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Gynandropsis gynandra (L.) Briq.) as a red spider mite (Tetranychus urticae Koch) repellent in cut-flower rose (Rosa hybrida L.) cultivation
Scientia Horticulturae 114 (2007) 194–198 www.elsevier.com/locate/scihorti
African spider flower (Cleome gynandra L./Gynandropsis gynandra (L.) Briq.) as a red spider mite (Tetranychus urticae Koch) repellent in cut-flower rose (Rosa hybrida L.) cultivation Samuel Nyalala a, Brian Grout b,* a
Department of Horticulture, Egerton University, P.O. Box 536, Njoro, Kenya b Postgraduate School, Writtle College, Chelmsford Essex CM1 3RR, UK
Received 5 September 2006; received in revised form 25 May 2007; accepted 5 June 2007
Abstract Companion planting of Cleome gynandra, of Kenyan origin, in beds of cut-flower roses reduces significantly red spider mite (Tetranychus urticae Koch) infestation without any detrimental effect on productivity or flower quality. The level of reduction is dependent upon the density of the C. gynandra plants with 15 plants in a 1.8 m2 bed (8.3 plants m2) being the most effective, planted either around the bed perimeter or within the rows of roses. The relatively high density of C. gynandra plants required may limit the direct application of this technology in export-focused, greenhouse rose production yet may be of significant value as a supplement to other mite-control strategies. The potential benefits of such companion planting for growers of field roses and those involved in some domestic markets are also evident. Research into the nature and extraction of the active, volatile mite-repellant components of C. gynandra is indicated. # 2007 Elsevier B.V. All rights reserved. Keywords: Cleome gynandra; Spider mite; Miticide; Rose; Flower quality
1. Introduction Globally, the rose (Rosa hybrida L.) is one of the most important ornamental crops produced as cut flowers, pot and outdoor plants, and accounts for some 75% of the total flower production in world-leading producer countries such as Kenya and Ecuador (Dohm et al., 2001; Armstrong, 2004; Laws, 2005). In the Dutch auctions, the rose tops the list of cut flowers sold and is among the top 10 indoor and garden plants, accounting for more than 30% of the total auction turnover. In 2005, some 3.5 billion cut roses were sold, with close to 1 billion of those coming from Africa (Vereniging van Bloemenveilingen in Nederland, 2006). Spider mites (T. urticae Koch) are a major threat to the production of quality roses (Pemberton et al., 1997; De Moraes and Tamai, 1999; Pertwee, 2000; De Hoog, 2001; Josvold and
* Corresponding author at: Department of Agricultural Sciences, University of Copenhagen, Hojbakkegord Alle 13, 2630 Taastrup, Denmark. Tel.: +45 353 33407; fax: +45 353 33478. E-mail address: [email protected] (B. Grout). 0304-4238/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2007.06.010
Chaney, 2001) as they pierce leaf cells and withdraw sap, leading to lethal cell collapse and visible spotting on the upper leaf surfaces. Heavy infestation can cause hyper-necrosis with significant desiccation and leaf fall (Bolland et al., 1998; Landeros et al., 2004). As cut flowers are grown for their appearance and aesthetic value the commercial tolerance of such damage is low and, typically, very close to zero in export markets. T. urticae mites are vigorous, multiplying both sexually and asexually and completing their life cycle within 4–24 days (Cherian, 2003). They overwinter successfully in protected environments, thrive in the conditions that commercial rose growers strive for (25–28 8C, 60–70% RH) and are reported as acquiring resistance to many broad-spectrum, synthetic miticides (De Moraes and Tamai, 1999; Pedigo, 1999; Josvold and Chaney, 2001; Lee et al., 2003). Miticides account for more than 40% of the pesticide volume applied to rose crops (Josvold and Chaney, 2001) and 25–50% of the total cost of pest control depending on the rose variety, season and region (Cherian, 2003; Van Blindeman and Labeke, 2003; Labuchange, 2005). Typically, glasshouse growers find it necessary to spray miticides every 7–14 days, often changing the miticide as populations
S. Nyalala, B. Grout / Scientia Horticulturae 114 (2007) 194–198
are monitored, for many compounds are developmental-stage specific (Pemberton et al., 1997). Further, effective spray penetration into the relatively dense foliage produced under commercial conditions is difficult to achieve, particularly with respect to the undersides of the leaves. Miticides are expensive, can pose a significant risk to human health and environmental safety if used inappropriately (De Moraes and Tamai, 1999) and may eliminate beneficial organisms including valuable spider mite predators (Pedigo, 1999). Biological control and/or the use of resistant varieties as alternatives to miticides are being advocated (Fenton, 2003, Hole and Salunkhe, 2005; Labuchange, 2005). The pressure to consider biocontrol is increased by the enforcement, in the export market, of European codes of practice aimed at reducing and eventually eliminating pesticides (Sayila, 2002). Additionally, the market demand for pesticide-free flowers is rising and organic flower production is increasing rapidly, with the major producer countries showing significant interest in the practice. Bio-control of red spider mite using predacious mites such as Neoseiulus fallacis (Pedigo, 1999), Phytoseiulus persimilis (De Moraes and Tamai, 1999; De Vis and Barrera, 1999; Jimenez and Acosta, 1999; Cherian, 2003), Amblyseius californicus and the gall midge larva, Feltiela acrisuga (Cherian, 2003) is, like chemical control, expensive, often difficult to implement and sustain. It also demands a high level of technical skill. Furthermore, bio-control agents have a narrow target range, do not eradicate the pest nor rescue the host entirely from infection and may not be compatible with the use of chemical bactericides and fungicides (Armstrong, 2001). Finally, T. urticae is a relatively mobile mite and placing mite predators in the middle of a colony is rarely effective (Jacobson, 2004; Landeros et al., 2004). Currently, rose growers rely on P. persimilis, which has been described as the most effective biocontrol agent for spider mites in many crops (Opit et al., 2004). However, its efficacy to control the red spider mite is highly dependent on relative humidity, a difficult parameter to control accurately. Other natural alternatives to these predator strategies are, therefore, worthy of serious consideration and a number of plant species have been identified as producing volatile compounds that are toxic or repellent to spider mites (Boyd and Alverson, 2000; Chiasson et al., 2001; Chiasson et al., 2004). The African Spider Plant (Cleome gynandra L./Gynandropsis gynandra (L.) Briq.) is a semi-cultivated, leafy vegetable widely used in Eastern African countries such as Kenya and Uganda, both major rose producers. It is used locally as a medicament, an insecticide and a miticide (Chweya and Mnzava, 1997; Mnzava, 1990). Kenyan farmers use the leaves to eliminate mites from chicken plumage and it repels effectively all stages of the livestock ticks Rhipicephalus appendiculatus and Amblyomma variegatum, with high levels of acaricidal activity (Malonza et al., 1992). These repellent/ miticide properties are attributed to volatile oils emanating from the leaves (Ndungu et al., 1995; Chweya and Mnzava, 1997; Lwande et al., 1999). As mites and ticks both belong to the Order Acarina, it might be assumed that C. gynandra would
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have a degree of repellent effect on spider mites, including T. urticae Koch, the red spider mite. There are no reports in the current literature to support this view but our unpublished data indicates that over 48 h red spider mites will move away from C. gynandra leaves, from infested to clean rose leaves, to distances in excess of 20 cm. Consequently, we have investigated the effects of C. gynandra as a companion plant to reduce mite infestation on rose plants, and to demonstrate its potential as a source of extracted mite repellent or miticide. 2. Materials and methods 2.1. Plant material, plant growth conditions and mite colony production Two-year rose bushes (Rosa hybrida (L.) var. Red Corvette) were grown in an unheated glasshouse in mobile, raised beds (1.9 m 0.95 m), separated by at least 1.0 m from neighbouring beds. Two rows of five plants were maintained in each bed, equally spaced between neighbouring plants and the bed margins. The plants were maintained under standard, commercial conditions and hard pruned in October 2003. No subsequent miticide treatments were applied and by June 04 moderately severe red spider mite infestation was recorded on all of the plants, which were then cut back to 15 cm above ground level in July 2004 to produce new-grown foliage. Seeds of C. gynandra L. were obtained commercially from Simlaw Seeds (Nairobi, Kenya) and sown into modules using commercial seedling compost. Three weeks after germination, the seedlings were transplanted into 2-l plastic containers with commercial potting compost and were maintained in an unheated glasshouse. 2.2. Effect of C. gynandra planting density on increases in spider mite infestation Potted, 5-week C. gyandra plants were sunk, in a randomised pattern, into the rose beds at a density of 5, 10, 15 or 20 plants per bed, with 0 as a control. Each bed was replicated twice. The total number of rose leaves with indications of spider mite infestation was recorded, for each plant, at Day 0 and Day 7. Potted plants were used as they could readily be moved into commercial planting systems, such as hydroponic houses or mobile cultivation systems (Wijchman, 2004). 2.3. Impact of C. gynandra density and spatial arrangement on spider mite infestation, plant growth and cut-flower rose quality growth and quality of roses Potted, 5-week C. gynandra L. plants were sunk into the rose beds in August 2004 at densities of 5, 10 or 15 plants per bed (with 0 as a control), between the two rows of plants or around the perimeter of the bed. For five randomly selected rose plants in each bed the maximum plant height from the compost surface was recorded at Day 14, together with the number of stems, flower buds and open flowers per plant. Stem length and
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S. Nyalala, B. Grout / Scientia Horticulturae 114 (2007) 194–198
weight were also determined for harvested cut flowers. The number of leaves on each plant with evidence of red spider mite infestation was recorded at Day 0, 7, 14 and 21. The beds were maintained according to commercial practices and without miticide treatment throughout the experimental period. 2.4. Statistical analysis The data were subjected to analysis of variance using GENSTAT for Windows (6th and 7th ed., Lawes Agricultural Trust, Rothamsted Experimental Station) and the means separated using LSD. 3. Results
Table 2 Planting pattern of C. gynandra and its effect on the mean number of infested leaves per rose plant C. gynandra plants/m
1 1
Inter-row at 5 plants/m Inter-row at 10 plants/m 1 Inter-row at 15 plants/m 1 Perimeter at 5 plants/m 1 Perimeter at 10 plants/m 1 Perimeter at 15 plants/m 1 Control Significance
Day 0
Day 7
Day 14
Day 21
0.5 0.3 0.0 0.8 0.3 0.2 0.5 NS
0.6 0.3 0.0 0.8 0.5 0.3 1.5
1.6 1.3 0.3 2.7 0.8 0.3 5.3
7.6 7.1 2.0 8.9 4.0 1.5 19.5
**
pq pq p qr pq pq r
xy x x y x x z
***
c c ab c b a d
***
Means followed by the same letters are not significantly (P = 0.05). NS: not significant. ** Significant at a = 0.01. *** Significant at a = 0.001.
3.1. Effect of C. gynandra planting density on increases in red spider mite infestation 4. Discussion The mean number of leaves per rose plant showing indications of spider mite infestation 7 days after the introduction of C. gynandra plants varied significantly with their density, with 15 and 20 C. gynandra plants per bed exhibiting lower mean numbers of affected leaves than those treatments with 5 and 10 plants per bed (Table 1). 3.2. Impact of C. gynandra density and spatial arrangement on spider mite infestation, plant growth and cut-flower quality growth and quality of roses While there were no significant differences between plants in the number of rose leaves with spider mite at the onset of the experiment, highly significant differences were observed from 7 days to the end of the study at 21 days (Table 2). There was no difference in effect between C. gynandra plants spaced around the perimeter of the beds or planted between the rows of roses, but there was a clear effect, in both cases, of increasing the number of C. gynandra plants in the bed. Plant height, the number of new shoots, flower buds and open flowers per plant were not significantly different at 14 days and no significant differences were observed in stem length or weight of flowers cut to commercial specification (Table 3). Table 1 Mean number of rose leaves per plant (n = 20) with spider mite symptoms initially at Day 0 and Day 7, with potted C. gynandra plants set in the rose beds at various densities C. gynandra plants/m2 rose bed
Mean number of infested rose leaves per plant Initial (Day 0)
Day 7
0 5 10 15 20
5.3 3.6 2.5 1.8 3.5
23.5 9.6 7.4 3.0 4.7
n mn m m mn
d c bc a ab
Means followed by the same letters are not significantly different at P = 0.05.
4.1. Effect of C. gynandra planting density on increases in red spider mite infestation The effectiveness of C. gynandra in reducing spider mite infestation on flowering rose bushes increases with planting density, presumably reflecting the dispersion of volatile compounds produced by this species, and others in the genus, known to be effective on mites and helminths (Malonza et al., 1992; Ndungu et al., 1995; Chweya and Mnzava, 1997; Lwande et al., 1999; Ajaiyeoba et al., 2001). As spider mite damage in a single stem can lead to the rejection of a whole rose cut-flower consignment in the international marketplace (Pertwee (2000), even the most effective density of 15 C. gynandra plants per bed may not meet near-zero tolerance requirements. However, the situation for some domestic markets, particularly in under-developed but rapidly growing economies, may be more accommodating. For other crops affected by this pest the treatment might be more directly applicable to commercial production as, for example, the economic threshold for strawberry is reported as five mites per leaf (English-Loeb and Hesler, 2003). A high density of companion planting can increase the height and reduce yield and yield components of the crop plant (Muoneke and Asiegbu, 1997) typically due to competition for light, water or nutrients and, in some instances, allelopathic effects (Kruse et al., 2000). This does not occur in the rose/C. gynandra pairing where yield (stems per plant), at the optimal density of C gynandra required to minimise the mite infestation is not reduced. Infestations spread by mite locomotion, wind and transport on animals and humans typically ingress from the plot edges and, consequently, the perimeter planting shown to be effective in this study would act as a barrier to mite entry. Whilst interplanting of C. gynandra can be shown to reduce infestation, there was no evidence for lethal effects in the study. This supports earlier, unpublished, data where no significant mite mortality was recorded when infested rose leaves were bagged with fresh C. gynandra leaves for 4 days.
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Table 3 Effect of C. gynandra companion planting on subsequent quality of cut-flower roses C. gynandra plant density and spacing per bed
Spider mite affected leaves
Plant height (cm)
New shoots
Flower buds
Open flowers
Cut stem length (cm)
Cut stem weight (g)
5 inter-row 10 inter-row 15 inter-row 5 perimeter 10 perimeter 15 perimeter Control Significance
1.6 1.3 0.3 2.7 0.8 0.3 5.3
73.2 79.9 68.0 72.9 68.6 70.2 74.0 NS
0.9 1.6 1.5 1.5 1.3 1.1 1.7 NS
2.4 4.4 3.1 2.6 2.9 2.7 2.9 NS
1.0 1.5 0.9 1.0 0.4 0.8 1.1 NS
59.5 61.2 54.7 59.1 54.7 60.7 58.7 NS
35.6 35.1 27.2 31.5 29.8 31.0 33.6 NS
***
***
Significant at a = 0.001.
Spider mites are known to acquire resistance to miticides relatively quickly (Wang and Liu, 1994; Karlik et al., 1995; Pemberton et al., 1997; Josvold and Chaney, 2001; Cherian, 2003; Van Leeuwen et al., 2004) and it might be supposed that they would react similarly to the repellent volatiles emitted by C. gynandra. However, in the wild there is no evidence of mite infestation of C. gynandra (Chweya and Mnzava, 1997), suggesting that companion planting would be sustainable. The effectiveness of volatile oils isolated from C. gynandra in controlling mite populations, in both plants and animals, is clearly of future interest. References Ajaiyeoba, E.O., Onocha, P.A., Olarenwaju, O.T., 2001. In vitro anthelmintic properties of Buchholzia coriaceae and Gynandropsis gynandra extracts. Pharm. Biol. 39 (3), 217–220. Armstrong, H., 2001. Increasing ways to biologically control pests. FlowerTech 4 (7), 22–25. Armstrong, H., 2004. Kenya expands rose production. FlowerTech 7 (3), 6–9. Bolland, H.R., Gutierrez, J., Flechtmann, C.H.W., 1998. World catalogue of the spider mite family (Acari: Tetranychidae), Brill, Leiden. Boyd, D.W., Alverson, D.R., 2000. Repellancy effects of garlic extracts on twospotted spider mite, Tetrancus urticae Koch. Cherian, S., 2003. Biological control of mites in roses. FloraCulture Int. 13 (9), 20–23. Chiasson, H.A., Belanger, N., Bostanian, N., Vincent, C., Poliquin, A., 2001. Acaricidal properties of Artemisia absinthium and Tanacetum vulgare (Asteraceae) essential oils obtained by different methods of extraction. J. Econ. Entomol. 94, 167–171. Chiasson, H.A., Bostanian, N, Vincent, C., 2004. Acaricidal properties of a Chenopodium-based botanical. J. Econ. Entomol. 97, 1373–1377. Chweya, J.A., Mnzava, N.A., 1997. Cat’s Whiskers (Cleome gynandra). FAO/ IPGR, Rome. De Hoog Jr., J., 2001. Handbook for Modern Greenhouse Rose Cultivation. Applied Plant Research, Aalsmeer. De Moraes, G.J., Tamai, M.A., 1999. Biological control of Tetranychus spp. on ornamental plants. Acta Horticult. 482, 247–252. De Vis, R., Barrera, A.J., 1999. Use of two predators Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) and Neoseiulus californicus McGregor (Acari: Phytoseiidae) for the biological control of Tetranychus urticae Koch (Acari: Tetranychidae) in roses in the Bogota plateau. Acta Horticult. 482, 259–267. Dohm, A., Ludwig, C., Schilling, D., Debener, T., 2001. Transformation of roses with genes for antifungal proteins. Acta Horticult. 547, 27–33. English-Loeb, G., Hesler, S., 2003. The impact of Two-spotted spider mite (TSSM) on June-bearing strawberries grown in New York. Final project
report to the North American Strawberry Growers Association. Cornell University, NY State. Faber, D., 2006. Innovation—Annual Report 2005. Vereniging van Bloemenveilingen in Nederland, Lieden. Fenton, L.J., 2003. Knocking out nature: floriculture through the eyes of an environmentalist. FloraCulture Int. 13 (2), 22–25. Hole, U.B., Salunkhe, G.N., 2005. Studies on the relative resistance of rose cultivars to two spotted spider mite (Tetranychus urticae Koch). J. Maharashtra Agric. Univ. 30 (3), 316–317. Jacobson, R., 2004. Not all spider mites are equal. Grower 141 (14), 11. Jimenez, L., Acosta, A., 1999. Life cycle and some predatory aspects of Phytoseiulus persimilis Athias-Henriot and Tetranychus urticae Koch on ‘Visa’ Rose. Acta Horticult. 482, 253–258. Josvold, S.A., Chaney, W.E., 2001. Evaluation of reduced risk and other biorational miticides on the control of spider mite (Tetranychus urticae). Acta Horticult. 547, 93–96. Karlik, J.F., Goodell, P.B., Osteen, G.W., 1995. Sampling and treatment thresholds for spider mite management in field-grown rose plants. HortScience 30 (6), 1268–1270. Kruse, M., Strandberg, M., Strandberg, B., 2000. Ecological effects of allelopathic plants—a review. National Environmental Research Institute—NERI Technical Report no. 315, Ilkeborg, Denmark. Labuchange, L., 2005. IPM of spider mite in roses. Floracult. Int. 15 (2), 12. Landeros, J., Guevara, L.P., BadiiM, H., Flores, A.E., Pa´manes, A., 2004. Effect of different densities of the twospotted spider mite Tetranychus urticae on CO2 assimilation, transpiration, and stomatal behaviour in rose leaves. Exp. Appl. Acarlol. 32 (3), 187–198. Laws, N., 2005. 2003—A strong year for floriculture. Floracult. Int. 15 (2), 26– 29. Lee, Y.S., Song, M.H., Ahn, K.S., Lee, K.Y., Kim, J.W., Kim, G.H., 2003. Monitoring of miticide resistance in two-spotted spider mite (Tetranychus urticae) populations from rose greenhouses in Korea. J. Asia Pacific Entomol. 6 (1), 91–96. Lwande, W., Ndakala, A.J., Hassanali, A., Moreka, L., Nyandat, E., Ndungu, M., Amiani, H., Gitu, P.M., Malonza, M.M., Punyua, D.K., 1999. Gynandropsis gynandra essential oil and its constituents as tick (Rhipicephalus appendiculatus) repellents. Phytochemistry 50 (3), 401–405. Malonza, M.M., Dipeolu, O.O., Amoo, A.O., Hassan, S.M., 1992. Laboratory and field observations on anti-tick properties of the plant Gynandropsis gynandra (L.) Brig. Vet. Parasitol. 42, 123–136. Mnzava, N.A., 1990. Studies on tropical vegetables. 2. Amino and fatty acid composition in seed of Cleome (Gynandropsis gynandra L. Briq) selections from Zambia. Food Chem. 35 (4), 287–293. Muoneke, C.O., Asiegbu, J.E., 1997. Effect of okra planting density and spatial arrangement in intercrop with maize on the growth and yield of the component species. J. Agron. Crop Sci. 179 (4), 201–207. Ndungu, M., Lwande, W., Hassanali, A., Moreka, L., Chhabra, S.C., 1995. Cleome monophylla essential oil and its constituents as tick (Rhipicephalus appendiculatus) and maize weevil (Sitophilus zeamais) repellents. Entomol. Exp. Appl. 76 (3), 217–222.
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Opit, G.P., Nechols, R., Margolies, D.C., 2004. Biological control of two-spotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), using Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseidae) on ivy geranium: assessment of predator release ratios. Biol. Control 29 (3), 445–452. Pedigo, L.P., 1999. Entomology and Pest Management, 3rd ed. Prentice-Hall Inc., New Jersey. Pemberton, H., Kelly, J.W., Ferare, J., 1997. Production of Pot Roses. Timber Press, Oregon. Pertwee, J., 2000. Production and Marketing of Roses. Reed Business Information, Doetinchem. Sayila, A., 2002. Kenya defends attacks by environmentalists. FlowerTech 5 (3), 15–17.
Van Blindeman, L., Labeke, M.C., 2003. Control of the two-spotted spider mite (Tetranychus urticae Koch) in glasshouse roses. Commun. Agric. Appl. Biol. Sci. 68 (4), 249–254. Van Leeuwen, T., Stillatus, V., Tirry, L., 2004. Genetic analysis and crossresistance spectrum of a laboratory-selected chlorfenapyr resistant strain of two-spotted spider mite (Acari: Tetranychidae). Exp. Appl. Acarol. 32 (4), 249–261. Wang, W., Liu, T.S., 1994. Toxicity of mixtures of several miticides with the fungicide triforine against the two-spotted spider mite on roses. Bull. Taichung Dist. Agric. Improve. Station 44, 1–11. Wijchman, G., 2004. Mobile cultivation system gets roses moving. FlowerTech 7 (1), 16–19.
African spider flower (Cleome gynandra L./Gynandropsis gynandra (L.) Briq.) as a red spider mite (Tetranychus urticae Koch) repellent in cut-flower rose (Rosa hybrida L.) cultivation Samuel Nyalala a, Brian Grout b,* a
Department of Horticulture, Egerton University, P.O. Box 536, Njoro, Kenya b Postgraduate School, Writtle College, Chelmsford Essex CM1 3RR, UK
Received 5 September 2006; received in revised form 25 May 2007; accepted 5 June 2007
Abstract Companion planting of Cleome gynandra, of Kenyan origin, in beds of cut-flower roses reduces significantly red spider mite (Tetranychus urticae Koch) infestation without any detrimental effect on productivity or flower quality. The level of reduction is dependent upon the density of the C. gynandra plants with 15 plants in a 1.8 m2 bed (8.3 plants m2) being the most effective, planted either around the bed perimeter or within the rows of roses. The relatively high density of C. gynandra plants required may limit the direct application of this technology in export-focused, greenhouse rose production yet may be of significant value as a supplement to other mite-control strategies. The potential benefits of such companion planting for growers of field roses and those involved in some domestic markets are also evident. Research into the nature and extraction of the active, volatile mite-repellant components of C. gynandra is indicated. # 2007 Elsevier B.V. All rights reserved. Keywords: Cleome gynandra; Spider mite; Miticide; Rose; Flower quality
1. Introduction Globally, the rose (Rosa hybrida L.) is one of the most important ornamental crops produced as cut flowers, pot and outdoor plants, and accounts for some 75% of the total flower production in world-leading producer countries such as Kenya and Ecuador (Dohm et al., 2001; Armstrong, 2004; Laws, 2005). In the Dutch auctions, the rose tops the list of cut flowers sold and is among the top 10 indoor and garden plants, accounting for more than 30% of the total auction turnover. In 2005, some 3.5 billion cut roses were sold, with close to 1 billion of those coming from Africa (Vereniging van Bloemenveilingen in Nederland, 2006). Spider mites (T. urticae Koch) are a major threat to the production of quality roses (Pemberton et al., 1997; De Moraes and Tamai, 1999; Pertwee, 2000; De Hoog, 2001; Josvold and
* Corresponding author at: Department of Agricultural Sciences, University of Copenhagen, Hojbakkegord Alle 13, 2630 Taastrup, Denmark. Tel.: +45 353 33407; fax: +45 353 33478. E-mail address: [email protected] (B. Grout). 0304-4238/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2007.06.010
Chaney, 2001) as they pierce leaf cells and withdraw sap, leading to lethal cell collapse and visible spotting on the upper leaf surfaces. Heavy infestation can cause hyper-necrosis with significant desiccation and leaf fall (Bolland et al., 1998; Landeros et al., 2004). As cut flowers are grown for their appearance and aesthetic value the commercial tolerance of such damage is low and, typically, very close to zero in export markets. T. urticae mites are vigorous, multiplying both sexually and asexually and completing their life cycle within 4–24 days (Cherian, 2003). They overwinter successfully in protected environments, thrive in the conditions that commercial rose growers strive for (25–28 8C, 60–70% RH) and are reported as acquiring resistance to many broad-spectrum, synthetic miticides (De Moraes and Tamai, 1999; Pedigo, 1999; Josvold and Chaney, 2001; Lee et al., 2003). Miticides account for more than 40% of the pesticide volume applied to rose crops (Josvold and Chaney, 2001) and 25–50% of the total cost of pest control depending on the rose variety, season and region (Cherian, 2003; Van Blindeman and Labeke, 2003; Labuchange, 2005). Typically, glasshouse growers find it necessary to spray miticides every 7–14 days, often changing the miticide as populations
S. Nyalala, B. Grout / Scientia Horticulturae 114 (2007) 194–198
are monitored, for many compounds are developmental-stage specific (Pemberton et al., 1997). Further, effective spray penetration into the relatively dense foliage produced under commercial conditions is difficult to achieve, particularly with respect to the undersides of the leaves. Miticides are expensive, can pose a significant risk to human health and environmental safety if used inappropriately (De Moraes and Tamai, 1999) and may eliminate beneficial organisms including valuable spider mite predators (Pedigo, 1999). Biological control and/or the use of resistant varieties as alternatives to miticides are being advocated (Fenton, 2003, Hole and Salunkhe, 2005; Labuchange, 2005). The pressure to consider biocontrol is increased by the enforcement, in the export market, of European codes of practice aimed at reducing and eventually eliminating pesticides (Sayila, 2002). Additionally, the market demand for pesticide-free flowers is rising and organic flower production is increasing rapidly, with the major producer countries showing significant interest in the practice. Bio-control of red spider mite using predacious mites such as Neoseiulus fallacis (Pedigo, 1999), Phytoseiulus persimilis (De Moraes and Tamai, 1999; De Vis and Barrera, 1999; Jimenez and Acosta, 1999; Cherian, 2003), Amblyseius californicus and the gall midge larva, Feltiela acrisuga (Cherian, 2003) is, like chemical control, expensive, often difficult to implement and sustain. It also demands a high level of technical skill. Furthermore, bio-control agents have a narrow target range, do not eradicate the pest nor rescue the host entirely from infection and may not be compatible with the use of chemical bactericides and fungicides (Armstrong, 2001). Finally, T. urticae is a relatively mobile mite and placing mite predators in the middle of a colony is rarely effective (Jacobson, 2004; Landeros et al., 2004). Currently, rose growers rely on P. persimilis, which has been described as the most effective biocontrol agent for spider mites in many crops (Opit et al., 2004). However, its efficacy to control the red spider mite is highly dependent on relative humidity, a difficult parameter to control accurately. Other natural alternatives to these predator strategies are, therefore, worthy of serious consideration and a number of plant species have been identified as producing volatile compounds that are toxic or repellent to spider mites (Boyd and Alverson, 2000; Chiasson et al., 2001; Chiasson et al., 2004). The African Spider Plant (Cleome gynandra L./Gynandropsis gynandra (L.) Briq.) is a semi-cultivated, leafy vegetable widely used in Eastern African countries such as Kenya and Uganda, both major rose producers. It is used locally as a medicament, an insecticide and a miticide (Chweya and Mnzava, 1997; Mnzava, 1990). Kenyan farmers use the leaves to eliminate mites from chicken plumage and it repels effectively all stages of the livestock ticks Rhipicephalus appendiculatus and Amblyomma variegatum, with high levels of acaricidal activity (Malonza et al., 1992). These repellent/ miticide properties are attributed to volatile oils emanating from the leaves (Ndungu et al., 1995; Chweya and Mnzava, 1997; Lwande et al., 1999). As mites and ticks both belong to the Order Acarina, it might be assumed that C. gynandra would
195
have a degree of repellent effect on spider mites, including T. urticae Koch, the red spider mite. There are no reports in the current literature to support this view but our unpublished data indicates that over 48 h red spider mites will move away from C. gynandra leaves, from infested to clean rose leaves, to distances in excess of 20 cm. Consequently, we have investigated the effects of C. gynandra as a companion plant to reduce mite infestation on rose plants, and to demonstrate its potential as a source of extracted mite repellent or miticide. 2. Materials and methods 2.1. Plant material, plant growth conditions and mite colony production Two-year rose bushes (Rosa hybrida (L.) var. Red Corvette) were grown in an unheated glasshouse in mobile, raised beds (1.9 m 0.95 m), separated by at least 1.0 m from neighbouring beds. Two rows of five plants were maintained in each bed, equally spaced between neighbouring plants and the bed margins. The plants were maintained under standard, commercial conditions and hard pruned in October 2003. No subsequent miticide treatments were applied and by June 04 moderately severe red spider mite infestation was recorded on all of the plants, which were then cut back to 15 cm above ground level in July 2004 to produce new-grown foliage. Seeds of C. gynandra L. were obtained commercially from Simlaw Seeds (Nairobi, Kenya) and sown into modules using commercial seedling compost. Three weeks after germination, the seedlings were transplanted into 2-l plastic containers with commercial potting compost and were maintained in an unheated glasshouse. 2.2. Effect of C. gynandra planting density on increases in spider mite infestation Potted, 5-week C. gyandra plants were sunk, in a randomised pattern, into the rose beds at a density of 5, 10, 15 or 20 plants per bed, with 0 as a control. Each bed was replicated twice. The total number of rose leaves with indications of spider mite infestation was recorded, for each plant, at Day 0 and Day 7. Potted plants were used as they could readily be moved into commercial planting systems, such as hydroponic houses or mobile cultivation systems (Wijchman, 2004). 2.3. Impact of C. gynandra density and spatial arrangement on spider mite infestation, plant growth and cut-flower rose quality growth and quality of roses Potted, 5-week C. gynandra L. plants were sunk into the rose beds in August 2004 at densities of 5, 10 or 15 plants per bed (with 0 as a control), between the two rows of plants or around the perimeter of the bed. For five randomly selected rose plants in each bed the maximum plant height from the compost surface was recorded at Day 14, together with the number of stems, flower buds and open flowers per plant. Stem length and
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weight were also determined for harvested cut flowers. The number of leaves on each plant with evidence of red spider mite infestation was recorded at Day 0, 7, 14 and 21. The beds were maintained according to commercial practices and without miticide treatment throughout the experimental period. 2.4. Statistical analysis The data were subjected to analysis of variance using GENSTAT for Windows (6th and 7th ed., Lawes Agricultural Trust, Rothamsted Experimental Station) and the means separated using LSD. 3. Results
Table 2 Planting pattern of C. gynandra and its effect on the mean number of infested leaves per rose plant C. gynandra plants/m
1 1
Inter-row at 5 plants/m Inter-row at 10 plants/m 1 Inter-row at 15 plants/m 1 Perimeter at 5 plants/m 1 Perimeter at 10 plants/m 1 Perimeter at 15 plants/m 1 Control Significance
Day 0
Day 7
Day 14
Day 21
0.5 0.3 0.0 0.8 0.3 0.2 0.5 NS
0.6 0.3 0.0 0.8 0.5 0.3 1.5
1.6 1.3 0.3 2.7 0.8 0.3 5.3
7.6 7.1 2.0 8.9 4.0 1.5 19.5
**
pq pq p qr pq pq r
xy x x y x x z
***
c c ab c b a d
***
Means followed by the same letters are not significantly (P = 0.05). NS: not significant. ** Significant at a = 0.01. *** Significant at a = 0.001.
3.1. Effect of C. gynandra planting density on increases in red spider mite infestation 4. Discussion The mean number of leaves per rose plant showing indications of spider mite infestation 7 days after the introduction of C. gynandra plants varied significantly with their density, with 15 and 20 C. gynandra plants per bed exhibiting lower mean numbers of affected leaves than those treatments with 5 and 10 plants per bed (Table 1). 3.2. Impact of C. gynandra density and spatial arrangement on spider mite infestation, plant growth and cut-flower quality growth and quality of roses While there were no significant differences between plants in the number of rose leaves with spider mite at the onset of the experiment, highly significant differences were observed from 7 days to the end of the study at 21 days (Table 2). There was no difference in effect between C. gynandra plants spaced around the perimeter of the beds or planted between the rows of roses, but there was a clear effect, in both cases, of increasing the number of C. gynandra plants in the bed. Plant height, the number of new shoots, flower buds and open flowers per plant were not significantly different at 14 days and no significant differences were observed in stem length or weight of flowers cut to commercial specification (Table 3). Table 1 Mean number of rose leaves per plant (n = 20) with spider mite symptoms initially at Day 0 and Day 7, with potted C. gynandra plants set in the rose beds at various densities C. gynandra plants/m2 rose bed
Mean number of infested rose leaves per plant Initial (Day 0)
Day 7
0 5 10 15 20
5.3 3.6 2.5 1.8 3.5
23.5 9.6 7.4 3.0 4.7
n mn m m mn
d c bc a ab
Means followed by the same letters are not significantly different at P = 0.05.
4.1. Effect of C. gynandra planting density on increases in red spider mite infestation The effectiveness of C. gynandra in reducing spider mite infestation on flowering rose bushes increases with planting density, presumably reflecting the dispersion of volatile compounds produced by this species, and others in the genus, known to be effective on mites and helminths (Malonza et al., 1992; Ndungu et al., 1995; Chweya and Mnzava, 1997; Lwande et al., 1999; Ajaiyeoba et al., 2001). As spider mite damage in a single stem can lead to the rejection of a whole rose cut-flower consignment in the international marketplace (Pertwee (2000), even the most effective density of 15 C. gynandra plants per bed may not meet near-zero tolerance requirements. However, the situation for some domestic markets, particularly in under-developed but rapidly growing economies, may be more accommodating. For other crops affected by this pest the treatment might be more directly applicable to commercial production as, for example, the economic threshold for strawberry is reported as five mites per leaf (English-Loeb and Hesler, 2003). A high density of companion planting can increase the height and reduce yield and yield components of the crop plant (Muoneke and Asiegbu, 1997) typically due to competition for light, water or nutrients and, in some instances, allelopathic effects (Kruse et al., 2000). This does not occur in the rose/C. gynandra pairing where yield (stems per plant), at the optimal density of C gynandra required to minimise the mite infestation is not reduced. Infestations spread by mite locomotion, wind and transport on animals and humans typically ingress from the plot edges and, consequently, the perimeter planting shown to be effective in this study would act as a barrier to mite entry. Whilst interplanting of C. gynandra can be shown to reduce infestation, there was no evidence for lethal effects in the study. This supports earlier, unpublished, data where no significant mite mortality was recorded when infested rose leaves were bagged with fresh C. gynandra leaves for 4 days.
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Table 3 Effect of C. gynandra companion planting on subsequent quality of cut-flower roses C. gynandra plant density and spacing per bed
Spider mite affected leaves
Plant height (cm)
New shoots
Flower buds
Open flowers
Cut stem length (cm)
Cut stem weight (g)
5 inter-row 10 inter-row 15 inter-row 5 perimeter 10 perimeter 15 perimeter Control Significance
1.6 1.3 0.3 2.7 0.8 0.3 5.3
73.2 79.9 68.0 72.9 68.6 70.2 74.0 NS
0.9 1.6 1.5 1.5 1.3 1.1 1.7 NS
2.4 4.4 3.1 2.6 2.9 2.7 2.9 NS
1.0 1.5 0.9 1.0 0.4 0.8 1.1 NS
59.5 61.2 54.7 59.1 54.7 60.7 58.7 NS
35.6 35.1 27.2 31.5 29.8 31.0 33.6 NS
***
***
Significant at a = 0.001.
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