Bean fly, management practices, and biological control in Malawian subsistence agriculture

Agriculture Ecosystems & Environment ELSEVIER

Agriculture, Ecosystemsand Environment 50 (1994) 103- I I I

Bean fly, management practices, and biological control in Malawian subsistence agriculture Deborah K. Letourneau Board of Environmental Studies College Eight, UniversiO, of Cal(fornia, Santa Cruz. C,1 95064, USA

Accepted 8 March 1994

Abstract

Subsistence farmers with little access to costly farm inputs such as pesticides and fertilizers must rely on natural pest regulation and cultural controls. To assess the effects of different management practices on a key pest, bean fly densities were compared among 19 farmers' fields in central Malawi. The close proximity of these fields, synchrony of planting dates, and similar field sizes allowed a rigorous, empirical comparison of the relative susceptibility of different bean varieties, the effects of soil fertility, and effects of surrounding vegetation. The two most commonly used varieties differed significantly in bean fly infestation levels. Total soil nitrogen was positively correlated with the most common species of bean fly (Ophiomyia spencerella); and soil phosphorus levels were negatively correlated with population densities of both bean fly species. Similar rates of biological control of bean flies by parasitic wasps occurred in all fields. Complementary experiments with potted plants showed a direct relationship between synthetic NPK fertilizer level and O. spencerella density. However, the effect was reversed in treatments with soluble fish protein fertilizer. In addition, straw mulching of newly sown fields, a practice not used by farmers in the study, may reduce bean fly damage.

1. Introduction

Subsistence farmers in tropical agroecosystems are challenged with a rich array of insect pests and warm climatic conditions which support many pest generations per year. However, severe economic constraints reduce the options available for crop protection and place strategic importance on cultural practices, such as the selection of varieties and planting dates, as key elements affecting pest levels (e.g. Seshu-Reddy, 1990; Zethner, 1991 ). Advances in agricultural ecology suggest that many crop management decisions can affect pest levels directly or indirectly through the action of natural enemies. For example, colonization patterns of pests and their

natural enemies often respond to intercropping (Altieri and Letourneau, 1982; Russell, 1989; Sheehan and Shelton, 1989; Andow, 1991), weeding practices (Altieri et al., 1977; Pavuk and Barrett, 1993) and living mulches (Brust et al., 1986; Bugg et al., 1990). Pest levels can be regulated in some systems though the use of artificial mulches (Cardona et al., 1981; Necibi et al., 1992), and specific effects of tillage practices on different ground dwelling pests and predators are becoming predictable (House and All, 1981; House and Stinner, 1983; All and Musick, 1986; Tonhasca and Stinner, 1991; Turnock et al., 1993). Increased tissue nitrogen levels in fertilized crops can result in a change in pest densities and plant tolerance (Scriber, 1984; Shaw et al.,

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D. K Letourneau /Agriculture, Ecos),stems and Environment 50 (1994) 103-111

1986; Ajayi, 1990; Funderbunk et al., 1991 ; Hunt et al., 1992), and can also affect natural enemies (Fox et al., 1990). These complex interactions remain poorly understood yet may be critical to maintaining high yields and reducing risk under subsistence farming conditions. To assess the effects of different cultural practices on pest levels in a tropical subsistence crop, the author collected on-farm samples in Central Malawi of bean flies (Diptera: Agromyzidae), which are major pests of beans in the Old World tropics (Hill, 1983). Experimental field trials have shown that certain bean varieties are resistant to bean fly (e.g. Talekar et al., 1988; Karel and Maerere, 1985; Chiang and Talekar, 1980), that tall rice stubble residues can disrupt bean fly oviposition (Litsinger and Ruhendi, 1984), and that soil amendments can decrease plant suitability for bean flies (Floor et al., 1984). This paper ( 1 ) compares bean fly incidence and parasitism levels with respect to management practices on Malawian subsistence farms, (2) reports results of a complementary field experiment designed to test effects of soil nitrogen found in onfarm comparisons, and (3) assesses the effects of straw mulch on early attack of bean plants by bean flies.

2. Methods

2. I. Study site and pest biology Nineteen fields, located within an area of 2 km 2 around two villages in the Kalira District near Ntchisi, Central Malawi, were sampled in 1990. These subsistence farms are located at approximately 1240 m elevation and receive an average of 1085 mm precipitation annually, with most of the rain occurring during October-April. The sandy loam or loamy sand soils are moderately acidic and fields are located on hillsides which vary in slope and aspect. Three species of bean fly, Ophiomyia phaseoli (Tryon), O. spencerella (Greathead) and O. centrosematis (DeMeijere) occur in Malawi, with the former two species causing significant yield losses, especially in late-planted bean (L.

Kantiki, personal communication, 1990). Eggs, deposited in the leaf tissue or stem, produce larvae which descend the stem, damage the vascular tissue, and pupate at the stem-root junction just below the soil surface (Greathead, 1968). Heavily infested plants yellow and die before the flowering stage, and eggs deposited when the plants have just emerged give rise to disproportionately severe damage. The major natural enemy of bean flies in Malawi is the parasitoid wasp Opius phaseoli ( Hymenoptera: Braconidae).

2.2. Farmer interviews All farmers within the area who had sown a bean crop with the first rains on 25 November 1990 were interviewed in Chichewa with the aid of the Kalira District field officer who translated questions and responses. The farmers were asked to describe their production practices including the use of soil amendments, crop rotations, varietal selections, planting times, and mixed-cropping patterns. A list of bean pests was requested from each farmer, with a description of the pest and the type of damage it caused.

2.3. On-farm sampling Fields were selected in close proximity with uniform planting dates to allow better resolution of the effects of other variables on bean fly infestation levels. Bean fly, weed, and soil samples were collected 24-26 days after the emergence of the bean crop to coincide with the pupation stage of the initial bean fly attack. One hundred bean plants were uprooted on each farm using a stratified randomization method and excluding edge rows from the sample. A cardinal direction was pre-designated for selecting the sample plant among bean plants in the same hill. Based on the pattern of varietal plantings provided by the farmer, the 100 plants were taken as proportional subsamples from each bean cultivar. The stem was uprooted, cut below the lowest leaf and placed in clear plastic tubes (15 c m × 2 . 4 cm) covered on both ends with nylon mesh (modified from Greathead, 1968 ). Infestation rates and parasitism levels were determined by counting

D.K. Letourneau / Agriculture, Ecosystems and Environment 50 (1994) 103- I / 1

emergents from these stems and from pupariae dissected from the stems after 12 days. Because the adult flies can be identified positively only by dissecting out the genitalia, the numbers of O. phaseoli, O. spencerella and O. centrosematis were determined on the basis of pupal coloration which differs among the three species (Greathead, 1968). To characterize possible effects of soil quality on bean fly incidence and effects of surrounding vegetation, these parameters were surveyed on each farm. Twelve soil samples (15 cm cores), taken as three subsamples at random points in each quarter of the field, were combined, mixed, air dried, and subjected to a full soil analysis at Chitedze Research Institute in Lilongwe (exchangeable cations (meq kg-~ soil) Ca, Mg, K, Na, H, AI; TEB (meq kg-t soil), available P (/~g g-t soil (p.p.m.)), OM (%), Kjeldahl N (%), percentage sand, silt, and clay, texture, and pH ). The area of each field was measured, and bean density was described by the space between planting ridges and the number of bean and maize plants per station. Farmers had kept the fields hoed, leaving very few weeds to flower and provide sources of nectar and pollen. The surrounding vegetation bordering each side of the field was characterized as woodland, grassland, shrubland, or specific crops.

105

trients) added in solution to the pots at 0.25, 0.5, and 1.0 times their recommended levels. Two bean seeds (Nasaka variety) were sown in each 12 cm pot after burying the pot in the ridge flush with the soil level. Pots were fertilized three times: one, four and eight days after plant emergence, to create differences in plant quality during the major period of bean fly oviposition. Each of the three fertilizers applied at three rates and a control (zero fertilizer added) were replicated ten times to obtain a sufficient number of stems for a sample. At 25 days after emergence, all plants were harvested from the pots and held in cages as described above. Although none of the farmers in the Ntchisi area used mulch, studies in the Philippines with shallow mulches and tall rice stubble (Litsinger and Ruhendi, 1984) suggested that a deep mulch might deter bean flies. Three seeds of Nasaka variety beans were sown in each station (30 cm apart) in four pairs of mulched and non-mulched plots after approximately 25 cm straw mulch was applied. The stems of 50 plants, randomly selected from the inner four rows within each plot 25 days after sowing, were placed in plastic tubes for emergence of flies or parasitoids.

2.5. Data analyses

2.4. Experiments To complement empirical data from on-farm studies, the effects of fertilizers and mulch on bean fly incidence were tested in experiments with potted bean plants at the University of Malawi, Bunda College of Agriculture. Campus research fields are located 20 km southwest of Lilongwe, at an elevation of 1116 m with 934 mm annual rainfall. The effects of three fertilizers on bean fly densities were tested using three fertilizers (1) 20:20:20, (2) 23:19:17 plus 0.02% boron, 0.05% copper, 0.1% iron, 0.05% manganese, and 0.05% zinc as micronutrients, and (3) soluble, hydrolyzed fish protein ( 12: 0.6: 1.3 plus 1% Na, 0.01% Mg, 5 p.p.m. Mn, 40 p.p.m. Fe, 4 p.p.m. Cu, 15 p.p.m. Zn, and 1 p.p.m. Se as micronu-

Bean fly density (mean number of bean flies per stem), percent parasitism, and species composition of bean flies and parasitoids were compared across farms with simple statistics, between the major varieties and between mulched and non-mulched treatments with ANOVA, and among fertilizer treatments with regression analyses. Soil and vegetation parameters (total N, P, K, pH, OM, silt, clay, org C, Na, Mg, Ca, TEB, weed species richness, bean density, and surrounding vegetation) were subjected to multivariate analyses to determine combinations of practices or conditions that may affect bean fly infestation levels. All analyses were conducted using Statistical Analysis Systems Ltd. Inc. (1988) on a Toshiba 3100SX.

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D.K. Let ourneau / Agriculture, Ecosystems and Environment 50 (I 994) 103- I 11

3. Results

Several practices were common to every farmer in the study: ( 1 ) all fields were prepared for sowing by hand-hoeing the soil into ridges and furrows, (2) all beans were intercropped with maize, with both climbing and bush cultivars sown on ridges in the same hole with the maize, (3) all fields were small (ranging from 0.21 to 1.20 ha, a typical size in Malawi despite an estimate of 1.25 ha as the minimum area needed for subsistence (Sofranko and Fliegel, 1989), (4) none of the farmers used insecticides on wet-season beans, and (5) all fields had been weeded carefully so that flowering weeds were found only rarely. With respect to insect pests, each of the farmers described 'kanunde' leaf beetles (Coleoptera: Chrysomelidae: Ootheca spp.), and most mentioned cutworms. None of the farmers recognized the minute bean fly itself as a pest, but were probably describing the symptoms of bean fly infestation when they referred to a 'blight' which causes bean plants to wither and die. Farmers reported a wide range of crop histories, fertilization practices and varietal selections. Fourteen of 19 fields had been sown to beans and maize in the previous wet season, burned, and left fallow during the dry period May-November 1990. Tobacco, a major cash crop sown on four farms in the previous wet season, was heavily fertilized with 20:20:0 plus CAN (calcium ammonium nitrate) or urea; farmers assumed this fertilization would leave a residue for the following maize crop. Two of the fields had been fertilized with synthetic soil amendments (20: 20: 0) before sowing. Manure was applied to these two fields plus three others. Total N and available P in the soils tended to be higher, on average, if the field had been fertilized or if the previous crop had been tobacco (Table 1 ) but small sample sizes prevented a statistical interpretation of these trends. All but two of the 19 farmers surveyed grew more than one bean cultivar for reasons involving yield, marketability, and flavor. Sowing each bean cultivar in a separate part of the field, 40% of the farmers grew two varieties, and 50% grew

three or more bean cultivars. Risk aversion was the most common reason for using varietal mixtures, with 50% of the farmers mentioning differential susceptibility of bean cultivars to drought, blight, and flooding. The other farmers sowing more than one bean cultivar did so because of seed availability (25%) or because different cultivars were grown for market than for home consumption (25%). Three species of bean fly were reared from young bean plants sampled from farmers' fields: 0. spencerella and O. phaseoli were the common species, and O. centrosematis was found occasionally. First generation bean fly densities varied among fields, with a range of 0. 1-7.6 flies per ten plants. Pupal densities within individual stems ranged from zero to three. Different bean cultivars, even on the same farm, tended to be consistent with respect to relative levels of susceptibility to bean fly. Of the two most common cultivars, 'Nanyati' showed significantly greater incidence of bean fly puparia than did 'Salima' (Table 2). The other bean cultivars did not occur on enough farms to satisfy the assumptions of ANOVA, but the extremely low levels of bean flies in the 'Kholombe' cultivar may warrant further study (Table 2). The farmers identified Nanyati as a desirable cultivar for consumption and for market and Salima as one that is resistant to the 'blight' that causes the plants to wither and die. Although the farmers could not ascertain the cause of the blight, the symptoms described were consistent with bean fly damage. The proportion of surrounding fields containing beans was negatively correlated with the puparial density (r 2= 0.38, P = 0.038 ). Parasitism rates of different Ophiomyia species were not determined directly in this study by dissecting out each of the pupae from the 1900 stems collected on farms. However, mass rearings from stems (yielding parasitoids and flies) and counts of remaining pupal cases (color indicating the species), showed a positive correlation between percent parasitism and the proportion of pupae that were from O. phaseolus (r2=0.36, P = 0.036). This suggests that O. phaseolus was attacked by the parasitoid Opius phaseoli more frequently than was the other bean fly O. spen-

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D.K. Letourneau / Agriculture, Ecosystems and Environment 50 (I 994) 103-111 Table 1 Comparison of soil quality among farms (values are X _+SE) grouped by fertilizer application and crop history Current amendments

Previous crop

n

Kjeldahl N (%)

P (p.p.m.)

K (meg kg -~ )

Organic matter (%)

pH

Fertilizer applied None applied

Maize or tobacco Maize Tobacco

5 9 4

0.12 + 0.01 0.10-+0.01 0.12+0.03

23.8 _+3.2 18.1-+3.6 21.8+6.7

0.6 + 0.6 0.7+1.0 0.7-+0.6

2.5 _+0.08 2.9-+0.33 3.2-+0.41

5.6 + 0.04 5.7-+0.11 5.6-+0.09

Table 2 Comparison of bean fly levels and parasitism rates among common varieties on farms in Ntchisi. Values (means_+ SE per ten plants) with different letters are significantly different (ANOVA, P < 0.05 ) Bean variety

No. fields

No. O. phaseoli pupae

No. O. spencerella pupae

No. adult bean flies

Percent parasitism

Nanyati Zoyera Chizama Salima Kholombe

9 5 5 I1 2

1.0 + 0.2a 1.2_+0.4 0.7_+0.2 0.7 _+0.2a 0.3 +_0.3

4.0 + 1.0a 3.7_+ 1.4 2.1 +0.4 1.6 _+0.5b 1.0_+ 0.4

3.8 _+0.9a 3.8_+ 1.6 2.3_+0.6 1.4 _+0.4b 0.7 + 0.5

14.4 + 4.3a 19.6_+8.7 21.6_+6.3 21.2 _+7.6a 33.0_+ 33.0

cerella, a trend also found by Tengecho et al. (1988) in Kenya. According to a step-wise regression using all soil parameters, densities of the two bean fly species correlated with different soil factors (Table 3 ). Although both O. phaseoli and O. spencerella pupal densities were negatively correlated with soil P, only O. spencerella responded strongly to soil N levels. For O. spencerella, a combination of soil N, organic matter, P and pH explained 67% of the variance in puparial density among farms. Lin et al. (1977) found that low pH was associated with low bean fly levels (O. phaseoli) in soybean, and predicted that acidic soils (pH Table 3 Stepwise regression using all soil quality parameters and bean fly infestation levels among 19 farms at Ntchisi, Malawi to detect associations between soil management practices and pest damage Bean

Fly predictor(s)

PartialR 2

F

p

O. phaseoli O. spencereUa

Phosphorus Nitrogen Organic matter Phosphorus pH

0.34 0.31 0.11 0.15 0.10

8.7 7.6 2.9 5.3 4.3

0.009 0.013 0.106 0.036 0.058

<6.0) such as those in this study (Table l) would not be conducive to bean fly populations. Trials with potted plants at Bunda College partially supported findings on the relationship between soil N and bean fly levels. As predicted from samples of farmers' fields, the concentration of synthetic nitrogen fertilizer (and presumably soil N) was significantly correlated with an increase in O. spencerella density but not with O. phaseoli density (Table 4). However, the opposite trend was observed when soluble fish powder was applied to pots at concentrations approaching the recommended level. In contrast to the apparent increase in susceptibility exhibited by beans with the addition of synthetic N fertilizer, N as soluble fish powder appears to reduce attack by O. spencerella. Because the mulch held residual moisture, beans in mulched plots emerged 2-3 days earlier than did non-mulched beans. Although the number of unparasitized bean flies emerging from mulched and non-mulched beans was not significantly different (Table 5), pupal density was significantly greater in non-mulched bean. Thus, actual crop damage suffered by non-mulched bean was greater than in the mulched treatment because a greater total number of bean flies fed

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D.K. Letourneau / Agriculture, Ecosystems and Environment 50 (1994) 103- I 11

Table 4 Regression analyses (SAS-GLM) on NPK fertilizers at 0, 0.25, 0.5 and I times the recommended application rate with bean fly infestation of potted beans, variety "Nasaka' Fertilizer

Bean fly

Adjusted R 2

F

p

20: 20:20 23:19:17 11.5:0.5:1.3

O. spencerella O. spencerella O. spencerella

0.98 0.85 0.84

182.7 18.4 17.1

0.005 0.050 0.054

Table 5 Mean abundance ( _+SE) of adult bean flies, pupae (yielding bean flies or parasitoids), and parasitism levels of bean flies in a randomized complete block design with mulched and non-mulched beans, variety 'Nasaka' in monoculture. Means followed by different letters are significantly different (ANOVA, P < 0.08 ) Treatment

N

Bean flies per ten plants

Bean fly pupae per ten plants

% Parasitism by Opius

Mulch No Mulch

4 4

139_+ 1.8a 18.0 + 4.5a

26.2 + 2.9a 45.0 + 9.6b

46.4 + 5.7a 60.6 _+2. I b

and developed on non-mulched plants than on mulched plants (Table 5). Significantly greater levels of bean fly parasitism in non-mulched plots compensated for these densities in terms of the next generation of bean flies, but not for the young bean plants.

4. Discussion

This study suggests that Malawian farmers are aware of the symptoms caused by bean fly attack and probably incorporate bean fly resistant cultivars into their cropping schemes despite the fact that the tiny flies themselves commonly are not known. Similar perceptions have been found in interviews with Filipino farmers who were familiar with external feeders but did not recognize the leaf and stem-mining bean fly as a pest (Litsinger et al., 1980). Kenyan farmers were knowledgeable about the symptoms of the shootfly as a pest of maize but could not identify the fly as the causal agent of those symptoms (Conelly, 1987). The subtle nature of bean fly damage in Malawi is compounded by the occurrence of several species which, according to this study, respond differently to cultural practices. The predominance of only two species O. spencerella and O. phaseoli in farmers' fields was

expected for two reasons: (1) common bean (Phaseolus vulgaris) is not a suitable host for O. centrosernatis (Talekar and Lee, 1988 ) and (2) even in soybean, a preferred host, only a few individuals of O. centrosematis reach the puparial stage when other species of Ophiomyia are present, suggesting that it is a poor competitor with the other stem-boring maggots. In this study, O. phaseoli was less susceptible to differences in plant quality driven by soil conditions but more susceptible to the common parasitoid O. phaseoli than was its conspecific O. spencerella. The only fertilizer experiment the author has found showed that graduated applications of phosphorus caused a decrease in bean fly damage (Floor et al., 1984). These results are consistent with the correlative findings in farmers' fields in Malawi. Synthetic N fertilizer rates were positively correlated with the density of O. spencerella in experiments with potted plants (and field experiments to be published separately), but this was not the case for soluble fish powder. Several explanations are possible including (1) nutrient imbalance of N, P and K, (2) poor uptake of N in the soluble protein formulation, and (3) an actual qualitative difference which affords the benefit but not the detriment of N fertilization of beans. Although no formal studies have been conducted, farmers in California have noted pest

D.K. Letourneau / Agriculture, Ecosystems and Environment 50 (1994) 103-111

deterrence in some crops when fertilized with this p r o d u c t (J. Ball, p e r s o n a l communication, 1993 ) as compared with adjacent fields with synthetic NPK fertilizers. N derived from fish carcasses was chosen as a possible new byproduct that could come from Lake Malawi's large fishing industry. In contrast to the neutral effects of shallow mulch on bean fly in the Philippines for O. phaseoli on cowpea (Litsinger and Ruhendi, 1984), deep straw mulch did tend to reduce bean fly damage to beans. This early protection is important for survival of the young bean crop which can suffer greatly from vascular tissue damage, and a reduction from approx. 4.5 pupae per plant to 2.6 pupae per plant is similar to the control achieved by applying Lindane in Tanzania (Karel and Matee, 1986). In their study, insecticide reduction of bean fly from 3.8 to 2 pupae per plant resulted in a 33% increase in yield. It may be advisable to remove mulch after a few weeks, however, if it promotes termite invasion or enhances diseases. Neither surrounding vegetation nor varietal resistance affected parasitism rates of bean fly in this study, although the negative correlation between the number of surrounding bean fields and bean fly density in the stems indicates that first generation colonists could be limiting. It is now well known (Duffey and Bloem, 1986; Barbosa, 1988 ) that some cultivars with substantial levels of resistance against key herbivores also disrupt the critical control of the pest by its parasitoids. An effective program of pest control is most stable when a number of different stresses are imposed on the pest population. Therefore, compatibility checks among control practices are critical, and parasitism rates are important parameters to measure when evaluating resistant varieties in the field.

5. Conclusion For subsistence farmers who must balance an equation involving crop selection, spacing patterns, timing of harvest, supply of labor and fertilizer, etc. knowledge of the effect of these deci-

109

sions on crop damage by pests is critical. This study of bean fly in Malawi suggests that farmers are already taking advantage of diversity among land races and cultivars to reduce risks in bean production. It also indicates that fertilization practices may affect plant susceptibility to bean fly, and provides preliminary evidence that two locally available inputs, fish powder and mulch, can mitigate pest problems in intercropped bean.

Acknowledgment This research was conducted while the author was at the University of Malawi, Bunda College of Agriculture as a Fulbright Scholar with the Bean-Cowpea CRSP program. Additional funding was provided by the Rockefeller Foundation, US-AID, and the University of California Santa Cruz, Academic Senate. Dr. A. K. Walker identified the parasitoids at the Commonwealth Institute of Entomology. Excellent technical assistance was provided by F. Arias G., Y. Tembo, B. Chiwaula, C. Kafwafwa, R. Kantiki, K. Luhanga, P. Mkupatira, and M. Mwafulirwa. Thanks are expressed to K. Kester, P. Rosset and L. Weir for improving previous drafts.

References Ajayi, O., 1990. Possibilities for integrated control of the millet stem borer, Actgona ignefusalis Hampson (Lepidoptera: Pyralidae) in Nigeria. Ins. Sci. Appl., 11(2): 109117. All, J.N. and Musick, G.J., 1986. Management of vertebrate and invertebrate pests. In: M.A. Sprague and G. Triplett (Editors), No-Tillage and Surface Tillage Agriculture. Wiley, New York, pp. 347-388. Altieri, M.A. and Letourneau, D.K., 1982. Vegetation management and biological control in agroecosystems. Crop Prof., l (4): 405-430. Altieri, M.A., Schoonhoven, S. and Doll, J.D., 1977. The ecological role of weeds in insect pest management systems: A review illustrated with bean (Phasiolus vulgaris L.) cropping systems. PANS, 23: 185-206. Andow, D.A., 1991. Vegetational diversity and arthropod population response. Annu. Rev. Entomol., 36:561-586. Baliddawa, C.W., 1985. Plant species diversity and crop pest control: an analytical review. Insect Sci. Applic., 6: 479487.

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D.K. Letourneau/Agriculture. Ecosystems and Environment 50 (1994) 103-111

Barbosa, P., 1988. Natural enemies and herbivore-plant interactions: influence of plant allelochemicals and host specificity. In: P. Barbosa and D.K. Letourneau (Editors ), Novel Aspects of Insect-Plant Interactions. Wiley, New York, pp. 201-229. Blumberg, A.Y. and Crossley, Jr., D.A., 1983. Comparison of soil surface arthropod populations in conventional tillage, no-tillage and old field systems. Agro-Ecosystems, 8: 247-253. Brust, G.E., Stinner, B.R. and McCartney, D,A., 1986. Tillage and soil insecticide effects on predator-black cutworm (Lepidoptera: Noctuidae) interactions in corn agroecosystems. J. Econ. Entomol., 78: 1389-1392. Bugg, R.L., Phatak, S.C. and Dutcher, J.D., 1990. Insects associated with cool-season cover crops in Southern Georgia: Implications for pest control in truck-farm systems and pecan agroecosystems. Biol. Agric. Hort., 7:17-45. Cardona, C., van Schoonhoven, A., Gomez, L., Garcia, J., and Garzon, F., 1981. Effect of artificial mulches on Empoasca krameri Ross and Moore populations and dry bean yields. Environ. Entomol., 10: 705-707. Chiang, H.S. and Talekar, N.S., 1980. Identification of sources of resistance to beanfly (Ophiomyia phaseoli) and two other agromyzid flies ( Ophiomyia centrosematis, Melanagromyza sojae) in soybean and mungbean. J. Econ. Entomol., 73(2): 197-199. Conelly, W.T., 1987. Perception and management of crop pests among subsistence farmers in South Nyanza, Kenya. In: J. Tait and B. Napompeth (Editors), Management of Pests and Pesticides: Farmers' Perceptions and Practices. Westview Press, Boulder, CO, pp. 198-209. Duffey, S.S. and Bloem, K.A., 1986. Plant defense, herbivore-parasite interactions and biological control. In: M. Kogan (Editor), Ecological Theory and Integrated Pest Management Practice, Wiley, New York. Floor, J., Stoetzer, H.A. and Okongo, A.O., 1984. Increased tolerance of dry beans to bean fly as a result of fertilizer application. Ann. Rep. Bean Improv. Coop., 2: 141-142. Fox, L.R., Letourneau, D.K., Eisenbach, J. and van Nouhuys, S., 1990. Parasitism rates and sex ratios of a parasitoid wasp: effects of herbivore and plant quality. Oecologia, 83: 414-419. Funderbunk, J.E., Teare, I.D. and Rhoads, F.M., 1991. Population dynamics of soybean insect pests vs. soil nutrient levels. Crop Sci., 31 (6): 1629-1633. Greathead, D.J., 1968. A study in East Africa of the bean flies (Dipt., Agromyzidae) affecting Phaseolus vulgaris and their natural enemies, with the description of a new species of Melanogromyza Hend. Bull. Ent. Res., 59: 541561. Hill, D.S., 1983. Agricultural Insect Pests of the Tropics and their Control. Cambridge Univ. Press, Cambridge, 746 pp. House, G.J. and All, J.N., 1981. Carabid beetles in soybean agroecosystems: community composition and ecosystem interactions. Environ. Entomol., 10:194-196. House, G.J. and Stinner, B.R., 1983. Arlhropods in no-tillage soybean agroecosystems: community composition and

ecosystem interactions. Environ. Management, 7: 23-28. Hunt, D.W.A., Drury, C.F. and Maw, H.E.L., 1992. Influence of nitrogen on the performance of Colorado potato beetle (Coleoptera: Chrysomelidae) on tomato. Environ. Entomol., 21 (4): 817-821. Karel, A.K. and Maerere, A.P., 1985. Evaluation of common bean cultivars for resistance to bean fly ( Ophiomyia phaseoli Tryon). Ann. Rep. Bean Improvement Coop., 28: 1516. Karel, A.K. and Matee, J.J., 1986. Yield Losses in common beans following damage by beanfly, Ophiomyia phaseoli Tryon (Diptera: Agromyzidae). Ann. Rep. Bean Improvement Coop., 29: 115-116. Lin, F.J., Wang, T.C. and Hsieh, C.Y., 1977. Population fluctuations of soybean miner, Ophiomyia phaseoli (Tryon). Bull. Inst. Zool., Academia Sinica, 17( 1): 69-76. Litsinger, J.A. and Ruhendi. 1984. Rice stubble and straw mulch suppression of preflowering insect pests of cowpeas sown after puddled rice. Environ. Entomol., 13: 509514. Litsinger, J.A., Price, E.C. and Herrera, R.T., 1980. Small farmer pest control practices for rain-fed rice, corn, and grain legumes in three Philippine provinces. Philipp. Entomol., 4: 65-96. Necibi, S., Barrett, B.A. and Johnson, J.W., 1992. Effects of a black plastic mulch on the soil and plant dispersal of cucumber beetles, Acalymma vittatum (F.) and Diabrotica undecimpunctata howardi Barber (Coleoptera: Chrysomelidae ), on melons. J. Agric. Entomol., 9 ( 2 ): 129-135. Pavuk, D.M. and Barrett, G.W., 1993. Influence of successional and grassy corridors on parasitism of Plathypena scabra (F.) (Lepidoptera: Noctuidae) larvae in soybean agroecosystems. Environ. Entomol., 22 (3): 546. Russell, E.P., 1989. Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environ. Entomol., 18: 590-599. Scriber, J.M., 1984. Nitrogen nutrition of plants and insect invasion, In: R.D. Hauck (Editor), Nitrogen in Crop Production. Am. Soc. Agron., pp. 441-460. Seshu-Reddy, K.V., 1990. Cultural control of Chilo spp. in graminaceous crops. Insect Sci. Appl., 1I (4/5): 703-712. Shaw, M.C., Wilson, M.C. and Rhykerd, C.L., 1986. Influence of phosphorus and potassium fertilization on damage to alfalfa, Medicago sativa L., by the alfalfa weevil, Hypera postica (Gyllenhall) and potato leafhopper, Ernpoascafabae (Harris). Crop Prot., 5: 245-249. Sheehan, W. and Shelton, A.M., 1989. Parasitoid response to concentration of herbivore food plants: finding and leaving plants. Ecology, 70: 993-998. Sofranko, A.J. and Fliegel, F.C., 1989. Malawi's Agricultural Development: A Success Story? Agric. Econ., 3:99-113. Statistical Analysis Systems Institute, 1988. SAS/STAT Guide for Personal Computers, 6th Edn., Cary, NC. Talekar, N.S., Yang, H.C. and Lee, Y.H., 1988. Morphological and physiological traits associated with agromyzid (Diptera: Agromyzidae) resistance in mungbean. J. Econ. Entomol., 81 (5): 1352-1358.

D,K. Letourneau / Agriculture, Ecosystems and Environment 50 (1994) 103-111 Tengecho, B. and Couison, C.L. and D'Souza, H.A., 1988. Distribution and effect of bean flies, Ophiomyia phaseoli and O. spencerella, on beans at Kabete, Kenya. Insect Sci. Applic., 9(4): 505-508. Titayavan, M., 1987. The phenology and distribution pattern of soybean stem flies and their natural enemies in the Upper Northern Thailand. Dept. of Entomol., Chiang Mai Univ., Thailand, 72 pp. Tonhasca, Jr., A. and Stinner, B., 1991. Effects of strip intercropping and no-tillage on some pest and beneficial inver-

tebrates of corn in Ohio. Environ. Entomol., 20 ( 5 ):

111 1251 -

1258.

Turnock, W.J., Timlick, B. and Palaniswamy, P., 1993. Species and abundance of cutworms (Noctuidae) and their parasitoids in conservation and conventional tillage fields. Agric. Ecosystems Environ., 45: 213-227. Zethner, O., 199 I. Integrated pest and land management experiences and perspectives in the Gambia. Insect Sci. Appl., 12(5/6): 541-545.