biological control of the cassava mealybug, phenacoccus manihoti (hom., pseudococcidae) by...

Agriculture, Ecosystems and Environment, 32 (1990) 39-55 39 Elsevier Science Publishers B.V., Amsterdam

Biological control of the cassava mealybug, Phenacoccus manihoti (Hom., Pseudococcidae) by Epidinocarsis lopezi (Hym., Encyrtidae) in West Africa, as influenced by climate and soil

P. N e u e n s c h w a n d e r l, W . N . O . H a m m o n d ~, O. A j u o n u ~, A. G a d o m, N. E c h e n d u 2, A,H. B o k o n o n - G a n t a 3, R. A l l o m a s s o l

a n d I. O k o n m

International Institute of Tropical Agriculture, Biological Control Programme, B.P. 080932 Cotonou (B~nin)

2National Root Crop Research Institute, Umudike, Umuahia (Nigeria) 3Service de la Protection des V~g~taux, Direction de l'Agriculture, B.P. 58, Porto-Novo (B~nin)

(Accepted for publication 31 January 1990 )

ABSTRACT

Neuenschwander, P., Hammond, W.N.O., Ajuonu, O., Gado, A., Echendu, N., Bokonon-Ganta, A.H., Allomasso, R. and Okon, I., 1990. Biological control of the cassava mealybug Phenacoccus manihoti (Horn., Pseudococcidae) by Epidinocarsis Iopezi (Hym., Encyrtidae) in West Africa, as influenced by climate and soil. Agric. Ecosystems Environ., 32: 39-55.

Population data concerning the cassava mealybug (CM) Phenacoccus manihoti Matile-Ferrero, the introduced parasitoid Epidinocarsis lopezi (De Santis), and indigenous antagonists were collected, together with ecological and plant growth variables, during a survey of 414 fields covering all ecological zones of Nigeria and Benin, for evaluation in multiple regression analyses. The choice of fields was unbiased, and insect populations were estimated from large random samples. Seven years after the first release of E. lopezi, the entire area, with the exception of an isolated CM population near Lake Chad, had been colonized by the parasitoid. Within the area of distribution ofE. lopezi, average CM populations were very low (1.6 CM per shoot tip), highest densities being found in the forest transition zone. The mean tip damage score on a scale from 1 to 5 was only 1.2. Only 3.2% of all tips were strongly stunted, the same percentage had more than 10 CM, and no tip had over 1000 CM. However, significant tip damage persisted on the 4.8% of fields with unmulched, sandy soils in the forest zone. In these fields, 3.3 times fewer CM were needed to cause heavy stunting than on less stressed plants on soils with mulch, or clay, or less rain. This deleterious effect of leaching and lack of crop rotation was alleviated completely in the fields which had a small amount of mulch. Thus, agronomic factors, mediated through the condition of the plant, influenced biological control.

0167-8809/90/$03.50 © 1990 - - Elsevier Science Publishers B.V.

40 p. NEUENSCHWANDER ET AL.

I N T R O D U C T I O N

In the early 1970s, the cassava mealybug (CM), Phenacoccus manihoti Matile-Ferrero, was accidentally introduced from South America to Africa where it became the major pest of cassava (Matile-Ferrero, 1977; Herren, 1981; Fabres and Boussienguet, 1981; Nwanze, 1982; Herren and Lema, 1983). In a large scale biological control project against this pest, undertaken by the International Institute of Tropical Agriculture (IITA) in collaboration with several international agencies (Herren, 1987 ), the solitary, host specific parasitoid Epidinocarsis lopezi (De Santis) was imported from South Amer- ica and first released in Nigeria in 1981 (Herren and Lema, 1982). From seven release areas in the southern part of Nigeria (Herren et al., 1987), E. lopezi spread through Benin and all of Nigeria into Niger (G. Doga, personal communication, 1987). By 1990 it has been successfully established in 24 countries of the African cassava belt and had spread over an area of more than 12.7 million km 2 (Herren et al., 1987; Neuenschwander and Herren, 1988, personal communication, 1990).

Regular monitoring in two areas near Ibadan and Abeokuta from 1981 to 1988 showed that CM populations declined after the releases ofE. lopezi, and remained low (Hammond and Neuenschwander, 1990). Four surveys in 1983 and 1984, covering all of south-western Nigeria, demonstrated that E. lopezi prevented CM outbreaks in most fields (Neuenschwander and Hammond, 1988 ) and its efficiency was confirmed in exclusion experiments (Neuensch- wander et al., 1986 ). A computer simulation model for the growth of cassava (Gutierrez et al., 1988a,b) predicted that E. lopezi is capable of preventing tuber yield losses, and the impact of the native coccinellids (Neuenschwander et al., 1987) in suppressing CM populations was judged to be small. These predictions were confirmed by yield and insect population data from a wide geographical range in southern Ghana and C6te d'Ivoire in 1986 (Neuen- schwander et al., 1989).

These surveys that showed a high level of biological control had been done on systematically chosen fields without selecting for a particular CM population level. Persistent reports, albeit from small scale field trials or local obser- vations, of high CM populations particularly in Congo (N6non and Fabres, 1988; B. Le Rii, Y. Iziquel, A. Biassangama and A. Kiyindou, personal communication, 1988) lead, however, to the conclusion that biological control by E. lopezi was not satisfactory under all conditions. Because parasitoids of pests with a wide range often are efficient only in some ecological niches and inef- ficient in others (DeBach et al., 1971 ), a wider coverage was dearly necessary.

The present survey was therefore made across all ecological and edaphic zones of Nigeria and Benin at the end of the dry season, when CM populations are highest, in order to specify under which conditions E. lopezi gave satisfactory control.

CLIMATE AND SOIL EFFECTS ON BIOCONTROL OF CASSAVA MEALYBUG 41

MATERIALS AND METHODS

Figure 1 shows the route o f a survey covering all regions of Nigeria and the Republ ic of Benin conducted by two teams from 12 February to 2 March 1988. As in previous surveys (Neuenschwander and H a m m o n d , 1988; Neuenschwander et al., 1989), fields were selected without bias, so that the results are representat ive of large areas and comparable between surveys. Groups of cassava fields were chosen for sampling every 50 km. Each group consisted o f three cassava fields as close as possible to each other, but occa- sionally only one or two fields could be found within the next 10 km. A few fields that had been abandoned by farmers and were completely overgrown with weeds were excluded.

Fields were categorized as detailed in Neuenschwander et al. ( 1989 ) in order to use the values as independent (X) and dependent (Y) variables, with the corresponding subscripted numbers, in multiple regression analyses. Field

, \ @

I

/ BENIN i "'! "~... f j / J+

"-.-,t t / F ', \ r<." , iS . ~ . / ~ i . ,.4 +

Fig. 1. Map of survey in Nigeria and Benin in February-March 1988 covering 143 locations. Rain forest and forest transition zones shaded; squares = large towns; dots = mealybug and Epi- dinocarsis lopezi recovered; circled dots (both in Anambra State) = mealybug at exceptionally high population densities and E. lopezi present; small circles = mealybug only, at low population densities; large circle (near Lake Chad ) = mealybug only, at high population density; crosses = no mealybug).

42 P. NEUENSCHWANDER ET AL.

variables included: (1) the ecological zones from the coast to the interior (rain forest, forest transition zone, Guinea savannah, Sudan savannah, Sahel savannah); (2) soil type ( 1 -- sand, 2 = sandy loam-silt, 3 = sandy loam with gravel, 4 = clay, 5 = clay with gravel); (3) organic matter on the soil surface ( 1 = thick layer of mulch, 2 = little mulch, 3 = soil surface exposed); (4) wee- diness ( l= l i t t l e , 2=med ium, 3=modera te) ; (5) planting density (expressed as mean distance between living plants, in cm); (6) cultivar (farmers', Ministry of Agriculture, or IITA cultivars); (7) crop age in months.

Cassava growth was described as means from l 0 randomly selected plants (Neuenschwander and Hammond, 1988 ), on which the numbers of branching levels (8), growing tips (9), and leaves (10) were assessed. Mean CM damage and CM populations were estimated by counting on one terminal shoot of each of these selected plants the number of second and third instars (11), the number of fourth instars (12), and by estimating the number of first instar CM (13). On the same shoot tips, the mean number of mummies ( = parasitized, hardened CM ) (14), coccinellids of all stages (15 ), and ants (16) were noted. The severity of an earlier CM attack, when the plants were still young, was estimated by the mean percentage stunted nodes on the first branching level (17).

In addition to these 10 shoot tips which were investigated in detail, 50 tips were scored in situ, i.e. without breaking them (Neuenschwander et al., 1989 ). The mean of the log numbers of settled CM, i.e. first to fourth instars, (18) was estimated as follows: total CM numbers on each tip were assigned to one of five categories: 0; 1-9; 10-99; 100-999; >t 1000. The log(x+ l ) transformed upper limits of each category are 0, 1, 2, 3, 4, and the mean numbers in each category are 0, 0.5, 1.5, 2.5, 3.5, respectively. The means per 50 tips were calculated from the transformed data. The same tips were also scored according to the tip damage scale (19) described by K.F. Nwanze (PRONAM, 1978 ): 1 = healthy tip, 2 = curling of leaf margins, 3 = slight stunting, 4 = heavy stunting, 5 = defoliation. Because the number of predators and parasitoids could not be counted under the conditions of the survey, the proportion of shoot tips carrying living parasitoids, hyperparasitoids, or mummies containing them (20), predators (21), and ants (22) was used as a surrogate for their numbers. This number increases as the absolute number of organisms increases (Wilson and Room, 1983; Schulthess et al., 1989 ). Damage by the variegated grasshopper Zonocerus variegatus L. (23) and the cassava green mite Mononychellus tanajoa (Bondar) (24) was assessed ( 1 = n o damage, 2 to 4 = light to heavy damage) in the field.

Finally, 10 infested shoot tips per group of fields were collected and stored in a paper bag for emergence of the parasitoids, hyperparasitoids, and predators (Neuenschwander and Hammond, 1988). The total number of mummies (25) and the number of hyperparasitoids (26) in each paper bag were determined.


For the different variables describing CM populations ( ]"1 to Yj), separate multiple regression analyses using a linear model with environmental, insect, and plant factors (X~ to Xj) and some of their interactions were done as described in Neuenschwander et al. ( 1989 ), avoiding obvious self-correlations. Only X-variables having a significant slope b (at P<0.05 ) with one of the Y variables were retained. Some variables were reclassified into fewer categories, and some variables were not used in the final analysis. Different methods for estimating CM population densities (variables 11, 12, and 18) were compared. For all regressions, the t-value of b, with an asterisk if significant at P < 0.05, and the explained variance R 2, a re shown.

RESULTS

The survey covered 143 locations, which were at least 50 km apart from each other (Fig. 1 ). A total of 102 locations (71.3% ) had CM as judged from the 60 tips inspected in each field. In 94.8% of all fields in the forest zones (rain forest and forest transition zone), at least one CM was found. Distri- bution of the CM in the savannah zones was more irregular and mainly con- fined to the Guinea savannah. In the forest, 84.5% of all fields, or 89.1% of all CM infested fields, had E. lopezi (Table 1 ). In the savannah, E. lopezi was found in 56.5% of all infested fields which were within its distribution. One isolated field in Lake Chad had a high CM population without E. lopezi. Be- cause it was hundreds of kilometres from the nearest CM infestation, which was much smaller, it was considered to be outside the distribution of the exotic parasitoid. Indigenous coccinellids were found much less frequently than

TABLE 1

Percentage of locations in Nigeria and Benin having cassava mealybug, Epidinocarsis lopezi, and coccinellids. Based on 50 cassava shoot tips observed in situ and 10 dissected tips in each field, with one to three fields per location, February-March 1988

Ecological zone Number of locations ( = ioo%)

Percentage of locations having:

Cassava E. lopezi Coccinellids mealybug ~

Savannah 2 85 55.3 30.6 20.04 Forest 3 58 94.8 84.5 24.1

qncluding two locations where the mealybug was found only in the dissected samples. All locations, except the only field in the Sahei savannah, were within the range of distribution of E. lopezi. Distance between locations: 1> 50 km. 2Consisting of Guinea, Sudan, and Sahel savannah. SConsisting of rain forest and forest transition zone. 4Including two locations where coccinellids were found though mealybugs were lacking.


E. lopezi. In two locations in the Sudan savannah, coccinellids were found on cassava in the absence of CM.

CM population densities and shoot tip damage scores were low (Table 2) , the exception being the field sampled near Lake Chad in the Sahel savannah. Highest means were found in the transition zone. On individual tips, the following CM numbers and tip damage scores (Table 3) were recorded: 90.2% had no damage at all or showed only slight curling of some leaves, i.e. scores 1 and 2. Some 96.8% of all shoot tips had less than 10 CM. Only 3.2% showed heavy damage, i.e. scores 4 and 5, and 0.4% had more than 100 CM. No terminal shoot was found having more than 1000 CM. At lower levels of tip

TABLE2

Mean mealybug population density per shoot tip together with tip damage scores, in different ecological zones. Fifty tips per field, from 414 fields in Nigeria and Benin, in February-March 1988

Ecological zone Number Number of CM Tip damage of fields

per tip 1,3 +_ SE score 2"3 + SE

Rain forest 104 0.12 a 0.014 1.27 a 0.030 Forest transition zone 72 0.14 a 0.020 1.50 b 0.085 Guinea savannah 174 0.07 b 0.011 1.14 ¢ 0.023 Sudan savannah 63 0.01 c 0.003 1.02 d 0.008 Sahel savannah 1 0.46 d 1.96 ab

IAs log(x+ 1 ). 2Scoring scale from 1 to 5 ( 1 = no damage, 5 = total defoliation ). 3Means _+ SE; means followed by the same letter do not differ significantly (P< 0.05 ).

TABLE3

Cassava mealybug infestation and tip damage score in Nigeria and Benin, in February-March 1988. Percentage cassava tips falling into the different categories of mealybug numbers (log- estimates) and damage scores; 50 tips from each of 413 fields within the area of distribution of Epidinocarsis lopezi. In parentheses: number of fields with tips in this category

Damage score

1 2 3 4 5 sum

NoCM 80.8 (411) 1.6 (91) 1.0 (46) 0.7 (17) 0.1 (8) 84.2 I - 9 C M 1.2 (55) 6.3 (190) 3.8 (133) 1.2 (57) 0.1 (2) 12.6 10-99CM 0.0 (4) 0.3 (23) 1.7 (97) 0 .8(53) 0 .0(5) 2.8 100-999 CM 0.1 (9) 0.3 (23) 0.0 (3) 0.4 > 1000 CM 0

Sum 82.0 8.2 6.6 3.0 0.2 100.0


damage, CM populations increased with damage scores, but most of the heav- ily damaged tips (score 5 ) had no longer any living CM. If only fields from the 100 infested locations were considered, still 86.2% of all shoot tips were virtually undamaged (scores 1 or 2).

Some badly infested shoot tips were found in every ecological zone, but heavy infestations were clearly clustered in Anambra state (Fig. 1 ). In order to unders tand the condit ions leading to high CM infestations, multiple regression analyses involving plant, insect, and environmental factors were per- formed. Four independent factors with significant slopes were retained (Ta- ble 4). When mealybug infestations were characterized by the tip damage score (Y19) these variables accounted for 60% of the variance. Ecological zone (X1) and a combinat ion of factors described by the soil s t ructure-mulching interaction (X2.~) influenced the tip damage score significantly. Predators, almost exclusively coccinellids, (X2~) and, to a lesser degree, E. lopezi (X2o) were closely associated with CM damage. On average, 1.8% of all tips ( 11.4% of all infested tips) had a m u m m y (or adult E. lopezi), while 0.8% had a coccinellid larva, pupa, or adult. The mean damage score was only 1.2 on a scale from 1 to 5.

When l o g ( x + 1 ) estimates o f the population density (Yz8), based on 50 tips per field, were taken as the dependent variable (Table 5 ), there was little difference in the results. Again, ecological zone was an important factor, but the soi l -mulching interaction became less important and E. lopezi was more closely linked to CM numbers than the coccinellids. The explained variance was 45%.

A comparison of the methodologies for estimating CM populations, namely l o g ( x + 1 ) estimates on 50 tips versus counts on l0 tips, gave the following results: when CM counts (Xzz+ ze), excluding the est imated number o f first instars, were used as measure of the population density (Table 5 ), ecological

TABLE 4

Multiple regression for predicting mealybug damage score. Survey data of 413 fields in Nigeria and Benin within the area of distribution of Epidinocarsis lopezi, February-March 1988

Variable Regression statistics Mean + SE

b, t

Dependent variable YI9 Damage score 1.218 0.021

Independent variables X~ Ecological zone - 0.061 4.66* 2.482 0.051 X2,3 Soil X organic matter 0.070 2.65* 0.232 0.028 Xez Predators 0.077 16.68* 0.801 0.157 X2o E. lopezi 0.024 6.77* 1.753 0.206

Intercept= 1.249; x/MSE=0.266 with 408 degrees of freedom; explained variance R2=0.60; bj = partial regression coefficient; t = t-statistic; SE = standard error; * = significant at P < 0.05.

46 p. NEUENSCHWANDER ET AL.

TABLE 5

Multiple regression for predicting mealybug (CM) densities expressed either as estimated values using a log-scale by non-destructive sampling or as counted numbers from dissected tips, transformed to l og (x+ l ) or untransformed. Survey data of 413 fields in Nigeria and Benin within the distribution of Epidinocarsis lopezi. February-March 1988

Independent variable Regression statistics for

YI 1,12 = CM counts

untransformed t l og (x+ 1 )2

Yls = CM estimate

l og (x+ 1 )3

bj t bj t bj t

XI Ecological zone - 0 . 1 9 6 1.54 - 0 . 0 5 8 4.89* - 0 . 0 1 8 3.45* X2,3 Soil × organic matter -0 .431 1.67 - 0 . 0 1 8 0.74 - 0 . 0 0 2 0.25 X21 Predators 0.130 2.91 * 0.016 3.77* 0.013 7.29* )(20 E. lopezi 0.259 7.63* 0.028 8.99* 0.016 11.84"

Intercept 1.158 0.271 0.087 x/MSE 2.592 0.241 0.106 Explained variance R 2 0.19 0.31 0.45

1Mean counts per shoot tip, of second to fourth instar mealybugs, from 10 dissected tips per field. Mean_+ SE= 1.131 +0.141. 2Same counts, l og (x+ l ) transformed: Mean _+ SE = 0.185 + 0.014. 3Means per tip of log ( x + l ) estimates of mealybug numbers, from 50 tips observed in each field. Mean _+ SE = 0.081 +_ 0.007. bj= partial regression coefficient; t= t-statistics; * = significant at P < 0.05.

zone remained a significant factor only if the means of these counts were log (x+ 1 ) transformed. Beneficials, primarily E . l o p e z i , were the most closely associated variables, and soil variables were less important. The explained variance was 31% with transformed data and 19% using untransformed data. Average density, calculated from untransformed data, was only 1.1 CM per tip, thereby confirming the relative scarcity of mealybugs.

If first instars (X13) were included in the counts, the mean number of CM per tip was 1.6. The multiple regressions were very similar to those with second to fourth instars only, but explained variances were lower, namely 29 and 14%, with l og (x+ 1 ) transformed and untransformed counts, respectively.

In order to calibrate the procedure using log estimates, mealybug counts from the 659 tips of the 10-tip samples containing first to fourth instar CM were assigned to the categories used for log-estimates, i.e. 0, 1-9, 10-99, 100- 999 CM. When logs of actual counts (X~og 11 + 12 + 13 ) from individual tips were plotted against the calculated log values (Ylog ~1+ 12+ 13) from the same tips, the resulting straight line had tile formula: Ylog 11+ 12+ 13=0.067 + 0.929 Xlog 11+12+13 (r2=71%). This is very similar to the formula Y = 0 + 1.00 X describing identical results between the two approaches for estimating CM pop-


ulations. Fifty-tip samples underestimated CM numbers, as assessed from counts, by only 7.1%. When first instars were excluded, the explained variance was 71% and the slope was 0.906.

It is concluded that the two dependent variables based on 50 tips per field, i.e. damage scores (Y~9) and log-estimates of the CM population (Yls), gave higher explained variances than accurate counts of CM on ten tips per field (YH ÷ ~2). Although the damage scores were highly influenced by soil conditions, CM counts were less affected. Predators were more closely associated with stunted cassava tips, whereas E. lopezi frequency was better linked with actual CM numbers. Plant age (Xz) was tested as an additional variable but, surprisingly, did not contribute significantly to the explained variance. Simi- larly, weeds (X4), bushiness of the plant as expressed by the total number of tips (X9) or leaves (X~o) or leaves per tip, and ants (X22) did not give significant contributions. Cassava cultivar (Xr) was not used as a variable, because the vigorous, branching cassava cultivars from the Ministry of Agriculture and/or IITA were encountered in only 13.8% of all fields, clustered mainly in Oyo and Bendel states of Nigeria.

The influence of soil and mulching on the CM tip damage score (Y~9) was further investigated (Table 6 ). Under different combinations of soils and soil covers in the two main ecological zones, tip damage scores were very similar and close to l, i.e. no damage. The only exception concerned fields that were in the forest zone, on sandy soils without mulch (4.8% of all fields sampled). Their mean damage score was roughly double that in the remaining fields. When tip damage scores of neighbouring fields in the forest zone with the same sandy soil, some with and some without mulch, were compared (Table 7 ) the strong effect of mulching was confirmed in a quasi-experimental setting.

As expected, mean tip damage score (Y19) increased with the mean CM infestation per tip (X~8) expressed as log(x+ 1 ) 'Y t9 = 1.024+2.361 X~8 (N=413, t=27.47", r2=65%). But, because the soil-mulch interaction in the multiple regression analyses was more important when damage score was

TABLE6

Mealybug tip damage scores in 413 fields with different ecological and soil conditions within the distribution ofEpidinocarsis lopezi in Nigeria and Benin, February-March 1988

Ecological zone Sand Loam/clay

Medium- Low Medium- Low high OM OM high OM OM

Forest 1.25 (25) 2.19 (20) 1.24 (113) 1.37 (18) Savannah 1.23 (13) 1.34 (9) 1.13 (134) 1.02 (81)

x/MSE = 0.345 with 405 degrees of freedom; in parentheses: number of fields in each category; OM =organic matter.


TABLE 7

Mealybug population density and tip damage scores in neighbouring fields in the forest zones on sandy soil, some fields being mulched and others not. Six localities with a total of 17 fields, 11 with versus six without mulching. Nigeria and Benin, February-March 1988

With mulch Without mulch t-value

Mean CM per tip, as log(x+ 1 ) 0.04 0.36 3.16* Mean CM damage score t 1.29 2.06 5.59* Mean percentage bunch top 2 4.8 31.4 6.28*

11 = no damage to 5 = total defoliation. 2Total of tips with damage scores 3, 4, and 5. Calculated as arc sinx/p.

1.2-

CL -.~ 1.0-

~. 0.8-

0.6-

0.4-

~ O.2- o

0.0 2 3 4

tip damage score 5

Fig. 2. Mean number of mealybugs per tip +_ SE, expressed as log(x+ 1 ), on cassava shoot tips with different damage scores ( 1 = no damage, 5 = total defoliation), on plants growing on sandy unmuiched soils in the forest (white) and those under all other conditions (stippled). From 50 tips of each of413 fields in Nigeria and Benin, February-March 1988.

used as a dependent variable than with CM population estimates, the degree of stunting and mealybug numbers did not correspond closely. Figure 2 pre- sents mean mealybug numbers on individual tips sorted according to their degree of stunting, separately for the worst combinat ion of conditions, i.e. sandy unmulched soils in the rain forest, and for all other soils. Up to stunting score 2, the differences between the two growth conditions were small. But on shoot tips with scores 3 and 4, significantly more CM were found where the plant grew better than on those on leached out, unmulched sandy soils (tscore 3 = 17.39", N = 1359 tips; tscore 4=29.76", N = 6 1 2 tips). Thus, 3.3 times less mealybugs were needed to provoke stunting score 4 on plants growing under bad conditions than on those on other soils.

When stunting on the first branching level (]I17), i.e. early in the growth of the cassava plant, was considered as dependent variable (Table 8), the explained variance was only 15%. CM population density on the tips (XI8) was most closely associated with early damage. Stunting increased with crop age (X7), presumably because older plants had been planted at the beginning of


TABLE 8

Multiple regression analysis for predicting stunting on the first branching level of cassava. Sur- vey data of 413 fields in Nigeria and Benin, February-March 1988

Variable Regression statistics

bj t

Dependent variable Y: 7 Stunted nodes1 Independent variables X:8 Mealybugs in log(x+ 1 ) 14.792

X2 Soil type 2 I. 140 X7 Crop age 3 0.327

6.80* 4.17" 3.76*

'Calculated as arc sinx/p. Mean _+ SE = 3.435 _+ 0.330. 2Mean _+ SE = 2.596 _+ 0.055. 3Mean _+ SE = 8.499 _+ 0.174; max imum 24 months, m i n i m u m 2 months. by = partial regression coefficient; t = t-statistic; * = significant at P < 0.05.

the previous rainy season, when CM populations were still relatively high. Similarly, stunting was greater on the better soils where planting had been earlier. All other factors that could conceivably cause or influence stunting, including the cassava green mite (X24), contributed too little to the explained variance to be included.

Finally, E. lopezi population density, as expressed by the percentage of tips having at least one mummy (I:2o), was taken as the dependent variable in a multiple regression analysis (Table 9); it proved to be significantly affected by only a few factors. As already shown, E. lopezi presence became progres- sively lower towards the north which was reflected in the significant contri- bution of the variable ecological zone (Xl) when the whole data set was ana- lysed. By far the most important variable was the host population density (X~s). The significant soil-mulch interaction was confirmed by an evaluation of individual tips, among which those with E. lopezi were consistently more frequent on unmulched sandy soils, i.e. under conditions where CM was more numerous. Predator frequency (X21) was negatively correlated to E. lopezi frequency, but only if fields without the parasitoid were excluded from the analysis, e.g. fields in the north, among them those where coccinellids occurred even in the absence of the CM. Inclusion of plant growth, described by age of the plants (Xz), abundance of foliage (Xw) or tips per plant (Xg), and of antagonists or competitors, like hyperparasitoids (:(26) or ants (X22), did not give significant results.

The linear regression of mean E. lopezi frequency (1:2o) on CM density (X~s), over all 122 fields having E. lopezi, was as follows: }'2o = 2.467 + 18.662 X:8 ( t - 7.41 *, r 2 = 31% ). By comparison, the percentage of shoot tips having predators (Y2:), in the 54 fields having them, increased with the CM popu-


TABLE 9

Multiple regression analysis for predicting percentage of shoot tips having Epidinocarsis lopezi. Survey data of 413 fields in Nigeria and Benin, among which 122 had E. lopezi, in February- March 1988

Independent variable Regression statistics concerning:

all 4 i 3 fields 122 fields with E. lopezi

bj t bj t

X~ Ecological zone - 0.321 1.99" - 0.126 0.24 Xz~ Soil X organic matter 1.561 4.95* 1.936 2.97* Xjs Mealybugs in log ( x + 1 ) 15.618 11.84" 18.488 6.84* X2~ Predators -0 .042 0.71 -0 .192 2.04*

Intercept 0.951 2.263 x/MSE (degrees of freedom) 3.258 (408) 4.763 (117) Explained variance R 2 0.40 0.37

bj = partial regression coefficient; t = t-statistic; * = significant at P < 0.05.

lation density less than was the case with E. lopezi, and the explained variance remained very low: Y21 = 3.089 + 10.682 XI8 (t = 2.18", r 2 = 8 % ) .

The influence of the plant host on E. lopezi, independent of the reaction to host density, was evaluated as follows: for all fields with E. lopezi, the ratio of Y2o/Xls was compared with the mean number of leaves per tip (XIo/Xg), which gave a significant regression: Y2o/Xls=25.074+l.934 XIo/X9 ( t=2.95", r2=7%).

Hyperparasitoids could only be evaluated from the rather limited emergence data. The number of mummies yielding hyperparasitoids in each paper bag (I"26) increased sharply with the total number of mummies (X25): I126=0.474+0.153 )(25+0.00949 )(252 ( 8 = 8 6 , r2= 59%, tx~ =2.48*).

DISCUSSION

Epidinocarsis lopezi had previously been recovered in some northern states of Nigeria (T.A. Akinlosotu, E.D. Umeh and W.N.O. Hammond, personal communication, 1986; J. Noyes and P. Neuenschwander, personal communication, 1987 ) where it was lacking in the present survey. The Lake Chad basin therefore seems to be the only region in Nigeria to which E. lopezi has not spread, presumably because the surrounding areas have very little cassava.

After the introduction of E. lopezi, CM population levels dropped drasti- cally in south-western Nigeria (Hammond and Neuenschwander, 1990). In the present survey, CM populations over the wide range of ecological condi-


tions where E. lopezi had meanwhile spread were lower than reported for south-western Nigeria in 1984 (Neuenschwander and Hammond, 1988 ).

In view of previous criticism concerning the methods for assessing CM population densities (G.K.C. Nyirenda, personal communication, 1986, 1987, 1988 ), the different methods were compared. The quick count method de- rived from 50 tips clearly gave the more satisfactory results, i.e. lower variances, than the presumably more precise counting of CM on I 0 tips, which took about the same effort.

In Ghana and Crte d'Ivoire, E. lopezi's spread was associated with a de- crease in crop loss attributable to the CM (Neuenschwander et al., 1989). In the present survey, tuber yields were not measured and the impact ofE. lopezi can only be judged from stunting at the level of the terminal tips and the lower part of the main stem. Overall, this damage was as small as in south-eastern Ghana in 1986 (Neuenschwander et al., 1989) and lower than in south-western Nigeria in 1984 (Neuenschwander and Hammond, 1988 ). It can be concluded that biological control by E. lopezi in Nigeria and Benin is successful in preventing stunting of cassava plants by CM in most fields.

Persistent reports about considerable CM damage were, however, received from south-eastern Nigeria (E.D. Umeh, personal communication, 1988), Sierra Leone (L. Sesay, personal communication, 1987), Togo (H. Fischer, personal communication, 1987), Malawi (G.K.C. Nyirenda, personal communication, 1988 ), and - particularly - Congo (Nrnon and Fabres, 1988; B. Le Rii, Y. Iziquel, A. Biassangama and A. Kiyindou, personal communication, 1988). All reports came from local areas from fields often chosen for their high CM population. The present survey confirms some of these obser- vations and places them into a broader context, both geographically and ecologically.

Multiple regression analyses of field means demonstrated that, in the area of distribution of E. lopezi, CM populations were highest in the transition zone and significantly lower in the savannah zones and that soil and organic matter had a significant influence. It had previously been noted that CM was concentrated on cassava grown on marginal soils (Nwanze et al., 1979), though B. Le Rii, Y. Iziquel, A. Biassangama and A. Kiyindou (personal communication, 1988) found higher infestations on their better plots in Congo. In the present survey, sandy soils in the forest region predisposed the plant toward an increased CM attack. In the same area under similar rain patterns, however, soils containing clay retained enough water for adequate cassava growth. Conversely, sandy soils in the savannah, where leaching is less pro- nounced, yielded satisfactory cassava with low CM induced tip damage.

The leached out sandy soils in Anambra state were made even poorer because of the particularly strong agricultural pressure on the land, often leading to cultivation with cassava for many years. Similarly, in southern Togo, where CM damage is evident on cassava on sandy soils, fields have been under con- tinuous cassava cultivation for up to 20 years (H. Fischer, personal commu-

5 2 P. NEUENSCHWANDER ET AL.

nication, 1987 ). Though soils of tropical Africa are inherently infertile and processes of degradation are intense (Okigbo, 1980), it is only on the limited area with exceedingly poor soils, which usually prohibit any other agricultural activity, that the CM was severely damaging. In 1988, this niche comprised 4.8% of all cassava fields representative of Nigeria and Benin, but it might increase in the future with increasing pressure on the land, particularly near urban centres.

In the study area, crop stress was alleviated by an astonishingly small amount of mulch, sometimes consisting of not more than the dropped cassava leaves and some cut weeds. Mulch plays a role in water management (Lal, 1978; Okigbo and Lal, 1979; Lal, 1980) and recycling of nutrients (Vitousek, 1980), but its effects on pest management through drought stressed plants (Holtzer et al., 1988) or changes in plant nutrition (Dale, 1988) are controversial. Drought stress has been shown to improve the life-table parameters of the CM in the laboratory (Schulthess et al., 1987; Fabres and Le Rii, 1988). In addition, nitrogen availability to cassava, which is lower on unmulched sand, could affect CM. On plants stressed by lack of nitrogen, CM could be fa- voured in two ways: ( 1 ) Remobilization of amino acids from wilting leaves actually increases the nutritional value of the phloem sap where the CM feeds. (2) Reduced nitrogen supply might interfere with the maintenance of chem- ical defences like cyanide and latex by the cassava plant. Future studies into CM-cassava interactions for testing these hypotheses must take into account that cyanide levels are reported to change even during the day and between different parts of the plant, and that they correspond only weakly to the dis- tinction between "sweet" and "bitter" cassava cultivars (Nartey, 1981 ).

A detailed investigation of CM numbers per tip and the resulting tip damage revealed that the close relationship between the two variables was only valid up to damage score 2, i.e. for 90.2% of all tips. Higher stunting scores were caused by much lower numbers of CM on the stressed plants on sandy soils than under other conditions. This result demonstrates the dangers of indiscriminate use of damage scores not supported by population dynamic data, as pointed out previously by Yaninek et al. (1989).

The relationship between populations of parasitoids and insect hosts is more complicated than the simple relationship inherent in the analysis with dependent and independent variables. Such feedback mechanisms between attraction and host reduction can only be understood in population dynamic data with repeated measures in time (Hammond and Neuenschwander, 1990). Although E. lopezi presence in an area clearly lowered host populations in Ghana (Neuenschwander et al., 1989 ), more parasitoids were not linked with less hosts (Tables 4 and 5 ). Table 9 actually shows that more hosts attracted more parasitoids, which in turn attracted more hyperparasitoids. The results are explained by the density dependent behaviour of parasitoids and hyperparasitoids towards their host populations reported in the previous studies.


Coccinellids and ants were observed on cassava sometimes without insect hosts, presumably seeking shelter, searching for hosts, and being sustained by nectar from extrafloral nectaries. The multiple regression analysis showed a weakly significant mutual exclusion between E. lopezi and the indigenous coccineUids. This might be explained, on the one hand, by the preference of coccinellids for bunch tops with few leaves. On the other hand, naked tips are avoided by female E. lopezi, as observed in a glasshouse (Neuenschwander et al., 1984) or quantified in the present survey where leafiness of the plant had a small but significant influence on E. lopezi. Whether this is the same influence by synomones of infested plants on E. lopezi, as shown in the laboratory (Nadel and van Alphen, 1987 ), remains to be seen.

In conclusion, E. lopezi was proven to be effective in the great majority of ecological niches investigated. Where CM damage persisted, other beneficial insects are being introduced and distributed by IITA, following experience with other biological control programmes (DeBach et al., 1971 ). However, the good result with mulching of sandy soils, which needs confirmation, points to a solution by an agronomic technique in conjunction with biological control. It must be recalled, however, that under the same agronomic and edaphic conditions that now allow for good biological control, destructive CM infestations developed before the introduction ofE. lopezi.

ACKNOWLEDGEMENTS

This work was financed by the International Fund for Agricultural Devel- opment, Rome, aid agencies of Switzerland (DCA), Federal Republic of Ger- many (GTZ), Austria, Denmark, The Netherlands, Italy, and Norway. T.A. Akinlosotu (Obafemi Owalowo University, IAR&T Ibadan, Nigeria) and D. Akibo-Betts (IITA) participated as observers in part of the survey.

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