- Email: [email protected]
Effects of plant diversity on the density and herbivory of the flea beetle, Phyllotreta cruciferae Goeze, in California collard (Brassica oleracea) cropping systems
CROP PROTECTION (1983) 2 (4), 497-501
Effects of plant diversity on the density and herbivory of the flea beetle, Phyllotreta cruciferae Goeze, in California collard (Brassica oleracea) cropping systems MIGUEL A. ALTIERI
Division of Biological Control, University of California, Berkeley CA 94720, USA AND STEPHEN R. GLIESSMAN
Agroecology Program, Environmental Studies, University of California, Santa Cruz CA 95064, USA ABSTRACT. Populations of the flea beetle, Phyllotreta cruciferae Goeze (Coleoptera:Chrysomelidae), were' greater in weed-free collards than in collard monocultures and polycultures (intercropped with beans) left weedy for 2 or 4 weeks after transplanting or for the entire season. Flea beetle densities and amount of leaf damage per individual collard plant were significantlylower in the plots with crucifer weeds (mainly Brassicacampestris L.), possibly because the beetles preferred to feed and/or concentrate on this plant rather than on collards.
Introduction Cruciferous crops have been extensively used as model systems to test the hypothesis that vegetational diversity results in lower pest loads in agricultural systems (Cromartie, 1981). Most studies have shown a reduction in the abundance of particular herbivores in diversified cole crops when compared with monocultures. One such herbivore is the specialized crucifer-feeding flea beetle, Phyllotreta cruciferae Goeze (Coleoptera:Chrysomelidae). These flea beetles are quick colonizers ofcruciferous hosts growing in dense or nearly pure stands (Root, 1973), and will remain on these plants, depending on the vigour and quality of the host plants (Kareiva, 1982). However, when a particular host plant is grown intermingled with other non-host plants, the flea beetles may experience difficulty in locating and remaining°on the host plant (Tahvanainen and Root, 1972). Apparently, visual or 0261-2194/83/04/0497-05503.00 © 1983 Butterworth & Co (Publishers) Ltd
498
Plant diversity effects on flea beetles in collards
chemical stimuli from non-host plants can affect both the rate of colonization of the flea beetles and their tenure time on the host plants (Risch, 1981). This study was designed to investigate the role of plant diversity in the population dynamics of P. cruciferae and their feeding impact on collards (Brassica oleracea), when collards were grown with other cruciferous hosts, or other non-hosts (i.e. beans), or both. Materials and methods On 17 July 1981 an area of 3000 m 2 was ploughed, cultivated and divided into 24 plots each measuring 5 m 2 at the University of California's Santa Cruz farm and garden. The distance between plots was 5 m, and these interplot areas were kept free of vegetation by frequent harrowing. All plots were fertilized with chicken manure (1 kg/m2; 25 kg/plot) and sprinkler-irrigated when needed. Treatments were randomly assigned and each replicated three times: 1. 2. 3. 4. 5. 6. 7. 8.
Collard (cv. Georgia) monoculture kept weed free by hoeing all season. Collard monoculture kept weed-free for only 2 weeks after transplanting.* Collard monoculture kept weed-free for only 4 weeks after transplanting.* Collard monoculture weedy all season. Collard/field-bean (var. horticultural dwarf) polycultures kept weed-flee all season. Polycultures weed-free for 2 weeks post-transplant.* Polycultures weed-free for 4 weeks post-transplant.* Polycultures weedy all season.
In the monocultures and polycultures, 20-day-old greenhouse-grown collards (about 8-12 cm tall) were transplanted equidistantly at a density of 90 plants per plot. In the polycultures, 90 bean seeds were planted simultaneously between collards. Brassica campestris was the dominant weed in the 'weedy' plots, while Raphanus spp., Spergula arvensis, Convolvulus arvensis and Anagallis arvensis occured as several individuals but with cover less than 4% of the total plot area. Densities of flea beetles were estimated by directly counting the number of beetles found on 10 randomly selected collard and five B. campestris plants in each plot on three occasions (15, 30 and 45 days after transplanting). Direct observation was used because it has proved to be a very effective and accurate sampling method; however, its efficiency could be affected by the heterogeneity of the vegetation associated with the plants being sampled (Mayse, Price and Kogan, 1978; Bach, 1980). At these times, the number of leaves with flea-beetle damage (with holes larger than 0.5 cm 2) in each of the 10 collard plants was recorded. Flea beetle damage was distinguished as a pit feeding injury, as opposed to the strip feeding which is typical of lepidopterous larvae. Plant biomass in each plot was determined from oven-dried samples of collards and weeds clipped from 1 m 2 quadrats at harvest time (70 days after planting). To compare flea beetle densities between treatments, an analysis of variance was utilized to test for effects of diversity. The analysis was performed on three replicate plots for each combination of treatments. Differences in beetle densities were separated by Duncan's new multiple range test. * All 2- or 4-weekregimesare termed 'relaxed' weedingregimesin the text.
Weed-free all season Weed-free for 4 weeks after collard transplanting Weed-free for 2 weeks after collard transplanting Weedy all season
Collard-bean polycultures
Weed-free all season Weed-free for 4 weeks after collard transplanting Weed-free for 2 weeks after collard transplanting Weedy all season
Collard monocultures
Cropping system
13.1 + 6"5 d 15.0+7'8 d
4"9 + 2'3 c 0-6+0"5 e
6'7 d 32.1 c
10.9 d
4'3 +3'3 c
44'5 b 29.9 c
1-6+0.9 d
73'7+20'1 a 25"0 + 11'5 b
29.0+ 1.7 b 6-6 + 3"8 c
44"6 b
34.1 c
78" 1 + 16.3 a
29"3 + 1-7 b
54"4 a
2'3 + 1' 1 d
--
34'0 + 2.6 a
No. of flea beetles ( + SE)
84 85
28
0
52 142
42
0
93.2 234.5
25.7
0
55.2 438.2
52.3
0
309"4 115.2
324.0
334'4
243.0 226.1
361"3
213"6
Leaves in each collard plant with beetle damage (45 days Whole~-plant collard Per 10 Per 5 after transplanting) Weed density Weed biomass dry weight collard plants Brassica campestris plants (%) (individuals/m z) (g/m z) (g/m 2)
TABLE 1. Mean flea beetle (Phyllotreta cruciferae) densities, weed and crop biomass in various collard cropping systems in Santa Cruz, California. Means followed by the same letter in each column are not significantly different ( P = 0-05). All means are averages of three sampling dates (15, 30 and 45 days after transplanting)
Z
Z
Z
500
Plant diversity effects on flea beetles in collards
Results
Noticeable populations of P. cruciferae were present only during the first 45 days after transplanting. After this period, densities per plant dropped to a level of less than one flea beetle per collard, regardless of treatment. Flea beetle densities (expressed as mean densities for the three census dates: 15, 30 and 45 days after transplanting) were significantly greater in the weed-free collard monocultures than in all other treatments (Table 1). These differences in beetle numbers were consistent on the three sampling dates. A peak in numbers was apparent for all monoculture plots (except those which were weedy all season) at 30 days. This pattern was not apparent for polycultures. Allowing weed growth during selected periods of the crop cycle (2-4 weeks weed-free or weedy all season) resulted in lower flea beetle densities in the weedy monocultures than in the weed-free monocultures. Lowest densities occurred in systems allowed to remain weedy all season: no differences in the abundance of beetles were observed between collards kept weed-free for 2-4 weeks after transplanting. Even lower flea beetle densities were observed in collards intercropped with beans, especially in polycultures left weedy the entire season. In both monocultures and polycultures with 'relaxed' weeding regimes, flea beetle densities were at least five times greater on a per plant basis on Brassica campestris (the dominant plant of the weed community) than on collards. B. campestris germinated quickly and flowered early, each plant averaging a height of 39 cm, with 12 leaves and 16 open flowers, 60 days after germination. This apparent preference of P. cruciferae for B. campestris over collards resulted in a higher concentration of flea beetles on the wild crucifer, diverting flea beetles from collards and consequently diluting their feeding on the collards. As shown in Table 1, collards grown under various levels of weed diversity and/or polycultural patterns exhibited significantly less leaf damage than monoculture collards grown in weed-free situations. Plots in which weeds were suppressed during the initial 2-4 weeks of crop establishment showed lower weed growth than plots allowed to remain weedy all season. In all-season weedy polycultures there was significantly lower weed biomass than in all-season weedy monocultures. Apparently, the shading provided by the overlapping bean and collard canopies helped to suppress weeds. There appeared to be two patterns in collard yields: collards had higher biomass in the weed-free polycultures than in the weed-free monocultures, and weed competition did not seem to reduce collard growth in the all-season weedy monoculture, as it did in the collard all-season weedy polyculture.
Discussion a n d conclusions Increased plant diversity, in the form of'relaxed' weeding regimes or intercropping patterns, led to lower population densities of P. cruciferae. In our particular study, the effects of plant diversity on flea beetle populations could have been due to several interacting variables, such as host and non-host plant density and total plant density, which vary with diversity. It is obvious that flea beetles had to explore a much higher density of host and non-host plant material in the diversified monocultures and polycultures: they therefore might have experienced greater difficulty in locating suitable collard plants. It is possible that, once they located a suitable collard, the
MIGUEL A. ALTIERI AND STEPHEN R. GLIESSMAN
501
time that they spent on that plant depended both on plant quality and the nature of the associated plants. Studies have shown that certain Chrysomelid beetles tend to emigrate more from polycultures that included a non-host plant (beans in our case) than from host monocultures (Risch, 1981). When distance between collards is increased or confounded by the presence of other plant species, movements of flea beetles decrease and their distribution becomes increasingly random with respect to the location of high-quality collards (Kareiva, 1982). However, in the present experiment this was not reflected in increased variability in the amount of damage. It is also reasonable to hypothesize that the observed abundance and herbivory patterns displayed by flea beetles can be explained by chemical interactions. Field experiments have shown that the mustard oil present in many crucifers, allylisothiocyanate, is a powerful attractant to adults of P. cruciferae (Feeny, Paauwe and DeMong, 1970). Weedy species such as Brassica nigra have foliage concentrations of this glucosinolate 32 times higher than those found in cultivated crucifers (Cole, 1976). Although we did not performa chemical analysis of the plants involved, it is reasonable to expect higher concentrations of this glucosinolate in B. campestris than on collards (Kjaer, 1976), and therefore the preference of flea beetles for B. campestris (instead of collards) may simply reflect differing degrees of adaptation to the foliage levels of this particular glucosinolate in the weeds and collards. Acknowledgements Research reported here was supported by a grant from the University of California Appropriate Technology Program. References BACH, C.E. (1980). Effects of plant density and diversity on the population dynamics of a specialist herbivore, the striped cucumber beetle, Acalymma vittata (Fab.). Ecology 16, 1515 1530. COLE,R.A. (1976). Isothiocyanates, nitriles and thiocyanates as products of autolysis of glucosinolates in cruciferae. Phytochemistry 15, 754-762. CROMARTIE,W.J. (1981). The environmental control of insects using crop diversity. In: CRC Handbook of Pest Management in Agriculture, Vol. 1, pp. 223-250. (ed. by D. Pimentel). CRC Handbook Series in Agricultue. Boca Raton, Fla: CRC Press. FEENY,P., PAAUWE,K. ANDDEMONG,N. (1970). Flea beetles and mustard oils: host plant specificity of Phyllotreta cruciferae and P. striolata adults (Coleoptera:Chrysomelidae). Annals of the Entomological Society of America 63, 832-841. KAREIVA,P. (1982). Exclusion experiments and the competitive release of insects feeding on collards. Ecology 62, 696-704. KJAER,A. (1976). Glucosinolates in the CrUciferae. In: The Biology and Chemistry of the Cruciferae, pp. 207-219. (ed. by J.G. Vaughn and A.J. MacLeod). New York, Academic Press. MAYSE, M.A., PRICE, P.W. AND KOGAN, M. (1978). Sampling methods for arthropod colonization studies in soybean. Canadian Entomologist 110, 265-274. RISCH, S.J. (1981). Insect herbivore abundance in tropical monocultures and polycultures: An experimental test of two hypotheses. Ecology 62, 1325-1340. RooT, R.B. (1973). Organization of a plant-arthropod association in simple and diverse habitats: The fauna of collards (Brassica oleracea). EcologicalMonographs 43, 95-124. TAHVANAINEN,J.O. ANDROOT,R.B. (1972). The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera:Chrysomelidae). Oecologia 10, 321-342. Accepted 22 March 1983
Effects of plant diversity on the density and herbivory of the flea beetle, Phyllotreta cruciferae Goeze, in California collard (Brassica oleracea) cropping systems MIGUEL A. ALTIERI
Division of Biological Control, University of California, Berkeley CA 94720, USA AND STEPHEN R. GLIESSMAN
Agroecology Program, Environmental Studies, University of California, Santa Cruz CA 95064, USA ABSTRACT. Populations of the flea beetle, Phyllotreta cruciferae Goeze (Coleoptera:Chrysomelidae), were' greater in weed-free collards than in collard monocultures and polycultures (intercropped with beans) left weedy for 2 or 4 weeks after transplanting or for the entire season. Flea beetle densities and amount of leaf damage per individual collard plant were significantlylower in the plots with crucifer weeds (mainly Brassicacampestris L.), possibly because the beetles preferred to feed and/or concentrate on this plant rather than on collards.
Introduction Cruciferous crops have been extensively used as model systems to test the hypothesis that vegetational diversity results in lower pest loads in agricultural systems (Cromartie, 1981). Most studies have shown a reduction in the abundance of particular herbivores in diversified cole crops when compared with monocultures. One such herbivore is the specialized crucifer-feeding flea beetle, Phyllotreta cruciferae Goeze (Coleoptera:Chrysomelidae). These flea beetles are quick colonizers ofcruciferous hosts growing in dense or nearly pure stands (Root, 1973), and will remain on these plants, depending on the vigour and quality of the host plants (Kareiva, 1982). However, when a particular host plant is grown intermingled with other non-host plants, the flea beetles may experience difficulty in locating and remaining°on the host plant (Tahvanainen and Root, 1972). Apparently, visual or 0261-2194/83/04/0497-05503.00 © 1983 Butterworth & Co (Publishers) Ltd
498
Plant diversity effects on flea beetles in collards
chemical stimuli from non-host plants can affect both the rate of colonization of the flea beetles and their tenure time on the host plants (Risch, 1981). This study was designed to investigate the role of plant diversity in the population dynamics of P. cruciferae and their feeding impact on collards (Brassica oleracea), when collards were grown with other cruciferous hosts, or other non-hosts (i.e. beans), or both. Materials and methods On 17 July 1981 an area of 3000 m 2 was ploughed, cultivated and divided into 24 plots each measuring 5 m 2 at the University of California's Santa Cruz farm and garden. The distance between plots was 5 m, and these interplot areas were kept free of vegetation by frequent harrowing. All plots were fertilized with chicken manure (1 kg/m2; 25 kg/plot) and sprinkler-irrigated when needed. Treatments were randomly assigned and each replicated three times: 1. 2. 3. 4. 5. 6. 7. 8.
Collard (cv. Georgia) monoculture kept weed free by hoeing all season. Collard monoculture kept weed-free for only 2 weeks after transplanting.* Collard monoculture kept weed-free for only 4 weeks after transplanting.* Collard monoculture weedy all season. Collard/field-bean (var. horticultural dwarf) polycultures kept weed-flee all season. Polycultures weed-free for 2 weeks post-transplant.* Polycultures weed-free for 4 weeks post-transplant.* Polycultures weedy all season.
In the monocultures and polycultures, 20-day-old greenhouse-grown collards (about 8-12 cm tall) were transplanted equidistantly at a density of 90 plants per plot. In the polycultures, 90 bean seeds were planted simultaneously between collards. Brassica campestris was the dominant weed in the 'weedy' plots, while Raphanus spp., Spergula arvensis, Convolvulus arvensis and Anagallis arvensis occured as several individuals but with cover less than 4% of the total plot area. Densities of flea beetles were estimated by directly counting the number of beetles found on 10 randomly selected collard and five B. campestris plants in each plot on three occasions (15, 30 and 45 days after transplanting). Direct observation was used because it has proved to be a very effective and accurate sampling method; however, its efficiency could be affected by the heterogeneity of the vegetation associated with the plants being sampled (Mayse, Price and Kogan, 1978; Bach, 1980). At these times, the number of leaves with flea-beetle damage (with holes larger than 0.5 cm 2) in each of the 10 collard plants was recorded. Flea beetle damage was distinguished as a pit feeding injury, as opposed to the strip feeding which is typical of lepidopterous larvae. Plant biomass in each plot was determined from oven-dried samples of collards and weeds clipped from 1 m 2 quadrats at harvest time (70 days after planting). To compare flea beetle densities between treatments, an analysis of variance was utilized to test for effects of diversity. The analysis was performed on three replicate plots for each combination of treatments. Differences in beetle densities were separated by Duncan's new multiple range test. * All 2- or 4-weekregimesare termed 'relaxed' weedingregimesin the text.
Weed-free all season Weed-free for 4 weeks after collard transplanting Weed-free for 2 weeks after collard transplanting Weedy all season
Collard-bean polycultures
Weed-free all season Weed-free for 4 weeks after collard transplanting Weed-free for 2 weeks after collard transplanting Weedy all season
Collard monocultures
Cropping system
13.1 + 6"5 d 15.0+7'8 d
4"9 + 2'3 c 0-6+0"5 e
6'7 d 32.1 c
10.9 d
4'3 +3'3 c
44'5 b 29.9 c
1-6+0.9 d
73'7+20'1 a 25"0 + 11'5 b
29.0+ 1.7 b 6-6 + 3"8 c
44"6 b
34.1 c
78" 1 + 16.3 a
29"3 + 1-7 b
54"4 a
2'3 + 1' 1 d
--
34'0 + 2.6 a
No. of flea beetles ( + SE)
84 85
28
0
52 142
42
0
93.2 234.5
25.7
0
55.2 438.2
52.3
0
309"4 115.2
324.0
334'4
243.0 226.1
361"3
213"6
Leaves in each collard plant with beetle damage (45 days Whole~-plant collard Per 10 Per 5 after transplanting) Weed density Weed biomass dry weight collard plants Brassica campestris plants (%) (individuals/m z) (g/m z) (g/m 2)
TABLE 1. Mean flea beetle (Phyllotreta cruciferae) densities, weed and crop biomass in various collard cropping systems in Santa Cruz, California. Means followed by the same letter in each column are not significantly different ( P = 0-05). All means are averages of three sampling dates (15, 30 and 45 days after transplanting)
Z
Z
Z
500
Plant diversity effects on flea beetles in collards
Results
Noticeable populations of P. cruciferae were present only during the first 45 days after transplanting. After this period, densities per plant dropped to a level of less than one flea beetle per collard, regardless of treatment. Flea beetle densities (expressed as mean densities for the three census dates: 15, 30 and 45 days after transplanting) were significantly greater in the weed-free collard monocultures than in all other treatments (Table 1). These differences in beetle numbers were consistent on the three sampling dates. A peak in numbers was apparent for all monoculture plots (except those which were weedy all season) at 30 days. This pattern was not apparent for polycultures. Allowing weed growth during selected periods of the crop cycle (2-4 weeks weed-free or weedy all season) resulted in lower flea beetle densities in the weedy monocultures than in the weed-free monocultures. Lowest densities occurred in systems allowed to remain weedy all season: no differences in the abundance of beetles were observed between collards kept weed-free for 2-4 weeks after transplanting. Even lower flea beetle densities were observed in collards intercropped with beans, especially in polycultures left weedy the entire season. In both monocultures and polycultures with 'relaxed' weeding regimes, flea beetle densities were at least five times greater on a per plant basis on Brassica campestris (the dominant plant of the weed community) than on collards. B. campestris germinated quickly and flowered early, each plant averaging a height of 39 cm, with 12 leaves and 16 open flowers, 60 days after germination. This apparent preference of P. cruciferae for B. campestris over collards resulted in a higher concentration of flea beetles on the wild crucifer, diverting flea beetles from collards and consequently diluting their feeding on the collards. As shown in Table 1, collards grown under various levels of weed diversity and/or polycultural patterns exhibited significantly less leaf damage than monoculture collards grown in weed-free situations. Plots in which weeds were suppressed during the initial 2-4 weeks of crop establishment showed lower weed growth than plots allowed to remain weedy all season. In all-season weedy polycultures there was significantly lower weed biomass than in all-season weedy monocultures. Apparently, the shading provided by the overlapping bean and collard canopies helped to suppress weeds. There appeared to be two patterns in collard yields: collards had higher biomass in the weed-free polycultures than in the weed-free monocultures, and weed competition did not seem to reduce collard growth in the all-season weedy monoculture, as it did in the collard all-season weedy polyculture.
Discussion a n d conclusions Increased plant diversity, in the form of'relaxed' weeding regimes or intercropping patterns, led to lower population densities of P. cruciferae. In our particular study, the effects of plant diversity on flea beetle populations could have been due to several interacting variables, such as host and non-host plant density and total plant density, which vary with diversity. It is obvious that flea beetles had to explore a much higher density of host and non-host plant material in the diversified monocultures and polycultures: they therefore might have experienced greater difficulty in locating suitable collard plants. It is possible that, once they located a suitable collard, the
MIGUEL A. ALTIERI AND STEPHEN R. GLIESSMAN
501
time that they spent on that plant depended both on plant quality and the nature of the associated plants. Studies have shown that certain Chrysomelid beetles tend to emigrate more from polycultures that included a non-host plant (beans in our case) than from host monocultures (Risch, 1981). When distance between collards is increased or confounded by the presence of other plant species, movements of flea beetles decrease and their distribution becomes increasingly random with respect to the location of high-quality collards (Kareiva, 1982). However, in the present experiment this was not reflected in increased variability in the amount of damage. It is also reasonable to hypothesize that the observed abundance and herbivory patterns displayed by flea beetles can be explained by chemical interactions. Field experiments have shown that the mustard oil present in many crucifers, allylisothiocyanate, is a powerful attractant to adults of P. cruciferae (Feeny, Paauwe and DeMong, 1970). Weedy species such as Brassica nigra have foliage concentrations of this glucosinolate 32 times higher than those found in cultivated crucifers (Cole, 1976). Although we did not performa chemical analysis of the plants involved, it is reasonable to expect higher concentrations of this glucosinolate in B. campestris than on collards (Kjaer, 1976), and therefore the preference of flea beetles for B. campestris (instead of collards) may simply reflect differing degrees of adaptation to the foliage levels of this particular glucosinolate in the weeds and collards. Acknowledgements Research reported here was supported by a grant from the University of California Appropriate Technology Program. References BACH, C.E. (1980). Effects of plant density and diversity on the population dynamics of a specialist herbivore, the striped cucumber beetle, Acalymma vittata (Fab.). Ecology 16, 1515 1530. COLE,R.A. (1976). Isothiocyanates, nitriles and thiocyanates as products of autolysis of glucosinolates in cruciferae. Phytochemistry 15, 754-762. CROMARTIE,W.J. (1981). The environmental control of insects using crop diversity. In: CRC Handbook of Pest Management in Agriculture, Vol. 1, pp. 223-250. (ed. by D. Pimentel). CRC Handbook Series in Agricultue. Boca Raton, Fla: CRC Press. FEENY,P., PAAUWE,K. ANDDEMONG,N. (1970). Flea beetles and mustard oils: host plant specificity of Phyllotreta cruciferae and P. striolata adults (Coleoptera:Chrysomelidae). Annals of the Entomological Society of America 63, 832-841. KAREIVA,P. (1982). Exclusion experiments and the competitive release of insects feeding on collards. Ecology 62, 696-704. KJAER,A. (1976). Glucosinolates in the CrUciferae. In: The Biology and Chemistry of the Cruciferae, pp. 207-219. (ed. by J.G. Vaughn and A.J. MacLeod). New York, Academic Press. MAYSE, M.A., PRICE, P.W. AND KOGAN, M. (1978). Sampling methods for arthropod colonization studies in soybean. Canadian Entomologist 110, 265-274. RISCH, S.J. (1981). Insect herbivore abundance in tropical monocultures and polycultures: An experimental test of two hypotheses. Ecology 62, 1325-1340. RooT, R.B. (1973). Organization of a plant-arthropod association in simple and diverse habitats: The fauna of collards (Brassica oleracea). EcologicalMonographs 43, 95-124. TAHVANAINEN,J.O. ANDROOT,R.B. (1972). The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera:Chrysomelidae). Oecologia 10, 321-342. Accepted 22 March 1983