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Soil-fertility management and host preference by European corn borer, Ostrinia nubilalis (Hübner), on Zea mays L.: A comparison of organic and conventional chemical farming
Agriculture Ecosystems& Envwonment ELSEVIER
Agriculture,
Ecosystems
and Environment
56 ( 1995) 1-8
Soil-fertility management and host preference by European corn borer, Ostrinia nubilalis (Hiibner), on Zea mays L.: A comparison of organic and conventional chemical farming P. L. Phelan *, J. F. Mason, B. R. Stinner Depurtment
of Entomology,The Ohio Agricultural Research & Development Center, The Ohio State University, Wooster, OH 44691, USA Accepted
11 August 1995
Abstract It has long been argued by proponents of organic agriculture that crop losses to insects and diseases are reduced by this farming method, and that reduced susceptibility to pests is a reflection of differences in plant health, as mediated by soil-fertility management. These reports although widespread are mostly anecdotal and largely without experimental foundation. In this study, the effects of two parameters of soil fertility on the host-preference behavior of an insect pest were measured: ( 1) the immediate effect of organic vs. inorganic fertilizers and (2) the long-term effect of soil -management history. Soils were collected from three pairs of neighbouring farms, each pair matched for soil type and compnsing organic and conventional chemical production systems. Each soil was potted and amended with mineral fertilizers, animal manures, or left amended. After planting the amended soils with maize (Zeu muys L.) in a greenhouse, European corn borer females (ECB), Ostriniu nubilalis (Httbner), were released to determine egg-laying preferences. For each of the three farm comparisons, there was a significantly higher level of ECB oviposition on plants in conventional soil. In two comparisons, there was also a significant amendment effect; however, the specific fertilizers leading to greater egg laying were not consistent among farm comparisons. Thus, the form of the fertilizer did not have consistent effects on maize susceptibility to ECB, but soil-management history did. Moreover, there was significant variation in egg laying among fertilizer treatments within the conventionally managed soil, but for plants in the organic soils, egg laying was uniformly low. Pooling results across all three comparisons, variance in egg laying was about 18 times higher among plants in conventional soil than among plants in organic soil. It is suggested that this difference is evidence for a form of biological buffering characteristic of organically managed soils. Also significant, ECB ovipositional preference did not correlate with plant biomass. Thus, these results suggest that soil-management practices can significantly affect the susceptibility of crops to pests, and do so without adversely affecting plant productivity. Kewwrd.s:
Soil management;
Organic farming; Host selection; Ovipositional
1. Introduction One of the long-held contentions of those employing organic-farming practices is that these agricultural sys* Corresponding author: Tel. 216-263-3728, Email. [email protected].
Fax. 216-263-3686,
0167~8809/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDIOl67-8809(95)00640-O
preference;
Crop resistance
terns reduce the occurrence of insect and disease outbreaks (Howard, 1940; Oelhaf, 1978). Although this view is widespread, there have been surprisingly few attempts to test its validity. Lower pest pressure in organic systems could result from the greater use of crop rotation and/or preservation of beneficial insects in the absence of pesticides. Alternatively, another fun-
2
P.L. Phelan et al. /Agriculture,
Table I Nutrient levels prior to experiment
CEC
pH
Ecosystems and Environment 56 (199.5) l-8
in soils collected from paired organically
% Org. Mat.
%N
and conventionally
managed farms
Nutrient level (Kg ha- I )
% Base Sat.
N@N
P
K
Mg
Ca
K
Mg
Ca
Furm Comptrrison I Organic 13 Conventional 9 Farm Compwison 2
5.2 6.8
4.4 2.9
0.24 0.16
75 45
19.5 179
544 325
344 421
1728 3018
4.8 4.3
10 18
30 78
Organic 11 Conventional IO Frrrm Compurison 3 Organic 7 Conventional 9
6.1 5.8
4. I 2.9
0.22 0.16
135 10
119 193
352 887
573 488
3466 2333
3.5 9.7
19 17
67 50
6.2 6.1
2.9 2.8
0.16 0.15
15 1s
29 92
138 374
354 344
2636 2726
2.1 4.8
18 14
80 68
damental axiom ascribed by organic farming is that “healthy soil produces healthy plants,” which are more resistant to insects and disease (Geisler, 1988; Luna, 1988). Although healthy soil is difficult to define, it has been argued that fertility practices that replenish and maintain high soil organic matter and that enhance the level and diversity of soil macro- and microbiota provide an environment that by some unknown process enhances plant health (Merrill, 1983). If soil-fertility practices do impact the physiological susceptibility of crops to insects and disease, two possible causes can be identified: the immediate effect of the amount and form of fertilizer used, e.g. animal manures vs. inorganic fertilizers, and the long-term effect of soil management history. Although there is an extensive literature documenting the relations between levels of individual plant nutrients and herbivore performance (Dale, 1988), virtually nothing is known about how either the form of nutrient input or the history of soil management affect pest performance. Here results are presented of greenhouse studies on soil collected from adjacent organic and conventional farms. After amending with either mineral nitrogen or organic manures, maize plants in these soils were compared for their propensity to elicit egg laying by European corn borer (ECB) , Ostrinia nubilalis (Hiibner)
2. Materials and methods 2.1. Soil-management
history
Soils were collected from paired farms, with one utilizing organic practices and a second adjacent farm
using conventional methods of tillage, fertility, and pesticide input. The organic farms in this study managed soil fertility using a combination of animal manures and different crop rotations (described below), and each of the conventional farms used inorganic fertilizers and a maize-soybean (Glycine mm) rotation. Soils were collected from the top 15 cm, taking care to match soil type within a farm pair. Where possible, samples from the two farms were taken from adjoining fields, but at least 8 m from field boundaries. Soil collections from within each farm were combined, mixed thoroughly, and sieved with a 1.2 cm X 1.2 cm holed screen to remove larger stones. Subsamples then were taken for soil analysis of nutrients and organic matter (Table 1) . For Farm Comparison 1, soil samples were collected in late August 1992. The farms were located in Wayne County, Ohio, with the collection sites about 100 m apart. The organic farm had been under organic management for 7 years with a rotation of alfalfa/grass, maize, maize, and oats interseeded with alfalfa/grass. Straw-packed dairy-cow manure was added at 12 OOO16 000 kg ha- ’before first-year maize and 20 000-24 000 kg ha-’ before second-year maize. The soil type was Canfield silt-clay loam and both the organic and conventional fields were planted in first-year maize at the time soil was collected. The paired fields of Farm Comparison 2 were located in Knox County, Ohio and were divided by a small dirt lane; collection sites were separated by about 25 m. The organic farm, which had been under organic management for 25 years, followed a rotation of red clover/grass, maize, soybeans, and wheat or oats. Straw-packed dairy-cow manure was
P.L. Phelun et al. /Agriculture,
Ecosystems and Environment
added at about 12 000 kg ha- ’before maize. The soil type for both fields was Chili silt-clay loam, and samples were collected in late November 1992. The conventional field had been last planted in maize, and the organic field was coming out of 14 months clover following wheat. The conventional field had been chisel plowed and the organic field disk plowed the preceding autumn. Soil for Comparison 3 was collected in February 1993 from adjoining farms located in Holmes County, Ohio. The organic farm was an Amish farm that had used horsedrawn tillage with a rotation of red clover/alfalfa/grass, maize, and wheat or oats for 75 years. Straw-packed dairy-cow manure was applied at approximately 33 000 kg ha- ’ before maize. The soil type was Canfield silt-clay loam; the sampled fields had both been in first-year maize the previous year and collection sites were separated by about 100 m. 2.2. Greenhouse studies For the first farm comparison, the two soils were placed in pots (2 1.6 cm diam X 20.3 cm high) and each soil type was amended for nitrogen using: (1) NH,NO?, (2) fresh dairy-cow manure, or (3) left unamended. Treatments for Comparisons 2 and 3 were the same except composted manure was also included. Rates of application were 164 kg ha-i N for each amendment based on the surface area of the soil top. For manures, this rate was based on total N as measured by nutrient analysis of each manure sample. All pots were watered and held for 1 week, then planted with four seeds of Zea mays L. (sweetcorn cv. Northern Extra Sweet). Plants were thinned to one per pot after reaching a height of 30-40 cm. Pots were arranged in a greenhouse using a randomized complete-block design, and the positions of pots within a block were rerandomized on a weekly basis. Supplemental lighting was provided by 400 W high pressure sodium lamps, spaced two per 3. I m X 1.8 m bench at a height of 1.3 m above the benches. The lights were maintained on a 16 h daylength. Temperatures typically ranged 2133°C during the day and 18-29°C during the night. A computer-controlled Greenhouse Environmental Manager (Q-Corn Corp., Santa Ana, CA) maintained temperatures, and monitored humidity and light levels. ECB pupae were obtained from the USDA-ARS Corn Insects Research Unit (Ankeny, IA). Two to 5 day old ECB adults were released twice per week into the
56 (1995) l-8
3
greenhouse, and plants were examined every 2-3 days for ECB eggs. Eggs were counted and removed, and their position on the plant recorded. Plant height and leaf stage (number of leaves with collars showing) and ECB egg laying were monitored until physiological maturity of the maize. Pots were watered as needed with deionized water. Dry weights of roots and shoots were determined at the end of Comparisons 2 and 3, with only shoot dry weight determined for Comparison 1. Plant growth and ECB ovipositional response were analyzed within each comparison by three-way ANOVA to determine the relative effect of soil source, form of N amendment, soil amendment interaction, and blocks (Snedecor and Cochran, 1980). Means were separated using Fisher‘s protected LSD when a significant soil-amendment interaction was indicated. Soil and amendment effects on variance in plant growth and ECB response across the three comparisons were also determined. Plant-growth data were standardized by dividing by the mean value for that farm comparison; egg laying was expressed as the proportion of total eggs for a comparison and was transformed by sin-‘x”‘. Relative variability between soils and among amendments was measured by the ratio of the variances (Fstatistic). Because these data are not independent and probably not normally distributed, a Monte Carlo approximation to the Permutation test was used to determine the probability of equal variances (Scheffe, 1959). Data sets were randomly resampled with replacement 10 000 times using the Resampling Stats computer program (Resampling Stats, Arlington, VA) to estimate P.
3. Results 3.1. Farm comparison 1 Release of ECB females was initiated during the 45th leaf stage, when plants were about 66% of their final height. Significant differences in egg laying were measured during the first 2 weeks of ECB release; Fig. la reflects the ovipositional response during this period. ANOVA of egg laying indicated a significant soil effect (F= 5.68, 135 d.f., P = 0.02) and amendment effect (F= 13.89, 235 d.f., P< 0.001). In addisoil Xamendment tion, there was a significant
4
2
P.L. Phelun et al. /Agriculture.
Ecosystems and Environment
(F= 6.02, 235 d.f., P = 0.006)) with no significant interaction, were measured for final plant height (data not shown). Mean heights for plants in conventional and organic soils were 105 cm and 98 cm, respectively. Most of the difference in plant height was attributable to plants in conventional soil amended with fresh manure, which were significantly taller than those in other treatments. Notably, although these plants were about 10% taller than manure-amended plants in organic soil, their shoot biomasses were equivalent (Fig. lb).
200
ii
2 P
H 100 0 Unamended
NH4N03
Fresh
Manure
Amendment 20
/
56 (1995) 1-R
/
3.2. Farm comparison 2 Release of ECB females began in the 5-&h leaf stage, when plants were about 66% of their final height 150
a)
T
120 K h ii w” Unamended
NH4N03
Fresh
90
Manure
Amendment 60
Fig. I. Farm Comparison I: (a) mean numbers of eggs laid by European corn borer females on and (b) final mean shoot biomass of maize plants grown in a greenhouse. Plants were grown in soils collected from either organically (solid bars) or conventionally (cross-hatched bars) managed farms, and were amended with NH4N03, fresh manure, or left unamended. T-bars denote standard errors: bars marked by the same letter are not significantly different by Fisher’s protected LSD when a significant soil-amendment interaction was indicated by ANOVA (n = 8)
interaction (F = 11.44, 235 d.f., P < 0.001) . Eggs laid per plant averaged 108 and 63 for conventional and organic soils, respectively. Between-soil differences in egg laying were caused almost solely by the greater number of eggs laid on plants in conventional soil amended with fresh manure, which were three to eight times higher than on any other treatment (Fig. la). ANOVA of shoot dry weight at harvest showed a nearly significant soil effect (F= 3.43, 135 d.f., P = 0.07), a significant amendment effect (F = 6.79, 235 d.f., P=O.O03), and no significant interaction (F=0.82, 235 d.f., P=O.45; Fig. lb). Mean dry weight for plants in organic and conventional soils were 12.8 g and 15.2 g, respectively. Significant effects of soil (F= 9.45, 135 d.f., P=O.O04) and amendment
30 Unamended
NH4N03
Fresh
Manure
Comp.
Manure
Manure
Camp.
Manure
Amendment
““amended
NH4N03
Fresh Amendment
Fig. 2. Farm Comparison 2: (a) mean numbers of eggs laid by European corn borer females on and (b) final mean shoot biomass of maize plants grown in a greenhouse. Plants were grown in soils collected from either organically (solid bars) or conventionally (cross-hatched bars) managed farms, and were amended with N&N03, fresh or composted manure, or left unamended. T-bars denote standard errors; bars marked by the same letter are not significantly different by Fisher’s protected LSD when a significant soil-amendment interaction was indicated by ANOVA (n = 6).
P.L. Phelun et (11./Agriculture. Ecosystems and Environment 56 (1995) I-8
(77.2-99.0 cm). As with Comparison I, the greatest differences in ECB egg laying was observed for the first 2 weeks of ECB release (Fig. 2a). ANOVA measured a significant soil effect (F=6.99, 128 d.f., P=O.Ol), with plants in conventional soil averaging 105 eggs per plant vs. 70 eggs per plant for those in organic soil. There were no significant amendment (F=0.61,328d.f.,P=0.58) orinteraction(F=0.66, 328 d.f., P = 0.58) effects, although between-soil differences in egg laying were greatest for the unamended and NH,NO,-amended plants. Treatment differences were measured in shoot biomass because of a significant amendment effect (F = 4.49,328 d.f., P = 0.01)) but not a significant soil effect (F=2.14, 128 d.f., P=O.15). There was alsoa significant soil-amendment interaction (F= 6.52, 328 d.f., P = 0.002) because of the differential response to amendments in the two soils. Plants amended with composted manure in the organic soil produced the greatest shoot mass, with fresh-manure-amended and NH,NO,-amended plants in organic soil intermediate between compost-amended and unamended plants (Fig. 2b). In the conventional soil, amendments did not significantly increase shoot biomass relative to the unamended soil. Root biomass (not shown) followed the same pattern as shoot mass, with no significant soil effect (F= 0.0, 128 d.f., P= 0.98), but a significant amendment effect (F= 2.98, 328 d.f., P= 0.05) and interaction (F= 5.91, 328 d.f., P = 0.003). Despite these differences in plant biomass, there was no significant soil, amendment, or interaction effects on final plant height (F < 1.O for each) ; plant heights were 135 cm and 138 cm for organic and conventional soils, respectively. 3.3. Farm comparison
3
350
300
$ a
250
ii w” i
200
150
100 Unamended
NH4NOB
Fresh
Manure
Comp. Manure
Manure
Comp. Manure
Amendment 40
-
30 3 5’ f 0
20
i; 2 m 10
0 Unamended
NH4N03
Fresh Ame”dme”t
8o/ cl
Unamended
T
NH4N03
Manure
i
Compost
Amendment
Release of ECB females was initiated at the 4th-5th leaf stage, when plants were about 56% of their final height (55.7-77.3 cm). Differences in ECB egg laying were observed for about the first 4 weeks (Fig. 3a). ANOVA measured a significant soil effect (F=6.13, 135 d.f., P= 0.02), with plants in conventional soil averaging 201 eggs per plant vs. 159 eggs per plant for those in organic soil. There was also a significant amendment effect (F = 7.82,335 d.f., P = 0.001)) with NH,NO,-amended plants receiving the greatest number of eggs, and a significant interaction effect
Fig. 3. Farm Comparison 3: (a) mean numbers of eggs laid by European corn borer females on and (b) final mean shoot biomass of maize plants grown in a greenhouse, and (c) percentage of earlystage plants developing symptoms of an unidentified disease. Plants were grown in soils collected from either organically (solid bars) or conventionally (cross-hatched bars) managed farms, and were amended with NH,NO,, fresh or composted manure, or left unamended. T-bars denote standard errors; bars marked by the same letter are not significantly different by Fisher‘s protected LSD when a significant soil-amendment interaction was indicated by ANOVA (n = 5). Percentages of disease incidence were transformed by sin‘xl” before analysis.
6
P.L. Phelan et al. /Agriculture, Ecosystems and Environment 56 (1995) 14
(F=3.95, 335 d.f., P=O.O2) because egg laying on the NH,N03-amended and compost-amended plants was elevated only in conventional soil, not in organic soil. Significant differences in shoot weights in this comparison were attributable solely to amendment effects (F = 17.11, 335 d.f., P < 0.001 ), without a significant soil effect (F = 0.38, 135 d.f., P = 0.54) or soil-amendment interaction (F = 0.03, 335 d.f., P = 0.99). Plants fertilized with NH4NOS produced the greatest shoot mass in both soils (Fig. 3b). Composted and fresh manure produced shoot mass intermediate to unamended and NH,N03-amended plants. Root mass was also significantly affected only by amendment (F= 12.78, 315 d.f., P
3.4. Treatment effects on variability in plant growth and ECB response In addition to effects on mean values of plant growth and insect response, soil-management history and fertilizers were analyzed across farm comparisons for effects on the variability in these parameters. Variance in oviposition was 17.8 times higher for plants in conventionally managed soil than for those in organic soil (P = 0.0024 measured by the Permutation test). In contrast, no significant differences in the variability of egg laying were measured among fertilizers. Likewise, variances in plant growth were very similar between soils and among fertilizers.
4. Discussion Despite the potential practical and biological significance of understanding how soil-fertility management affects crop susceptibility to pests, rather few attempts have been made to examine this relationship. Results of paired on-farm studies, although few in number, generally support the anecdotal reports of lower pest pressure in organic-production systems (Kowalski and Visser, 1979; Andow and Hidaka, 1989; Kajimura et al., 1993). In all three studies, evidence suggested that differences in plant physiology may have mediated pest levels. In contrast, natural enemies did not appear to explain lower pest levels on organic farms in these studies, as predator and parasite populations were either comparable between farm pairs or were higher in conventionally managed fields. Effects of the form of fertilizer on pests have been less clear. For example, Culliney and Pimentel ( 1986) measured higher Phyllotreta flea beetles populations on sludge-amended collard (Brassica oleracea) plots early in the season compared to mineral-fertilizeramended and unfertilized plots, but later in the season, in these same plots, population levels were lowest for beetles, as well as for aphids and lepidopteran pests. Plant growth followed the inverse pattern, with the sludge treatment producing the largest plants and the unfertilized soil producing the smallest. Crop susceptibility to pests is determined by both adult behavioral response (host finding and oviposition) and larval developmental response (efficiency of food conversion, developmental rate, and survival-
P.L. Phelan et al. /Agriculture, Ecosystems and Environment 56 (1995) l-8
ship). This study focused on the former as a first step towards understanding how soil management can affect ECB outbreaks. The present results extend the previous demonstrations of the effects of soil-managementpractices on crop pests and advance our understanding of this relationship by experimentally partitioning the contributions of fertilizer form and soil-management history. Because soils were compared from three pairs of farms, it can be concluded that soil-management effects were not the result of the unique conditions of any one location. On the contrary, management-history effects appear important, because in each of the three farm comparisons, plants in conventional soil received more ECB eggs overall. Second, by testing ECB response in the greenhouse, crop rotations and natural enemies can be excluded as direct causes for the differences found (this is not to diminish their possible significance in the farm setting, and crop-rotation history may have affected pests indirectly through changes in the soil). Rather, the results strongly suggest that soil-fertility management can significantly alter plant acceptability to ECB. Third, although a significant amendment effect was measured in two of three comparisons, the specific amendments leading to greater egg laying differed. In Farm Comparison 1, egg laying was higher on fresh-manure-amended plants in conventional soil than on all other treatments (Fig. la), but in Comparison 3 (Fig. 3a), egg laying was elevated for NH,NO,-amended and compost-amended plants in conventional soil. Thus, effects of the form of fertility (manures vs. inorganic) appeared dependent on the context of the soil onto which they were applied. This finding suggests an explanation for the incongruity among previous studies of the effects of fertilizer form on pests. To understand the link between fertility management and crop susceptibility to insects, it is particularly important to note that in the present study, although main effects were measured for soil history in each of the three comparisons, ECB egg laying generally was elevated in conventional-soil treatments only for one or two fertilizer treatments. This was particularly true 1 and 3, as reflected by significant for Comparisons interactions between soil and amendment in thesecomparisons. Thus, planting in the conventional soils did not necessarily lead to higher egg laying, but did increase its probability, depending on the fertilizer added. In contrast, ECB susceptibility remained uni-
7
formly low among plants in organic soils, irrespective of fertilizer amendments. This between-soil difference resulted in a significantly higher variance in egg laying on plants in conventional soils across the three comparisons. Studies indicate that organic management practices can enhance soil quality and reduce environmental stress on plants by improving soil structure and by increasing its capacity to buffer pH and levels of moisture and mineral nutrients (Rongjun, 1989; Arshad and Coen, 1992). In an analogous manner, the present results may represent the first evidence that long-term management of soil organic matter can also lead to buffering of a higher order, that of a plant‘s ability to resist insect pests. From a practical perspective, it is also notable that ECB ovipositional preference was not related to plant productivity (biomass). There was no consistent pattern in plant biomass with regard to either management history or the form of fertilizer among the three comparisons. Even within a soil type, there was no correlation between plant productivity and ECB ovipositional preference, indicating that ECB females did not simply prefer the largest plants. This lack of correlation between plant productivity and non-genetic resistance contrasts with the trade-off between plant growth and genetically based herbivore resistance commonly observed in natural plant populations (e.g., Cates, 1975; Berenbaum et al., 1986; Kakes, 1989). Crop-breeding programs have also frequently found an inverse relationship between insect resistance and yield (e.g. Klenke et al., 1986). Thus, the present studies suggest that non-genetic resistance to pests through plant fertility need not come at the expense of crop yield. In summary, the significance of the present study is in demonstrating that the ovipositional preference of a foliar pest can be mediated by soil differences in fertility-management history. Thus, the lower pest levels widely reported in organic-farming systems may, in part, arise from biochemical or mineral-nutrient differences in crops under such management practices, as investigated elsewhere (Phelan et al., 1995). The lower level ofECB oviposition on maize grown in organically managed soil, in addition to the higher variability of ECB response to maize in conventional soil, suggest that the buffering of soil processes previously attributed to high soil organic matter and microbial activity may
8
P.L. Phelan et al. /Agriculture, Ecosystems and Environment 56 (1995) I-8
also extend to the interactions ground herbivores.
of plants and above-
Acknowledgements The authors are indebted to L. Lewis and J. Dyer of the USDA-ARS Corn Insects Research Laboratory for rearing the insects used in this study. They also thank cooperating farmers for providing soils: J. Hartzler, A. Hostetler, D. Kline, B. Kohl, R. and G. Spray, and M. Yoder. Statistician B. Bishop aided in the analysis of the results, and R. Hammond, R. Lindquist, D. McCartney, and E. Zaborski provided critical reviews of the manuscript. Salaries and research support were provided by state and federal funds, Ohio Agricultural Research and Development Center Journal No. 18093.
References Andow, D.A. and Hid&, K., 1989. Experimental natural history of sustainable agriculture: Syndromes of production. Agric. Ecosystems Environ., 27: 447-462. Arshad, M. A. and Coen, G. M., 1992. Characterization of soil qua_ity: Physical and chemical criteria. Am. J. Altemat. Agric., 7: 25-31. Berenbaum, M.R.. Zangerl, A.R. and Nitao, J.K., 1986. Constraints on chemical coevolution: Wild parsnips and the parsnip webworm. Evolution, 40: 1215-1228. Cates, R.G., 1975. The interface between slugs and wild ginger: Some evolutionary aspects. Ecology, 56: 391&400. Culliney, T.W. and Pimentel, D., 1986. Ecological effects of organic agricultural practices on insect populations. Agric. Ecosystems Environ., 15: 253-266. Dale, D., 1988. Plant-mediated effects of soil mineral stresses on insects. In: E.A. Heinrichs (Editor), Plant Stress-lnsect Interactions Wiley, New York, pp. 35-l 10.
Geisler, F.R., 1988. Effects of organic manures on a host crop-pest relationship. In: P. Allen and D. Van Dusen (Editors), Global Perspectives in Agroecology and Sustainable Agricultural Systems. Proc. VI hit. Scientific Conf. Organic Agric. Movements, University of California, Santa Cruz, pp. 559-564. Howard, A., 1940. An Agricultural Testament. Oxford University Press, London, 253 pp. Kajimura, T., Maeoka, Y., Widiarta, I.N., Sudo, T., Hidaka, K. and Nakasuji, F., 1993. Effects of organic farming of rice plants on population density of leafhoppers and planthoppers. I. Population density and reproductive rate. Jpn. J. Appl. Entomol. Zool., 37: 137-144. Kakes, P., 1989. An analysis of the costs and benefits of the cyanogenie system in Trifolium repens L. Theor. Appl. Genet., 77: 111-118. Klenke, J.R., Russell, W.A. and Guthrie, W.D., 1986. Recurrent selection for resistance to European corn borer in a corn synthetic and correlated effects on agronomic traits. Crop Sci., 26: 86& 868. Kowalski, R. and Visser, P.E., 1979. Nitrogen in a crop-pest interaction: Cereal aphids. In: J.A. Lee, S. McNeil1 and L.H. Rorison (Editors), Nitrogen as an Ecological Parameter. Blackwell Scientific Publications, Oxford. Luna, J., 1988. Influence of soil fertility practices on agricultural pests. In: P. Allen and D. Van Dusen (Editors), Global Perspectives in Agroecology and Sustainable Agricultural Systems. Proc. Vi Int. Scientific Conf. Organic Agric. Movements, University of California, Santa Cruz, pp. 589-600. Merrill, M.C., 1983. Eco-agriculture: A review of its history and philosophy. Biol. Agric. Hort., 1: 181-210. Oelhaf, R. C., 1978. Organic Farming: Economic and Ecological Comparisons with Conventional Methods. Allanheld, Osmun, Montclair, NJ. Phelan, P. L., Norris, K. and Mason, J. R., 1995. Soil-management history and maize susceptibility to Ostrinia nubilalis (Hlibner ) oviposition: Evidence for plant mineral balance as a physiological mechanism. Environ. Entomol., submitted. Rongjun, C., 1989. Energy and nutrient flow through detritus food chains. Agric. Ecosystems Environ., 27: 205-215. Scheffe, H., 1959. The Analysis of Variance. Wiley, New York. Snedecor, G.W. and Co&an, W.G., 1980. Statistical Methods. The Iowa State University Press, Ames, IA, 507 pp.
Agriculture,
Ecosystems
and Environment
56 ( 1995) 1-8
Soil-fertility management and host preference by European corn borer, Ostrinia nubilalis (Hiibner), on Zea mays L.: A comparison of organic and conventional chemical farming P. L. Phelan *, J. F. Mason, B. R. Stinner Depurtment
of Entomology,The Ohio Agricultural Research & Development Center, The Ohio State University, Wooster, OH 44691, USA Accepted
11 August 1995
Abstract It has long been argued by proponents of organic agriculture that crop losses to insects and diseases are reduced by this farming method, and that reduced susceptibility to pests is a reflection of differences in plant health, as mediated by soil-fertility management. These reports although widespread are mostly anecdotal and largely without experimental foundation. In this study, the effects of two parameters of soil fertility on the host-preference behavior of an insect pest were measured: ( 1) the immediate effect of organic vs. inorganic fertilizers and (2) the long-term effect of soil -management history. Soils were collected from three pairs of neighbouring farms, each pair matched for soil type and compnsing organic and conventional chemical production systems. Each soil was potted and amended with mineral fertilizers, animal manures, or left amended. After planting the amended soils with maize (Zeu muys L.) in a greenhouse, European corn borer females (ECB), Ostriniu nubilalis (Httbner), were released to determine egg-laying preferences. For each of the three farm comparisons, there was a significantly higher level of ECB oviposition on plants in conventional soil. In two comparisons, there was also a significant amendment effect; however, the specific fertilizers leading to greater egg laying were not consistent among farm comparisons. Thus, the form of the fertilizer did not have consistent effects on maize susceptibility to ECB, but soil-management history did. Moreover, there was significant variation in egg laying among fertilizer treatments within the conventionally managed soil, but for plants in the organic soils, egg laying was uniformly low. Pooling results across all three comparisons, variance in egg laying was about 18 times higher among plants in conventional soil than among plants in organic soil. It is suggested that this difference is evidence for a form of biological buffering characteristic of organically managed soils. Also significant, ECB ovipositional preference did not correlate with plant biomass. Thus, these results suggest that soil-management practices can significantly affect the susceptibility of crops to pests, and do so without adversely affecting plant productivity. Kewwrd.s:
Soil management;
Organic farming; Host selection; Ovipositional
1. Introduction One of the long-held contentions of those employing organic-farming practices is that these agricultural sys* Corresponding author: Tel. 216-263-3728, Email. [email protected].
Fax. 216-263-3686,
0167~8809/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDIOl67-8809(95)00640-O
preference;
Crop resistance
terns reduce the occurrence of insect and disease outbreaks (Howard, 1940; Oelhaf, 1978). Although this view is widespread, there have been surprisingly few attempts to test its validity. Lower pest pressure in organic systems could result from the greater use of crop rotation and/or preservation of beneficial insects in the absence of pesticides. Alternatively, another fun-
2
P.L. Phelan et al. /Agriculture,
Table I Nutrient levels prior to experiment
CEC
pH
Ecosystems and Environment 56 (199.5) l-8
in soils collected from paired organically
% Org. Mat.
%N
and conventionally
managed farms
Nutrient level (Kg ha- I )
% Base Sat.
N@N
P
K
Mg
Ca
K
Mg
Ca
Furm Comptrrison I Organic 13 Conventional 9 Farm Compwison 2
5.2 6.8
4.4 2.9
0.24 0.16
75 45
19.5 179
544 325
344 421
1728 3018
4.8 4.3
10 18
30 78
Organic 11 Conventional IO Frrrm Compurison 3 Organic 7 Conventional 9
6.1 5.8
4. I 2.9
0.22 0.16
135 10
119 193
352 887
573 488
3466 2333
3.5 9.7
19 17
67 50
6.2 6.1
2.9 2.8
0.16 0.15
15 1s
29 92
138 374
354 344
2636 2726
2.1 4.8
18 14
80 68
damental axiom ascribed by organic farming is that “healthy soil produces healthy plants,” which are more resistant to insects and disease (Geisler, 1988; Luna, 1988). Although healthy soil is difficult to define, it has been argued that fertility practices that replenish and maintain high soil organic matter and that enhance the level and diversity of soil macro- and microbiota provide an environment that by some unknown process enhances plant health (Merrill, 1983). If soil-fertility practices do impact the physiological susceptibility of crops to insects and disease, two possible causes can be identified: the immediate effect of the amount and form of fertilizer used, e.g. animal manures vs. inorganic fertilizers, and the long-term effect of soil management history. Although there is an extensive literature documenting the relations between levels of individual plant nutrients and herbivore performance (Dale, 1988), virtually nothing is known about how either the form of nutrient input or the history of soil management affect pest performance. Here results are presented of greenhouse studies on soil collected from adjacent organic and conventional farms. After amending with either mineral nitrogen or organic manures, maize plants in these soils were compared for their propensity to elicit egg laying by European corn borer (ECB) , Ostrinia nubilalis (Hiibner)
2. Materials and methods 2.1. Soil-management
history
Soils were collected from paired farms, with one utilizing organic practices and a second adjacent farm
using conventional methods of tillage, fertility, and pesticide input. The organic farms in this study managed soil fertility using a combination of animal manures and different crop rotations (described below), and each of the conventional farms used inorganic fertilizers and a maize-soybean (Glycine mm) rotation. Soils were collected from the top 15 cm, taking care to match soil type within a farm pair. Where possible, samples from the two farms were taken from adjoining fields, but at least 8 m from field boundaries. Soil collections from within each farm were combined, mixed thoroughly, and sieved with a 1.2 cm X 1.2 cm holed screen to remove larger stones. Subsamples then were taken for soil analysis of nutrients and organic matter (Table 1) . For Farm Comparison 1, soil samples were collected in late August 1992. The farms were located in Wayne County, Ohio, with the collection sites about 100 m apart. The organic farm had been under organic management for 7 years with a rotation of alfalfa/grass, maize, maize, and oats interseeded with alfalfa/grass. Straw-packed dairy-cow manure was added at 12 OOO16 000 kg ha- ’before first-year maize and 20 000-24 000 kg ha-’ before second-year maize. The soil type was Canfield silt-clay loam and both the organic and conventional fields were planted in first-year maize at the time soil was collected. The paired fields of Farm Comparison 2 were located in Knox County, Ohio and were divided by a small dirt lane; collection sites were separated by about 25 m. The organic farm, which had been under organic management for 25 years, followed a rotation of red clover/grass, maize, soybeans, and wheat or oats. Straw-packed dairy-cow manure was
P.L. Phelun et al. /Agriculture,
Ecosystems and Environment
added at about 12 000 kg ha- ’before maize. The soil type for both fields was Chili silt-clay loam, and samples were collected in late November 1992. The conventional field had been last planted in maize, and the organic field was coming out of 14 months clover following wheat. The conventional field had been chisel plowed and the organic field disk plowed the preceding autumn. Soil for Comparison 3 was collected in February 1993 from adjoining farms located in Holmes County, Ohio. The organic farm was an Amish farm that had used horsedrawn tillage with a rotation of red clover/alfalfa/grass, maize, and wheat or oats for 75 years. Straw-packed dairy-cow manure was applied at approximately 33 000 kg ha- ’ before maize. The soil type was Canfield silt-clay loam; the sampled fields had both been in first-year maize the previous year and collection sites were separated by about 100 m. 2.2. Greenhouse studies For the first farm comparison, the two soils were placed in pots (2 1.6 cm diam X 20.3 cm high) and each soil type was amended for nitrogen using: (1) NH,NO?, (2) fresh dairy-cow manure, or (3) left unamended. Treatments for Comparisons 2 and 3 were the same except composted manure was also included. Rates of application were 164 kg ha-i N for each amendment based on the surface area of the soil top. For manures, this rate was based on total N as measured by nutrient analysis of each manure sample. All pots were watered and held for 1 week, then planted with four seeds of Zea mays L. (sweetcorn cv. Northern Extra Sweet). Plants were thinned to one per pot after reaching a height of 30-40 cm. Pots were arranged in a greenhouse using a randomized complete-block design, and the positions of pots within a block were rerandomized on a weekly basis. Supplemental lighting was provided by 400 W high pressure sodium lamps, spaced two per 3. I m X 1.8 m bench at a height of 1.3 m above the benches. The lights were maintained on a 16 h daylength. Temperatures typically ranged 2133°C during the day and 18-29°C during the night. A computer-controlled Greenhouse Environmental Manager (Q-Corn Corp., Santa Ana, CA) maintained temperatures, and monitored humidity and light levels. ECB pupae were obtained from the USDA-ARS Corn Insects Research Unit (Ankeny, IA). Two to 5 day old ECB adults were released twice per week into the
56 (1995) l-8
3
greenhouse, and plants were examined every 2-3 days for ECB eggs. Eggs were counted and removed, and their position on the plant recorded. Plant height and leaf stage (number of leaves with collars showing) and ECB egg laying were monitored until physiological maturity of the maize. Pots were watered as needed with deionized water. Dry weights of roots and shoots were determined at the end of Comparisons 2 and 3, with only shoot dry weight determined for Comparison 1. Plant growth and ECB ovipositional response were analyzed within each comparison by three-way ANOVA to determine the relative effect of soil source, form of N amendment, soil amendment interaction, and blocks (Snedecor and Cochran, 1980). Means were separated using Fisher‘s protected LSD when a significant soil-amendment interaction was indicated. Soil and amendment effects on variance in plant growth and ECB response across the three comparisons were also determined. Plant-growth data were standardized by dividing by the mean value for that farm comparison; egg laying was expressed as the proportion of total eggs for a comparison and was transformed by sin-‘x”‘. Relative variability between soils and among amendments was measured by the ratio of the variances (Fstatistic). Because these data are not independent and probably not normally distributed, a Monte Carlo approximation to the Permutation test was used to determine the probability of equal variances (Scheffe, 1959). Data sets were randomly resampled with replacement 10 000 times using the Resampling Stats computer program (Resampling Stats, Arlington, VA) to estimate P.
3. Results 3.1. Farm comparison 1 Release of ECB females was initiated during the 45th leaf stage, when plants were about 66% of their final height. Significant differences in egg laying were measured during the first 2 weeks of ECB release; Fig. la reflects the ovipositional response during this period. ANOVA of egg laying indicated a significant soil effect (F= 5.68, 135 d.f., P = 0.02) and amendment effect (F= 13.89, 235 d.f., P< 0.001). In addisoil Xamendment tion, there was a significant
4
2
P.L. Phelun et al. /Agriculture.
Ecosystems and Environment
(F= 6.02, 235 d.f., P = 0.006)) with no significant interaction, were measured for final plant height (data not shown). Mean heights for plants in conventional and organic soils were 105 cm and 98 cm, respectively. Most of the difference in plant height was attributable to plants in conventional soil amended with fresh manure, which were significantly taller than those in other treatments. Notably, although these plants were about 10% taller than manure-amended plants in organic soil, their shoot biomasses were equivalent (Fig. lb).
200
ii
2 P
H 100 0 Unamended
NH4N03
Fresh
Manure
Amendment 20
/
56 (1995) 1-R
/
3.2. Farm comparison 2 Release of ECB females began in the 5-&h leaf stage, when plants were about 66% of their final height 150
a)
T
120 K h ii w” Unamended
NH4N03
Fresh
90
Manure
Amendment 60
Fig. I. Farm Comparison I: (a) mean numbers of eggs laid by European corn borer females on and (b) final mean shoot biomass of maize plants grown in a greenhouse. Plants were grown in soils collected from either organically (solid bars) or conventionally (cross-hatched bars) managed farms, and were amended with NH4N03, fresh manure, or left unamended. T-bars denote standard errors: bars marked by the same letter are not significantly different by Fisher’s protected LSD when a significant soil-amendment interaction was indicated by ANOVA (n = 8)
interaction (F = 11.44, 235 d.f., P < 0.001) . Eggs laid per plant averaged 108 and 63 for conventional and organic soils, respectively. Between-soil differences in egg laying were caused almost solely by the greater number of eggs laid on plants in conventional soil amended with fresh manure, which were three to eight times higher than on any other treatment (Fig. la). ANOVA of shoot dry weight at harvest showed a nearly significant soil effect (F= 3.43, 135 d.f., P = 0.07), a significant amendment effect (F = 6.79, 235 d.f., P=O.O03), and no significant interaction (F=0.82, 235 d.f., P=O.45; Fig. lb). Mean dry weight for plants in organic and conventional soils were 12.8 g and 15.2 g, respectively. Significant effects of soil (F= 9.45, 135 d.f., P=O.O04) and amendment
30 Unamended
NH4N03
Fresh
Manure
Comp.
Manure
Manure
Camp.
Manure
Amendment
““amended
NH4N03
Fresh Amendment
Fig. 2. Farm Comparison 2: (a) mean numbers of eggs laid by European corn borer females on and (b) final mean shoot biomass of maize plants grown in a greenhouse. Plants were grown in soils collected from either organically (solid bars) or conventionally (cross-hatched bars) managed farms, and were amended with N&N03, fresh or composted manure, or left unamended. T-bars denote standard errors; bars marked by the same letter are not significantly different by Fisher’s protected LSD when a significant soil-amendment interaction was indicated by ANOVA (n = 6).
P.L. Phelun et (11./Agriculture. Ecosystems and Environment 56 (1995) I-8
(77.2-99.0 cm). As with Comparison I, the greatest differences in ECB egg laying was observed for the first 2 weeks of ECB release (Fig. 2a). ANOVA measured a significant soil effect (F=6.99, 128 d.f., P=O.Ol), with plants in conventional soil averaging 105 eggs per plant vs. 70 eggs per plant for those in organic soil. There were no significant amendment (F=0.61,328d.f.,P=0.58) orinteraction(F=0.66, 328 d.f., P = 0.58) effects, although between-soil differences in egg laying were greatest for the unamended and NH,NO,-amended plants. Treatment differences were measured in shoot biomass because of a significant amendment effect (F = 4.49,328 d.f., P = 0.01)) but not a significant soil effect (F=2.14, 128 d.f., P=O.15). There was alsoa significant soil-amendment interaction (F= 6.52, 328 d.f., P = 0.002) because of the differential response to amendments in the two soils. Plants amended with composted manure in the organic soil produced the greatest shoot mass, with fresh-manure-amended and NH,NO,-amended plants in organic soil intermediate between compost-amended and unamended plants (Fig. 2b). In the conventional soil, amendments did not significantly increase shoot biomass relative to the unamended soil. Root biomass (not shown) followed the same pattern as shoot mass, with no significant soil effect (F= 0.0, 128 d.f., P= 0.98), but a significant amendment effect (F= 2.98, 328 d.f., P= 0.05) and interaction (F= 5.91, 328 d.f., P = 0.003). Despite these differences in plant biomass, there was no significant soil, amendment, or interaction effects on final plant height (F < 1.O for each) ; plant heights were 135 cm and 138 cm for organic and conventional soils, respectively. 3.3. Farm comparison
3
350
300
$ a
250
ii w” i
200
150
100 Unamended
NH4NOB
Fresh
Manure
Comp. Manure
Manure
Comp. Manure
Amendment 40
-
30 3 5’ f 0
20
i; 2 m 10
0 Unamended
NH4N03
Fresh Ame”dme”t
8o/ cl
Unamended
T
NH4N03
Manure
i
Compost
Amendment
Release of ECB females was initiated at the 4th-5th leaf stage, when plants were about 56% of their final height (55.7-77.3 cm). Differences in ECB egg laying were observed for about the first 4 weeks (Fig. 3a). ANOVA measured a significant soil effect (F=6.13, 135 d.f., P= 0.02), with plants in conventional soil averaging 201 eggs per plant vs. 159 eggs per plant for those in organic soil. There was also a significant amendment effect (F = 7.82,335 d.f., P = 0.001)) with NH,NO,-amended plants receiving the greatest number of eggs, and a significant interaction effect
Fig. 3. Farm Comparison 3: (a) mean numbers of eggs laid by European corn borer females on and (b) final mean shoot biomass of maize plants grown in a greenhouse, and (c) percentage of earlystage plants developing symptoms of an unidentified disease. Plants were grown in soils collected from either organically (solid bars) or conventionally (cross-hatched bars) managed farms, and were amended with NH,NO,, fresh or composted manure, or left unamended. T-bars denote standard errors; bars marked by the same letter are not significantly different by Fisher‘s protected LSD when a significant soil-amendment interaction was indicated by ANOVA (n = 5). Percentages of disease incidence were transformed by sin‘xl” before analysis.
6
P.L. Phelan et al. /Agriculture, Ecosystems and Environment 56 (1995) 14
(F=3.95, 335 d.f., P=O.O2) because egg laying on the NH,N03-amended and compost-amended plants was elevated only in conventional soil, not in organic soil. Significant differences in shoot weights in this comparison were attributable solely to amendment effects (F = 17.11, 335 d.f., P < 0.001 ), without a significant soil effect (F = 0.38, 135 d.f., P = 0.54) or soil-amendment interaction (F = 0.03, 335 d.f., P = 0.99). Plants fertilized with NH4NOS produced the greatest shoot mass in both soils (Fig. 3b). Composted and fresh manure produced shoot mass intermediate to unamended and NH,N03-amended plants. Root mass was also significantly affected only by amendment (F= 12.78, 315 d.f., P
3.4. Treatment effects on variability in plant growth and ECB response In addition to effects on mean values of plant growth and insect response, soil-management history and fertilizers were analyzed across farm comparisons for effects on the variability in these parameters. Variance in oviposition was 17.8 times higher for plants in conventionally managed soil than for those in organic soil (P = 0.0024 measured by the Permutation test). In contrast, no significant differences in the variability of egg laying were measured among fertilizers. Likewise, variances in plant growth were very similar between soils and among fertilizers.
4. Discussion Despite the potential practical and biological significance of understanding how soil-fertility management affects crop susceptibility to pests, rather few attempts have been made to examine this relationship. Results of paired on-farm studies, although few in number, generally support the anecdotal reports of lower pest pressure in organic-production systems (Kowalski and Visser, 1979; Andow and Hidaka, 1989; Kajimura et al., 1993). In all three studies, evidence suggested that differences in plant physiology may have mediated pest levels. In contrast, natural enemies did not appear to explain lower pest levels on organic farms in these studies, as predator and parasite populations were either comparable between farm pairs or were higher in conventionally managed fields. Effects of the form of fertilizer on pests have been less clear. For example, Culliney and Pimentel ( 1986) measured higher Phyllotreta flea beetles populations on sludge-amended collard (Brassica oleracea) plots early in the season compared to mineral-fertilizeramended and unfertilized plots, but later in the season, in these same plots, population levels were lowest for beetles, as well as for aphids and lepidopteran pests. Plant growth followed the inverse pattern, with the sludge treatment producing the largest plants and the unfertilized soil producing the smallest. Crop susceptibility to pests is determined by both adult behavioral response (host finding and oviposition) and larval developmental response (efficiency of food conversion, developmental rate, and survival-
P.L. Phelan et al. /Agriculture, Ecosystems and Environment 56 (1995) l-8
ship). This study focused on the former as a first step towards understanding how soil management can affect ECB outbreaks. The present results extend the previous demonstrations of the effects of soil-managementpractices on crop pests and advance our understanding of this relationship by experimentally partitioning the contributions of fertilizer form and soil-management history. Because soils were compared from three pairs of farms, it can be concluded that soil-management effects were not the result of the unique conditions of any one location. On the contrary, management-history effects appear important, because in each of the three farm comparisons, plants in conventional soil received more ECB eggs overall. Second, by testing ECB response in the greenhouse, crop rotations and natural enemies can be excluded as direct causes for the differences found (this is not to diminish their possible significance in the farm setting, and crop-rotation history may have affected pests indirectly through changes in the soil). Rather, the results strongly suggest that soil-fertility management can significantly alter plant acceptability to ECB. Third, although a significant amendment effect was measured in two of three comparisons, the specific amendments leading to greater egg laying differed. In Farm Comparison 1, egg laying was higher on fresh-manure-amended plants in conventional soil than on all other treatments (Fig. la), but in Comparison 3 (Fig. 3a), egg laying was elevated for NH,NO,-amended and compost-amended plants in conventional soil. Thus, effects of the form of fertility (manures vs. inorganic) appeared dependent on the context of the soil onto which they were applied. This finding suggests an explanation for the incongruity among previous studies of the effects of fertilizer form on pests. To understand the link between fertility management and crop susceptibility to insects, it is particularly important to note that in the present study, although main effects were measured for soil history in each of the three comparisons, ECB egg laying generally was elevated in conventional-soil treatments only for one or two fertilizer treatments. This was particularly true 1 and 3, as reflected by significant for Comparisons interactions between soil and amendment in thesecomparisons. Thus, planting in the conventional soils did not necessarily lead to higher egg laying, but did increase its probability, depending on the fertilizer added. In contrast, ECB susceptibility remained uni-
7
formly low among plants in organic soils, irrespective of fertilizer amendments. This between-soil difference resulted in a significantly higher variance in egg laying on plants in conventional soils across the three comparisons. Studies indicate that organic management practices can enhance soil quality and reduce environmental stress on plants by improving soil structure and by increasing its capacity to buffer pH and levels of moisture and mineral nutrients (Rongjun, 1989; Arshad and Coen, 1992). In an analogous manner, the present results may represent the first evidence that long-term management of soil organic matter can also lead to buffering of a higher order, that of a plant‘s ability to resist insect pests. From a practical perspective, it is also notable that ECB ovipositional preference was not related to plant productivity (biomass). There was no consistent pattern in plant biomass with regard to either management history or the form of fertilizer among the three comparisons. Even within a soil type, there was no correlation between plant productivity and ECB ovipositional preference, indicating that ECB females did not simply prefer the largest plants. This lack of correlation between plant productivity and non-genetic resistance contrasts with the trade-off between plant growth and genetically based herbivore resistance commonly observed in natural plant populations (e.g., Cates, 1975; Berenbaum et al., 1986; Kakes, 1989). Crop-breeding programs have also frequently found an inverse relationship between insect resistance and yield (e.g. Klenke et al., 1986). Thus, the present studies suggest that non-genetic resistance to pests through plant fertility need not come at the expense of crop yield. In summary, the significance of the present study is in demonstrating that the ovipositional preference of a foliar pest can be mediated by soil differences in fertility-management history. Thus, the lower pest levels widely reported in organic-farming systems may, in part, arise from biochemical or mineral-nutrient differences in crops under such management practices, as investigated elsewhere (Phelan et al., 1995). The lower level ofECB oviposition on maize grown in organically managed soil, in addition to the higher variability of ECB response to maize in conventional soil, suggest that the buffering of soil processes previously attributed to high soil organic matter and microbial activity may
8
P.L. Phelan et al. /Agriculture, Ecosystems and Environment 56 (1995) I-8
also extend to the interactions ground herbivores.
of plants and above-
Acknowledgements The authors are indebted to L. Lewis and J. Dyer of the USDA-ARS Corn Insects Research Laboratory for rearing the insects used in this study. They also thank cooperating farmers for providing soils: J. Hartzler, A. Hostetler, D. Kline, B. Kohl, R. and G. Spray, and M. Yoder. Statistician B. Bishop aided in the analysis of the results, and R. Hammond, R. Lindquist, D. McCartney, and E. Zaborski provided critical reviews of the manuscript. Salaries and research support were provided by state and federal funds, Ohio Agricultural Research and Development Center Journal No. 18093.
References Andow, D.A. and Hid&, K., 1989. Experimental natural history of sustainable agriculture: Syndromes of production. Agric. Ecosystems Environ., 27: 447-462. Arshad, M. A. and Coen, G. M., 1992. Characterization of soil qua_ity: Physical and chemical criteria. Am. J. Altemat. Agric., 7: 25-31. Berenbaum, M.R.. Zangerl, A.R. and Nitao, J.K., 1986. Constraints on chemical coevolution: Wild parsnips and the parsnip webworm. Evolution, 40: 1215-1228. Cates, R.G., 1975. The interface between slugs and wild ginger: Some evolutionary aspects. Ecology, 56: 391&400. Culliney, T.W. and Pimentel, D., 1986. Ecological effects of organic agricultural practices on insect populations. Agric. Ecosystems Environ., 15: 253-266. Dale, D., 1988. Plant-mediated effects of soil mineral stresses on insects. In: E.A. Heinrichs (Editor), Plant Stress-lnsect Interactions Wiley, New York, pp. 35-l 10.
Geisler, F.R., 1988. Effects of organic manures on a host crop-pest relationship. In: P. Allen and D. Van Dusen (Editors), Global Perspectives in Agroecology and Sustainable Agricultural Systems. Proc. VI hit. Scientific Conf. Organic Agric. Movements, University of California, Santa Cruz, pp. 559-564. Howard, A., 1940. An Agricultural Testament. Oxford University Press, London, 253 pp. Kajimura, T., Maeoka, Y., Widiarta, I.N., Sudo, T., Hidaka, K. and Nakasuji, F., 1993. Effects of organic farming of rice plants on population density of leafhoppers and planthoppers. I. Population density and reproductive rate. Jpn. J. Appl. Entomol. Zool., 37: 137-144. Kakes, P., 1989. An analysis of the costs and benefits of the cyanogenie system in Trifolium repens L. Theor. Appl. Genet., 77: 111-118. Klenke, J.R., Russell, W.A. and Guthrie, W.D., 1986. Recurrent selection for resistance to European corn borer in a corn synthetic and correlated effects on agronomic traits. Crop Sci., 26: 86& 868. Kowalski, R. and Visser, P.E., 1979. Nitrogen in a crop-pest interaction: Cereal aphids. In: J.A. Lee, S. McNeil1 and L.H. Rorison (Editors), Nitrogen as an Ecological Parameter. Blackwell Scientific Publications, Oxford. Luna, J., 1988. Influence of soil fertility practices on agricultural pests. In: P. Allen and D. Van Dusen (Editors), Global Perspectives in Agroecology and Sustainable Agricultural Systems. Proc. Vi Int. Scientific Conf. Organic Agric. Movements, University of California, Santa Cruz, pp. 589-600. Merrill, M.C., 1983. Eco-agriculture: A review of its history and philosophy. Biol. Agric. Hort., 1: 181-210. Oelhaf, R. C., 1978. Organic Farming: Economic and Ecological Comparisons with Conventional Methods. Allanheld, Osmun, Montclair, NJ. Phelan, P. L., Norris, K. and Mason, J. R., 1995. Soil-management history and maize susceptibility to Ostrinia nubilalis (Hlibner ) oviposition: Evidence for plant mineral balance as a physiological mechanism. Environ. Entomol., submitted. Rongjun, C., 1989. Energy and nutrient flow through detritus food chains. Agric. Ecosystems Environ., 27: 205-215. Scheffe, H., 1959. The Analysis of Variance. Wiley, New York. Snedecor, G.W. and Co&an, W.G., 1980. Statistical Methods. The Iowa State University Press, Ames, IA, 507 pp.