is included as a check.

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4.3. Fertilizer effects on Rhamphicarpa infection and host performance This study showed that the application of fertilizer significantly reduces Rhamphicarpa plant numbers and biomass and alleviates negative effects of Rhamphicarpa presence on host performance. Fertilizer application has previously been shown to control parasitic weeds of the genus Striga. Nitrogen and phosphorus deficiencies in the soil stimulate the production of Striga seed germination stimulants (e.g. Yoneyama et al., 2007) and logically, application of N and P fertilizer has the opposite effect, resulting in reduced parasitism (e.g. Lopez-Raez et al., 2009). In the case of Rhamphicarpa, where host root exudates are no prerequisite for germination, soil fertility effects should be based on other mechanisms. Improved levels of soil nitrogen (Sweeney et al., 2008) and phosphorus (Blackshaw et al., 2004) are reported to stimulate weed growth rather than reducing it. In cases where improved soil fertility was reported to reduce weed growth, the reductions were due to improved competitiveness of the crop (e.g. Tollenaar et al., 1994). In the current study, host resilience and plant vigour, conferring weed competitiveness, could have been strengthened by improved soil fertility as fertilizer applications had significant positive effects on tiller numbers, plant height and straw biomass of rice. This in turn might have caused reductions in numbers and biomass of the parasitic weed. However, fertilizer applications also halved the numbers (not shown) and biomass of independently growing Rhamphicarpa plants. Hence increased host resilience and weed competitiveness could at most only partly explain these effects. Reduced Rhamphicarpa germination could be another underlying reason for these observed reductions.

5. Conclusions R. fistulosa is a serious and increasing problem to resource-poor rice producers of rain-fed lowlands in Benin and could well become an important constraint to increased rice production in the wider region. This can be concluded from the broad distribution of the species over the continent, the increasing exploitation of the species’ preferred ecosystems (the inland valleys) and the results of this case study showing that in time the weed is able to infest new rice-grown inland valleys. Rhamphicarpa causes yield losses that easily surpass 60% and its presence motivates farmers to abandon fields. Farmers in Benin currently lack effective management strategies against Rhamphicarpa. However, experiments presented in this study provided pointers for potential management strategies. Cultivars combining a high yielding ability with resistance and tolerance would provide farmers in Rhamphicarpa-infested areas with a useful component of an integrated crop and weed management strategy. Based on the results of this study, NERICA-L-32 would be a potentially suitable candidate in this respect. For identification of additional resistant and tolerant material good screening measures are needed. A suitable field measure for resistance could be based on above-ground parasitic Rhamphicarpa biomass, which is the difference between biomass found underneath a specific host genotype and the biomass found in absence of a host. Tolerance can be assessed visually by plotting relative yield losses against parasitic biomass. In addition to cultivar choice, the use of mineral fertilizer could also reduce parasitic infections and host damage. Further studies on the ecology and biology of R. fistulosa are needed to enhance our understanding of this facultative parasitic weed. Such insights can be used to develop agronomic practices that help minimising the infestation, infection and damage levels in rain-fed lowland rice.

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