This article was downloaded by: [University of North Carolina]On: 11 November 2014, At: 12:46Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office:Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

International Journal of Pest ManagementPublication details, including instructions for authors and subscriptioninformation:http://www.tandfonline.com/loi/ttpm20

Pest status and ecology of bean stem maggot(Ophiomyia spp.: Diptera: Agromyzidae) on theNiassa Plateau, MozambiqueG. DaviesPublished online: 26 Nov 2010.

To cite this article: G. Davies (1998) Pest status and ecology of bean stem maggot (Ophiomyia spp.: Diptera:Agromyzidae) on the Niassa Plateau, Mozambique, International Journal of Pest Management, 44:4, 215-223, DOI:10.1080/096708798228130

To link to this article: http://dx.doi.org/10.1080/096708798228130

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”)contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensorsmake no representations or warranties whatsoever as to the accuracy, completeness, or suitabilityfor any purpose of the Content. Any opinions and views expressed in this publication are the opinionsand views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy ofthe Content should not be relied upon and should be independently verified with primary sourcesof information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings,demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arisingdirectly or indirectly in connection with, in relation to or arising out of the use of the Content.

This article may be used for research, teaching, and private study purposes. Any substantialor systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, ordistribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use canbe found at http://www.tandfonline.com/page/terms-and-conditions

Pest status and ecology of bean stem maggot (Ophiomyia spp.: Diptera: Agromyzidae) on

the Niassa Plateau, Mozambique

(Keywords: bean stem maggot, Ophiomyia, Agromyzidae, ecology, pest control, Phaseolus vulgaris, Mozambique)

G. DAVIES

Instituto Nacional de InvestigacaÄ o Agrono mica, EstacaÄ o Agra ria de Lichinga, C.P. 238, Lichinga, Niassa, Mozambique

Abstract. Research was carried out on the Niassa Plateau, northernMozambique, with the aim of determining the phenology and importanceof bean stem maggot (BSM) (Ophiomyia spp.: Diptera: Agromyzidae) oncommon beans. The objective of the study was to gather information inorder to develop elements of an integrated control programme againstBSM for use by farmers in the local cropping system, characterized bylimited access to external inputs. Date of sowing trials were used in sixconsecutive rainy seasons to determine infestation rate of BSM duringthe main bean growing season and to determine damage due to thepest. These trials were also used to evaluate insecticide treatmentsagainst BSM and, at the same time, to undertake a survey of BSMparasitoids and the rates of parasitism from puparia collected at eachsowing date. It was observed that infestation rates of BSM increasedwith delay in date of sowing in each of the two growing periods duringthe season and that percentage plant loss and yield decrease wascorrelated with number of BSM per plant. Insecticide seed treatment waseffective in reducing infestation rates. BSM has two main parasitoids thatprobably play a role in limiting BSM population towards the end of thefirst growing period.

1. Introduction

Common bean (Phaseolus vulgaris L.) is a major

component of the local cropping system on the Niassa plateau

in northern Mozambique. The principal cropping system

consists of a maize ± bean ± Irish potato intercrop, grown on

large ridges during the rainy season between November and

June. Beans are grown in two distinct periods during the rainy

season, first as an intercrop (with maize as the principal crop)

between November and February and then as a relay crop

between March and June. They are also grown with residual

moisture in valley bottoms in the dry season between July and

November. Beans are used both for food and to generate a

cash income.

There are various physical and biological constraints upon

bean production on the plateau, depending on the growing

season, of which bean stem maggot (BSM) (Ophiomyia spp.

(Diptera: Agromyzidae)) is considered to be one of the most

important, especially in the rainy season (Heemskerk et al.,

1988). In 1988, work was started in Niassa to investigate the

phenology and importance of BSM in the context of the local

cropping system and as part of a general programme to improve

research efforts on common beans on the plateau. The specific

objective of the study has been to develop an integrated control

programme of pests and diseases for farmers in the region who

have very limited access to external inputs (fertilizers, insecti-

cides, etc.).

Recently, BSM has been the object of a research

programme initiated by the International Centre for Tropical

Agriculture (CIAT) in the eastern and southern African region

and aimed at coordinating the efforts of national research

programmes to understand the phenology of the pest, to

develop cultural and chemical control recommendations and to

develop resistant varieties. Three species are known to exist in

the southern Africa region (Ophiomyia spencerella (Greathead),

Ophiomyia phaseoli (Tyron) and Ophiomyia centrosematis (de

Meij.)) and methodologies have been developed to distinguish

between them (Allen and Smithson, 1986). Although the species

overlap in their distribution, they seem to have differing

environmental preferences. Sithanantham and Sohati (1989)

suggest that O. spencerella prefers areas of high rainfall and

medium to high altitude, while O. centrosematis prefers lower

altitudes. O. phaseoli was found in all areas in this Zambian

study. Autrique (1989), working in Burundi, found O. spencerella

to be predominant at high altitudes (1400 m± 2000 m) and to be

present at lower altitudes as part of a complex that included the

other two species. Replacement of O. phaseoli by O. spencer-

ella during the course of a season has also been observed in

Tanzania (Oree et al., 1990).

The life cycle of and damage caused by these pests in Africa

are well described (Tayor, 1958; Lays and Autrique, 1987; Karel

and Autrique, 1989). The female fly lays eggs in the stem,

hypocotyl or leaves of recently emerged bean plants although

the preferred oviposition sites differ depending on the species.

The larvae emerge after 2 ± 4 days and tunnel in the leaf petioles

and stem where they can cause extensive damage, especially in

young plants. Seriously infested plants suffer premature leaf fall

and can be severely stunted or killed. The fully grown larvae

pupate below the stem epidermis at ground level, the larval

period lasting about 10 days. The concentration of pupae at the

base of the stem causes swelling and can split open the stem

facilitating stem rots. However, affected bean plants often

produce adventitious roots above the pupation zone, and this

allows them to recover partially or fully from attack.

High damage levels have been reported by many sources,

as summarized by Gonzales (1986) with up to 50% or more

plant loss in Africa (Greathead, 1968; Karel and Autrique, 1989).

Tengecho et al. (1988) concluded that it was difficult to show a

relationship between grain yield and infestation of BSM, perhaps

due to the capacity of each plant to recuperate after the initial

infestation. Ampofo (1993) also reports strong interactions

between BSM and root rot diseases in some locations in

0967-0874/98 $12.00 Ó 1998 Taylor & Francis Ltd

INTERNATIONAL JOURNAL OF PEST MANAGEMENT, 1998, 44(4) 215± 223

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014

Tanzania, confirmed by screenhouse studies with Fusarium

spp., which can cause high mortality with otherwise low

infestations of BSM.

Many recommendations exist for cultural and chemical

control of BSM (for example summarized in Allen and Smithson

(1986)), seed treatment with endosulfan being possibly the most

effective in reducing infestation levels in purely physical terms

(Abate, 1991). Biological control involving parasitoids has been

investigated and described by Greathead (1968) among others.

Two Hymenopteran parasitoids parasitize BSM larvae in

significant numbers, a braconid, Opius melanagromyzae ( = pha-

seoli) Fischer (Braconidae: Hymenoptera), and a eucoilid,

Eucoilidea nitida (Cynpidae: Hymenoptera). Although they do

not seem to suppress infestation below economic damage

levels, both Sitanantham and Sohati (1989) and Autrique (1989)

consider that these parasitoids are at least partially responsible

for suppressing BSM incidence on late planted beans due to

increasing pupal parasitism during the season.

In this paper I present the results of a series of trials aimed

at establishing basic data on the phenology and importance of

BSM on the Niassa plateau and at formulating topics for further

research, together with initial recommendations for integrated

control of BSM in the local cropping system, recommendations

which are to be subsequently evaluated in farmers’ fields.

2. Materials and methods

A series of date of sowing trials was initiated at Lichinga

Agricultural Research Station in December 1988 and imple-

mented in six consecutive growing seasons. The objective was

to obtain basic data about BSM on the Niassa Plateau, including

information about infestation rates with sowing date in the main

(rain fed) growing season and subsequent damage levels,

simple life cycle data including information on parasitism, and

the efficacy of various insecticide treatments against BSM.

In each rainy season, separate trials were sown at monthly

intervals after the onset of the rains (usually mid-November to

early December), until their conclusion (early to late April). In the

majority of seasons trials were therefore sown on 14 December,

14 January, 14 February, 14 March and 14 April, depending on

local planting conditions. Sowings in November and April

depended on rainfall and were not undertaken if the season

had not started (no rain in November) or had ended (rain

finished by mid-March). Trials were sown at separate locations

within the research station to avoid carry-over between sowing

dates and to better sample `background’ BSM numbers. Exact

distance between trials varied but was always greater than

300 m and trials were usually isolated by other crops or fallow.

Each trial consisted of four treatments with four replications

in a Latin Square design. The treatments always included the

local variety Manteiga, the local variety Encarnado, with and

without insecticide treatment, and an improved variety, A 417,

with suspected tolerance or resistance to BSM. The insecticide

treatments to the variety Encarnado varied depending on local

availability over the trial period (see Section 3.3) but included

cypermethrin as a foliar treatment, endosulfan as a seed

treatment and diazinon as a seed treatment (the locally

recommended control method).

Trials were prepared using the local practice of planting on

ridges 1.40 m apart and beans sown at local densities (two

lines of beans to a ridge with 0.25 m between seed holes and

two plants a hole). All trials were fertilized at the locally

recommended rate of the equivalent of 40 kg/ha of nitrogen,

with urea or ammonium sulphate, 18 days after emergence

(d.a.e.). Phosphate and potassium are not considered limiting in

the research station soils. The trials were carried out in

monoculture in contrast to the local practice of maize-bean

intercropping to simplify management. (Talekar and Chen

(1985) did not observe any reduction in BSM infestation in

over 60 different intercrops.)

BSM infestation was assessed from counts of larvae and

pupae in 10 plants chosen at random in each plot 30 d.a.e.

Pupae collected at 30 d.a.e. were separated according to

species, using pupal colour and number of spiracles as

recommended by Allen and Smithson (1986). The separated

pupae were kept on blotting paper in glass vials sealed with

muslin, and the emergence of adult flies and parasitoids was

noted over a period of 6 months. In the first season counts were

made at daily intervals in all five sowing trials to monitor adult fly

and parasitoid emergence. In subsequent seasons counts for

each trial were made at monthly intervals to reduce the work

load.

Plant stand was counted at 10 d.a.e. and at harvest in order

to calculate the percentage plant loss. The yield of dry grain was

recorded in each plot after harvest and drying.

Results for the trials at each sowing date (number BSM/

plant, percentage plant loss and yield for each treatment) were

subjected to an ANOVA using the MSTATC statistical package

from Michigan State University, USA. At each sowing date

comparisons were made between varieties and the treated and

untreated plots for BSM infestation, percentage plant loss and

yield. Differences were tested using the least significant

difference (LSD) test where appropriate. Data were combined

over the six seasons and a regression analysis made to relate

BSM infestation with percentage plant loss and yield using the

same package. Regressions were tested for differences

between varieties, sowing dates and seasons.

3. Results

3.1. Observations on the biology and parasitoids of BSM

The principal species of BSM encountered on the Niassa

plateau was Ophiomyia spencerella characterized by a black

puparium, representing 91.9% ( 6 7.8) or more of pupae

sampled at each sampling date (table 1). The other species

characterized by a brown puparium were present at a reduced

rate. Together, Ophiomyia phaseoli and Ophiomyia centrose-

matis represented 8.1% ( 6 7.8) of pupae sampled but O.

centrosematis was present in very low numbers, less than 1%

of pupae sampled, and these two species were not routinely

separated in this work. There is a tendency for a greater

proportion of O. phaseoli/centrosematis at the beginning of the

rainy season in December and January (table 1).

Eucoilidea nitida was the principal parasitoid found para-

sitizing BSM followed by the parasitoid Opius melanagromyzi-

dae. The latter seems to be more efficient at parasitizing O.

phaseoli and is possibly the reason for the lower numbers of this

species found infesting beans (table 2(a)). A very low

percentage of other unidentified parasitoids was observed.

G. Davies216

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014

Generally, about half (47.2% 6 3.1) of collected puparia

emerged although total eclosion decreased throughout the

season (table 2(b)). Of emerged puparia, about half were BSM

adults (23% 6 2) and half parasitoids (23% 6 2). Percentage

emergence of parasitoids varied with sowing date, being

generally higher in the middle of the season.

Pest status and ecology of bean stem maggot 217

Table 1. BSM species sampled with date of sowing over six seasons, 1988 ± 94

Date of sowing No. of pupae% black pupae

Ophiomyia spencerella% Brown pupae

O. phaseoli/centrosematis

23 December 198812 January 19891 February 1989

21 February 198914 March 1989

303234134263350

91.793.694.092.494.3

8.36.46.07.65.7

11 December 198913 January 199014 February 199014 March 1990

4266140594

59.579.792.387.2

40.520.37.7

12.8

14 December 199014 January 199114 February 199114 March 199114 April 1991

4119550131942

87.894.993.696.295.2

12.25.16.43.84.5

14 December 199114 January 199214 February 199214 March 199214 April 1992

1539523984

665

100.091.995.898.898.5

0.08.14.21.21.5

14 December 199214 January 199315 February 199315 March 199314 April 1993

117389308237207

93.288.786.496.699.5

6.811.313.63.40.5

15 November 199315 December 199314 January 199414 February 199414 March 199414 April 1994

4397

57771887

539

93.082.593.489.797.798.0

7.017.56.7

10.32.32.0

Mean ( 6 s.e.) Ð 91.9 ( 6 7.8) 8.1 ( 6 7.8)

Table 2. Adult BSM and parasitoid emergence from collected puparia with (a) species of BSM (1990 ± 94) and (b) date of sowing in each season

(1988 ± 94)

% Puparia ecloded with:

SpeciesNo. pupaecollected

% Emergence(total) BSM Eucloidea Opius Other parasitoids

% Parasitism(total)

(a) With species (from December 1990)O. spencerellaO. phaseoliMean ( 6 s.e)

5453362Ð

43.848.5

46.1 ( 6 3.2)

25.414.7

20.2 ( 6 3.2)

10.212.8

11.5 ( 6 2.8)

7.620.4

13.8 ( 6 2.4)

0.50.7

0.6 ( 6 0.3)

18.333.9

25.9 ( 6 3.1)

(b) With date of sowing (1988 ± 1994)Sowing dateNovemberDecemberJanuaryFebruaryMarchAprilMean ( 6 s.e)

43615

2451256811711453

Ð

65.264.156.343.942.826.4

47.2 ( 6 3.1)

27.933.429.114.318.518.6

23.0 ( 6 2.0)

32.68.0

15.116.712.5

3.512.6 ( 6 1.7)

4.76.8

11.912.510.4

6.89.8 ( 6 1.0)

0.00.00.30.51.41.2

0.6 ( 6 0.2)

37.314.927.329.624.211.4

23.0 ( 6 2.0)

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014

In the first season, peak emergence of BSM adults was 42

days after crop emergence and for parasitoids 48 ± 58 d.a.e.

(figure 1). BSM adult eclosion was not observed after about

60 d.a.e. in any season although small numbers of parasitoids

continued to emerge until 6 months or more after sampling in the

field.

Various environmental factors including temperature (max-

imum or minimum), precipitation (mm of rain), relative humidity

(%) and number of rain-free days have been considered

important for severity of BSM infestation (Talekar and Chen,

1985). A simple regression analysis of BSM numbers per plant

as a function of each of these factors, both during the oviposition

period (5 ± 10 d.a.e.) and month of sowing, showed a significant

inverse relationship between the average maximum monthly

temperature and numbers of BSM per plant (slope (b) 6 standard

error= Ð 0.76 6 0.37, intercept (a) = 25.80, correlation

(r ) = Ð 0.37, Student’s t value (t ) = 2.07, P = 0.047 with 30

observations (n)). Analysis did not reveal any other direct

relationships.

Parasitoids have been considered important in limiting BSM

infestation, especially late in the season. BSM numbers

encountered per plant were not significantly correlated with

G. Davies218

Figure 1. Number of BSM and parasitoid adults emerging from BSM puparia with time after crop emergence, averaged over five sowing dates, first season, 1988 ± 89.

a

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014

percentage total parasitism in the same generation. However,

the number of BSM encountered infesting beans was signifi-

cantly correlated with the percentage parasitism in the preceding

generation (b= Ð 17.01 6 8.02, a = 72.60, r= Ð 0.41, t= 2.12,

P = 0.045, n = 24), especially of Eucoilidea nitida

(b= Ð 14.26 6 6.89, a = 47.06, r= Ð 0.41, t= 2.07, P = 0.050,

n= 24). It seems likely that the reduced infestation rate of

BSM on beans at the start of the second growing season is due

to the increase in parasitism during the first growing season

resulting in a decrease in BSM population at the beginning of the

second.

3.2. BSM infestation with date of sowing

Infestation of BSM on beans varied with date of sowing

during the main cropping season but the pattern was similar

across seasons for each variety (figure 2(a)). In all three

varieties infestation was low at the start of each bean planting

Pest status and ecology of bean stem maggot 219

b

c

Figure 2. (a) Number BSM per plant at 30 d.a.e., (b) percentage plant loss and (c) yield (kg/ha) of three bean varieties over six seasons in date of sowing trials at

Lichinga, 1988 ± 94.

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014

season (early to mid-December in the first season and early to

mid-March in the second) and rose with delay in sowing,

especially in the first planting season. In general, A 417

tended to have less BSM infestation in comparison with the

two local varieties. Encarnado and Manteiga (P< 0.05 in 9 of

30 trials).

Percentage plant loss was generally high and tended to be

greater in the middle of the rainy season (January and February,

figure 2(b)) although the differences between the varieties are

not generally significant (P< 0.05 in 8 out of 30 trials).

In contrast, the dry grain yield of beans was higher when sown

early in each planting season (December and March, figure 2(c)).

In the middle (January, February) and end (April) of the rainy

season yield was generally low. Within each planting trial A 417

tended to yield better than the local varieties, especially in the

middle of the season (P< 0.05 in 16 out of 30 trials).

G. Davies220

Figure 3. Number of BSM per plant at 30 d.a.e. with and without insecticide treatment to local bean variety Encarnado over six seasons, 1988 ± 94. 1, Cypermethrin

2+7 d.a.e.; 2, cypermethrin 2,7+14 d.a.e.; 3, diazinon 27.5 ec 5 ml/kg seed treatment; 4, diazinon 60 ec 2 ml/kg seed treatment; 5, endosulfan 50 ec 7.5 ml/kg seed

treatment.

Table 3. Regression analysis for percentage plant loss as a function of number of BSM per plant at 30 d.a.e., 1988 ± 94

Differences

Factor Level df b ( 6 s.e.) a r t Slope Level

Total All 88 3.00 6 0.65 30.36 0.44 4.61***a

Variety EncardoManteiga

A 417

282828

2.64 6 1.113.19 6 1.043.93 6 1.65

29.9729.9828.56

0.410.500.41

2.37*3.06*2.38* ns ns

Sowing date NovemberDecember

JanuaryFebruary

MarchApril

11616161615

9.10 6 4.534.14 6 1.062.96 6 1.220.96 6 1.294.23 6 2.401.16 6 0.66

24.2718.5130.2273.8926.3517.82

0.890.700.520.180.400.44

2.01ns3.90***2.44*0.75ns1.76ns1.77ns ns ***

Season 1988 ± 19891989 ± 19901990 ± 19911991 ± 19921992 ± 19931993 ± 1994

131013131316

0.92 6 2.344.70 6 1.846.72 6 0.830.53 6 1.734.93 6 2.482.83 6 1.22

50.4628.3515.8339.8318.4430.49

Ð 0.110.630.910.080.480.50

Ð 0.39ns2.56*8.07***0.30ns1.99ns2.33* * ns

df Ð degrees of freedom; b Ð slope ( 6 standard error); a Ð intercept; r Ð correlation coefficient; t Ð Student’s t value (H0: b=0).a***P < 0.001, **0.001< P < 0.1, ***0.01< P < 0.05; ns, not significantly different by t-test/ANOVA.

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014

3.3. BSM control with insecticide

This series of trials was also used to evaluate various

locally available insecticide treatments against BSM over the

duration of the trial. For this purpose the local variety

Encarnado was included at all sowing dates both treated and

untreated with insecticide.

BSM control proved possible with a range of insecticides

and application methods (figure 3). Cypermethrin (Ripcord 20

EC, 1 ml/l) applied as a foliar spray 2, 7 and 14 d.a.e.,

diazinon (Basudine 60 EC, 2 ml/kg) as a seed treatment and

endosulfan (EndosulfaÄ o 50 EC, 7.5 ml/kg) as a seed treatment

have all proved effective in significantly reducing BSM

infestation (P < 0.05 in 24 out of 29 trials). There is a tendency

for control to be less effective mid season (January, February)

and in this respect endosulfan provided the most consistent

protection.

3.4. Pest status of BSM

Beans are important both as greens (leaves and fresh pods)

and dry grain for local subsistence farmers, and so percentage

plant loss and final dry grain yield are both important production

indices. Combining data from across all the seasons and using

regression analysis both percentage plant loss (table 3) and final

yield of dry grain (table 4) were significantly related to BSM

infestation (r= 0.44, P < 0.001 and r= Ð 0.67, P< 0.001 respec-

tively). Percentage plant loss increases directly as a function of

number of BSM per plant while yield falls exponentially as a

function of BSM number.

Variety, sowing date and season potentially influence not

only BSM attack but also other bean production factors. The

data were tested for differences between varieties, sowing dates

and seasons in terms of response (slope) and level (intercept) in

order to assess better the link between BSM infestation and

percentage plant loss and yield.

There were no significant differences between varieties in

terms of their response (slope) or level (intercept) for percentage

plant loss (table 3) or yield (table 4). This suggests that A 417 is

no more resistant to BSM infestation than the two local varieties.

There were significant differences between sowing dates in

level of percentage plant loss (F = 25.9, P< 0.001) (table 3) and

yield (F = 3.6, P = 0.005) (table 4) as a function of BSM

infestation although the response did not differ significantly.

Yield levels also differ significantly (F = 3.8, P = 0.004) with

season (table 4) and there were significant differences in

response to BSM infestation with season for both percentage

plant loss (F = 2.3, P = 0.05) and yield (F = 4.4, P = 0.002).

Differences in level of response are to be expected between

sowing dates and between seasons due to uncontrollable

factors such as weather affecting bean development and BSM

infestation. Little difference in response would be expected to

BSM infestation across sowing dates and seasons if this was an

important limiting factor in bean production. It seems that the

significant differences in response seen were largely due to the

first season (1988 ± 89) in that it was atypical for showing both

decreasing percentage plant loss and increasing yield with

increasing BSM infestation.

4. Discussion

The observations made during the course of this trial

suggest that BSM is an important pest of beans on the Niassa

Plateau. It reached high infestation levels in all years of the trial

and displayed a more or less regular cycle of infestation during

each of the six seasons. The principal species found infesting

beans in each season was O. spencerella. There was a

tendency for a larger proportion of O. phaseoli/centrosematis

Pest status and ecology of bean stem maggot 221

Table 4. Regression analysis for dry grain yield (kg/ha) with number (In transformed) of BSM per plant, 1988 ± 1994

Differences

Factor Level df b ( 6 s.e) a r t Slope Level

Total All 88 Ð 183.8 6 21.6 461.2 Ð 0.67 Ð 8.51***a

Variety EncarnardoManteiga

A 417

282828

Ð 183.5 6 36.3Ð 192.4 6 35.4Ð 172.1 6 47.4

461.1476.2443.9

Ð 0.69Ð 0.72Ð 0.57

Ð 5.05***Ð 5.43***Ð 3.63*** ns ns

Sowing date NovemberDecemberJanuaryFebruary

MarchApril

11616161616

Ð 894.9 6 405.3Ð 265.4 6 102.8Ð 176.6 6 85.7

Ð 6.7 6 23.4Ð 179.7 6 50.0Ð 188.4 6 23.0

999.0588.3506.8

35.7414.0486.1

Ð 0.91Ð 0.54Ð 0.46Ð 0.07Ð 0.67Ð 0.92

Ð 0.221nsÐ 2.58*Ð 2.06nsÐ 0.29nsÐ 3.60*Ð 8.18*** ns **

Season 1988 ± 19891989 ± 19901990 ± 19911991 ± 19921992 ± 19931993 ± 1994

131013131316

47.4 6 49.6Ð 143.6 6 45.3Ð 337.4 6 53.9Ð 131.2 6 39.2Ð 216.5 6 85.1Ð 149.6 6 35.9

Ð 28.5354.5783.6384.0514.3421.2

0.26Ð 0.71Ð 0.87Ð 0.68Ð 0.58Ð 0.72

0.96nsÐ 3.17*Ð 6.26***Ð 3.34**Ð 2.54**Ð 4.16*** ** **

df Ð degrees of freedom; b Ð slope ( 6 standard error); a Ð intercept; r Ð correlation coefficient; t Ð Student’s t value (H0: b=0).a***P < 0.001, **0.001< P < 0.1, ***0.01 < P < 0.05; ns, not significantly different by t-test/ANOVA.

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014

to be found at the beginning of each main season, although not

large enough to be considered a species replacement as seen

in other bean growing areas (Oree et al., 1990).

Despite the difficulty of directly attributing damage to BSM

infestation, the analysis of the results suggests that, within the

range of infestations seen over the six seasons, percentage

plant loss will increase as a linear function of BSM infestation

and yield will decrease as an exponential (ln) function. In terms

of the average infestation of five BSM per plant observed over

the whole period this represents a 45.4% plant loss, an increase

of 15% plant loss in the presence of BSM, and a 329.3 kg/ha or

a 71.4% yield reduction. A considerable loss of yield due to this

pest. At the traditional sowing times (December and March)

BSM infestation is usually lower, 0.5 ± 1.0 BSM per plant,

representing about 32.6% plant loss, an increase of 2.2% plant

loss in the presence of BSM, and a 52.9 kg/ha or 11.5% yield

reduction.

In the trials yield was greatly reduced with increasing

infestation. Though caused at least partially by an increased

percentage plant loss, given the form of the yield response curve

to BSM infestation, it seems likely there are various other

aggravating factors. This suggests that BSM tunnelling in the

stem, besides generally weakening the plant, may also facilitate

the entry of root rots at ground level which has the potential to

rapidly increase yield loss even with small increases in

infestation (Ampofo, 1993). Sclerotium rolfsii Sacc., Rhizoctonia

solani KuÈhn and Fusarium solani (Martius) were all identified

infecting bean plants during the course of the trials.

Given the estimated losses due to BSM, the results of the

study can be used to suggest and formulate recommendations

for integrated control of this pest in the local cropping system. It

must, however, be borne in mind that there are also other

important limiting factors to bean production, especially soil

fertility and foliar diseases, which need to be addressed before

bean yield will significantly increase. In the farming system as a

whole, another important limiting factor is the poor commercia-

lization prospects in the context of the generally underdeveloped

economy on the plateau.

Utilization of cultural control recommendations should form

the basis of any integrated control programme for subsistence

farmers (Altieri, 1993). These data show that the most effective

cultural control method was to sow beans early in each growing

season (early December and early March) when natural

infestation rates due to BSM are low; in the first planting season

due to the dry season break in the life cycle in the main farm

(machamba), and in the second, due to the increase in

parasitism and the subsequent reduction of BSM population

towards the end of the first growing season.

Observations made in these trials show that most adult flies

emerge within 60 d.a.e. of the crop and so that although there is

little carry-over between seasons in crop residues, it is important

not to overlap crop seasons in the field. It is therefore

recommended to leave as long an interval as possible between

planting seasons, compatible with good husbandry (as, for

example, beans can suffer moisture stress if planted late in the

second planting season). In combination with this it is advisable

to plant beans in any given area simultaneously to avoid build up

of BSM numbers. Actual destruction of crop residues is not

highly beneficial in the case of BSM but is beneficial in the

control of various common foliar diseases.

Indigenous natural enemies are often important in suppres-

sing pest populations. Observations showed that there are two

principal parasitoids causing significant BSM mortality, although

they do not generally maintain the population of the pest below

damaging levels. Percentage parasitism increased during the

cropping season, especially the first bean season, and seemed

to play a part in reducing BSM infestation at the start of the

second bean growing season. Future research should aim at

clarifying the relationships between the BSM species and the

two principal parasitoids, especially the role of parasitoids in

suppressing BSM numbers with time during the whole cropping

season, and the possible role of Opius melanagromyzidae in

suppressing populations of O. phaseoli. These studies should

aim to identify areas where natural parasitism rates could be

enhanced, particularly at the start of the main cropping season

when field rates are low after the long dry season. In any case,

no insecticide should be applied to the intercrop between 40 and

70 d.a.e. of beans as this is the main period of parasitoid

emergence. It seems likely that if parasitoid emergence is

disrupted in the first growing season then BSM population will be

high for the start of the second season.

These trials suggest that the potential for chemical control of

BSM is good although protection levels must be high given the

large initial yield loss seen with even a small increase in

infestation rates. Endosulfan and diazinon seed treatments as

well as cypermethrin applied as a foliar spray 2, 7 and 14 d.a.e.

were all effective in controlling BSM. Seed treatment would be

preferable to foliar sprays since it should have less direct impact

on the observed parasitoids as well as being safer for farmers.

Endosulfan is more consistent in controlling BSM and its use

has also been recommended in other studies (Abate, 1991;

Trutmann et al., 1992). Further work should be done to

investigate and improve the effectiveness of diazinon seed

treatment as endosulfan is generally recognized as being toxic

in the environment and has actually been recently banned in

Mozambique.

It is difficult to calculate economic indicators for low

external input farmers due to the number of different factors

they take into account when making decisions (MacKay et al.,

1993) as well as their marginalization in the economy. Given

an otherwise healthy crop, seed treatment should be economic

even with low levels of BSM infestation. The cost of treatment

would be equivalent to about the cost of 3 kg of beans at

current prices, assuming a sowing rate of about 40 kg/ha

observed in the local cropping system and the current price of

insecticide. Chemical control is, however, generally beyond the

reach of the majority of farmers on the plateau due to various

factors, the most important being availability at the right time

and price (due to the necessity to buy in bulk). In addition,

from the cropping system perspective, it would be better not to

use insecticides at all in the first growing season when

expected yield is anyway low due to the high incidence of

foliar disease. In this last case Trutmann et al. (1992) report

that mixed fungicide/insecticide seed treatment can reduce risk

to the farmer’s investment.

5. Conclusions

In six consecutive seasons it has been possible to gather

basic information about BSM on common beans in Niassa and

G. Davies222

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014

to establish that it is an important annual pest of beans. It has

been possible to utilize this information to suggest elements of

an integrated control programme for local subsistence farmers in

the context of the local cropping system. Future work will

concentrate on testing these recommendations together with

farmers in their fields to evaluate better their impact and

feasibility.

References

ABATE, T., 1991. Seed dressing insecticides for bean fly [Ophiomyia phaseoli

(Tyron) (Diptera:Agromyzidae)] control in Ethiopia. Tropical Pest Manage-

ment, 37(4), 334 ± 337.

ALLEN, D. J. and SMITHSON, J. B. eds, 1986. Proceedings of the Bean Fly

Workshop Arusha ± Tanzania, 16 ± 28 November 1986. CIAT Pan-African

Workshop Series, No. 1 (Cali, Columbia: CIAT), pp. 29.

ALTIERI, M. A., 1993. Designing and improving pest management systems for

subsistence farmers. In M. A. Altieri (ed) Crop Protection Strategies for

Subsistence Farmers (London: Intermediate Technology Publications),

pp. 21 ± 43.

AMPOFO, J. K. O., 1993. Host plant resistance and cultural strategies for bean

stem maggot management. In Ampofo J. K. O. (ed) Second Meeting of the

Pan-Africa Working Group on Bean Entomology, Harare, Zimbabwe, 19 ±

22 September 1993. CIAT African Workshop Series, No. 25 (Cali,

Columbia: CIAT), pp. 4 ± 12.

AUTRIQUE, A., 1989. Bean pests in Burundi: their status and prospects for

control. In J. K. O. Ampofo (ed) Proceedings of the First Meeting of the

Pan-African Group on Bean Entomology, Nairobi, Kenya, 6 ± 9 August

1989. CIAT African Workshop Series, No. 11 (Cali, Columbia: CIAT),

pp. 1 ± 9.

GONZALES FRANCY, V., 1986. The bean fly, Ophiomyia phaseoli (Tyron)

(Diptera:Agromyzidae). Phaseolus, Beans Newsletter for Eastern Africa, 5,

19 ± 35.

GREATHEAD, D. J., 1968. A study in East Africa of the bean flies

(Dipt.:Agromyzidae) affecting Phaseolus vulgaris and of their natural

enemies, with a description of a new species Melanagromyza Hend.

Bulletin of Entomological Research, 59, 541 ± 561.

HEEMSKERK, W., AMANE, M., REIS, J. and FABIAÄ O, A., 1988. Resultados da

investigacaÄ o do feijaÄ o vulgar 82 ± 87. Phaseolus vulgaris. Documento do

Campo No. 1. Projecto UNDP/FAO/MOZ/86/009. (Maputo, Mozambique:

Instituto Nacional de InvestigacaÄ o Agrono mica (INIA)). pp. 122.

KAREL, A. K. and AUTRIQUE, A., 1989. Insects and other pests in Africa. In

Schwartz H. F. and Pastor-Corrales M. A. (eds) Bean Production Problems

in the Tropics, 2nd edition (Cali, Columbia: CIAT), pp. 455 ± 504.

LAYS, J. F. and AUTRIQUE, A., 1987. La Mouche du Haricot. Fiche Technique

No. 008, (Bujumbura, Burundi: Institut des Sciences Agronomiques du

Burundi), pp. 19.

MACKAY, K. T., ADALLA, C. B. and ROLA, A., 1993. Steps toward an alternate

and safe pest management system for small farmers in the Philippines. In

Altieri M. A. (ed) Crop Protection Strategies for Subsistence Farmers

(London: Intermediate Technology Publications), pp. 21 ± 44.

OREE, A., SLUMPA, S. and AMPOFO, J. K. O., 1990. Effect of environment

and location on the species composition and populations of beanfly

(Ophiomyia spp: Diptera, Agromyzidae) in Tanzania. In Smithson J. B. (ed)

Second Regional Workshop on Bean Research in Eastern Africa. CIAT

African Workshop Series No. 7 (Cali, Colombia: CIAT), pp. 220 ± 226.

SITHANANTHUM, S. and SOHATI, P. H., 1989. Bioecology and host plant

resistance against beanfly in Zambia. In Smithson J. B. (ed) Proceedings

of the First SADDC Regional Bean Research Workshop, Mbabane,

Swaziland, 4 ± 7 October 1989. CIAT African Workshop Series No. 6 (Cali,

Colombia: CIAT), pp. 168 ± 175.

TALEKAR, N. S. and CHEN, D. S., 1985. The beanfly pest complex of tropical

soybean. In Soybeans in Tropical and Subtropical Cropping Systems

(Shanhua, Taiwan: Asian Vegetable Research and Development Centre),

pp. 257 ± 271.

TAYLOR, C. E., 1958. The bean stem maggot. The Rhodesia Agricultural

Journal, 55, 634 ± 636.

TENGECHO, B., COULSON, C. L. and D’SOUZA, H. A., 1988. Distribution and

the effect of bean flies, Ophiomyia phaseoli and O. spencerella , on beans

at Kabete, Kenya. Insect Science and its Application, 9(4), 505 ± 508.

TRUTMANN, P., PAUL, K. B. and CISHABAYO, D., 1992. Seed treatments

increase yield of farmer varietal field bean mixtures in the central African

highlands through multiple disease and beanfly control. Crop Protection,

11, 458 ± 464.

Pest status and ecology of bean stem maggot 223

Dow

nloa

ded

by [

Uni

vers

ity o

f N

orth

Car

olin

a] a

t 12:

46 1

1 N

ovem

ber

2014