ENTOMOPHAGA42 (4), 1997, 543-557

FIRST OBSERVATIONS ON THE PARASITOIDS ASSOCIATED WITH LEPIDOPTEROUS PESTS OF COTTON IN BURKINA FASO J. C. STREITO(') • S. NIBOUCHE(2) Institut d'Etudes et de Recherches Agricoles, BP 7192, Ouagadougou, Burkina Faso.

A study was conducted in Burkina Faso from 1991 to 1994 on the parasitoids associated with the following lepidopterous pests of cotton: Helicoverpa armigera (Htibner), Earias spp., Diparopsis watersi (Rothschild), Spodoptera littoralis (Boisduval), Syllepte derogata (F.) and Anomis flava (E). Thirty-nine primary parasitoid species and ten secondary parasitoid species were collected. The mean annual parasitism rates were lower than 20%, except for S. derogata pupae (42.9%). Maximum weekly parasitism rates could be high, with 61.5% recorded for S. derogata pupae and 32.9% for H. armigera larvae. The highest parasitism rates were found for Meteorus laphygmarum Brues (Braconidae) on H. armigera, Xanthopimpla aliena Krieger (Ichneumonidae), Brachymeria olethria (Waterston) and B. citrea (Steffan) (Chalcididae) on S. derogata, Aleiodes dedivus (Szdpligeti), Dolichogenidea sp. (Braconidae) and Brachymeria feae Masi on Earias spp., an unidentified Tachinidae on A.flava and Metopius discolor Tosquinet (Ichneumonidae) on S. littoralis. Secondary parasitoids are mainly associated with Apanteles spp. (Braconidae) which parasitize S. derogata larvae. Some species of these secondary parasitoids such as Nesolynx phaeosoma (Waterston), Pedobius amaurocoelus (Waterston) (Eulophidae) and Aphanogmus fijiensis (Ferri~re) (Ceraphronidae) may also attack certain Braconidae or Chalcididae that are primary parasitoids of other lepidopterous pests. KEY-WORDS: parasitoids, cotton, Helicoverpa armigera, Earias, Diparopsis wa-

tersi, Spodoptera littoralis, Syllepte derogata, Anomis flava.

Lepidoptera are the main pests of cotton in Burkina Faso. Six of the species listed on cotton cause significant damage (Nibouche, 1992). Three noctuids attack fruiting parts of the plant: Helicoverpa (= Heliothis) armigera (Htibner), Diparopsis watersi (Rothschild) and Earias spp. There are two Earias species, E. biplaga Walker and E. insulana (Boisduval). Both species are generally simultaneously present in cotton fields, but their larval morphology is very similar and they are rarely distinguished from each other. Three Lepidoptera species mainly attack cotton leaves. These are two Noctuids, Spodoptera littoralis (Boisduval) and Anomis (= Cosmophylla) flava (F.) and Syllepte (= Sylepta) derogata (F.) in the Crambidae family.

(~) Correspondence: Service Regional de la Protection des Vdg6taux, 38 rue Sainte Catherine, 54000Nancy, France. (2) Correspondence: CIRAD, BP 5035, 34032 Montpellier cedex 1, France.

544

J. c. STREITO & S. NIBOUCHE

Lepidoptera are the main cause of production losses, which are estimated to average 43% of potential yield when there is no insecticide protection (Nibouche & Goz6, 1993). The insecticide protection provided today, almost exclusively based on the use of chemical pesticides, poses several problems (cost, potential negative effects on environment, risks of development of insecticide resistance) and need replacement by an integrated pest management strategy. This, among other things, requires knowledge of local entomophagous insects in terms of faunistics and biology. The current study reports the first observations on the parasitoid fauna associated with lepidopterous pests of cotton in Burkina Faso.

MATERIALS AND METHODS Observations were mainly carded out at the INERA (Institut d'Etudes et de Recherches Agricoles) experimental station at Farako-B~. This station is near Bobo-Dioulasso (4020 , W, 11 ~ N) in the cotton growing area, where all fields receive pesticide sprays. It is in the Sudanese climatic area (Sivakumar & Gnoumou, 1987), with a single rainy season from May-June to the end of October. A 0.25 ha cotton plot with no insecticide protection was used for the observations and collection of insects. Parasitoids were obtained by collecting and rearing their hosts in the laboratory. Caterpillars were collected in the field without taking their instar into account. Collection was performed weekly from the end of August to the end of October. All larvae found during the duration of the collection were collected. The number of larvae collected varied mainly according to the pest population level at the time of collection. H. armigera was the most extensively studied species with collection from 1991 to 1994. Few D. watersi larvae were reared because of low population levels in the field and high mortality rates during laboratory rearing. Earias spp. larvae were collected in 1992 and 1994. In 1994, S. littoralis, S. derogata and A.flava larvae were collected regularly. H. armigera, S. littoralis, Earias spp. larvae were reared on artificial diet (Giret & Couilloud, 1986; Giret, unpubl. data) A. flava and S. derogata larvae were reared on cotton leaves and D. watersi larvae on green bolls or cotton buds. To complete the inventory, one-off collections of caterpillars were carded out from 1992 to 1994 in smaliholders' fields (with chemical protection) in different places in the cotton growing area. Only D. watersi eggs were collected regularly from the end of June to the beginning of September 1994. H. armigera and A.flava eggs were collected on some occasions. Eggs were kept in the laboratory until hatching or the emergence of parasitoids. S. derogata and A. flava pupae (located in the leaves of cotton plants) were collected in the same way as larvae during 1994 for A.flava and in 1993 and 1994 for S. derogata. Earias spp. pupae, which are more difficult to observe, were collected only occasionally. H. armigera and D. watersi pupae were collected in the soil in 1993 and 1994. Several Hymenoptera cocoons and mummified caterpillars were collected in the field. Cocoons of Braconidae parasitizing S. derogata were collected weekly in 1993. All insects were reared at ambient temperature, relative humidity and photoperiod. Parasitoids were killed with ethyl acetate and sent to specialists for identification (see acknowledgements). The average annual parasitism rates were calculated by grouping all the insects collected during the year. The maximum weekly parasitism rate was noted for every host-parasitoid pair.

PARASITOIDS OF LEPIDOPTEROUS PESTS OF CO'I'I'ON IN BURKINA FASO

545

RESULTS

TROPHIC INTERACTIONS

A list of the parasitoids identified and their taxonomic status are provided in table 1. Thirty-nine species of primary parasitoids and 10 species of secondary parasitoids were identified. Trophic interactions between species are summarized in figure 1. Among 39 primary parasitoids, 27 species are 'specialists' that parasitize only one host. There was an average number 2.3 host species per non-specialist primary parasitoid species. On the other hand, only two species of secondary parasitoids are specialists (of nine species whose hosts were identified). There was an average of 2.5 hosts per non-specialist secondary parasitoid species. Secondary parasitoids are mainly associated with the Apanteles spp. which attack S. derogata larvae. PARASITOIDS OF HELICOVERPA ARMIGERA

Two Trichogrammatoidea species emerged from H. armigera eggs. The first species was Trichogrammatoidea lutea Girault. The second species had not been described before (Delvare, personal communication) but the small number of specimens collected did not allow description. Few eggs were collected: only 7 out of 65 (10.8%) were parasitized, with an average of 2.3 parasitoids per egg. The average annual larval parasitism rate at Farako-B~ station (table 2) varied from 0 (1991) to 16.1% (1994). The maximum weekly parasitism rate was 32.9%. The most common larval parasitoid was the Braconidae Meteorus laphygmarum Brues, which accounted for 81.1% of parasitoids collected from 1991 to 1994 (table 2). This dominance was almost systematic in one-off collection operations outside Farako-B~. Secondary parasitoids emerged from two M. laphygmarum cocoons. These parasitoids were Aphanogmus fijiensis (Ferri~re) and Nesolynx phaeosoma (Waterston). An atypical parasitoid complex was obtained from a collection of 82 larvae from farmers fields outside Farako-B~ in September 1992, where 20.7% of larvae were parasitized by unidentified nematodes. Fifteen pupae were collected in the soil during the dry season (January 1993 and February to April 1994) and 44 at the end of the rainy season (October 1994). None of them was parasitized. But nevertheless, three Tachinidae species emerged from pupae obtained after the rearing of larvae from one-off collections from farmers fields outside Farako-B~ (table 1). PARASITOIDS OF EARIAS SPP.

In 1992 and 1994, 425 larvae from Farako-B~ were reared. Average annual parasitism rates were similar at approximately 10% (table 3). Maximum rates were also similar in both years at 24.0 and 26.1%. Six parasitoid species emerged from larvae. None of them was dominant. The most common were Aleiodes dedivus (Szrpligeti), M. laphygmarum and Dolichogenidea sp. Only 17 pupae were collected, four of which were parasitized by different parasitoids: Pentaternus striatus (Szrpligeti), Brachymeria feae Masi and B. olethria (Waterston).

546

J. C. STREITO & S. NIBOUCHE

TABLE l

List of parasitoids collected, taxonomic status, host and stage attacked, maximum weekly parasitism rate reported during the study

Parasitoids

Hosts

DIPTERA TACHINIDAE 1 Carcelia sp.

2 Exorista sp. 3 Chetogena sp. 4 Winthemia dasyops Wiedemann 5 sp. 1 6 7 8 9 10

sp. sp. sp. sp.

2 3 4 5

sp. 6

HYMENOPTERA CHALCIDIDAE 11 Brachymeria sp. 12 Brachymeria olethria (Waterston) 13

B. feae Masi

14 B. citrea (Steffan) 15 B. kassalensis (Kirby) 16 Eurytoma syleptae Ferri~re

17 E. braconidis Ferri~re 18

E. lepidopterea Risbec

H. armigera S. littoralis D. watersi H. armigera H. amigera A. flava H. armigera S. littoralis A. flava A. flava A. flava Earias sp. S. littoralis S. littoralis

Stage attacked

larva larva larva larva larva larva larva

larva larva

A. flava S. derogata Earias sp. S. derogata Earias sp. A. flava S. derogata S. derogata A. flava Apanteles spp. Apanteles sagax Camptotypus sp.? S. derogata Apanteles spp. Apanteles sagax A. flava S. derogata

Host-stage from which the parasitoid emerges

Maximum weekly parasitism rate

pupa pupa pupa larva pupa pupa pupa larva pupa pupa, larva larva larva larva pupa

4.6% 3.2% 2.5% 0.6%

(4/87) (1/31) (I/40) (1/160) --1.1% (1/87) 1.4% (I/73) 4.7% (3/64) 3.1% (2/64) 13.3% (2/15) 4.5% (I/22) 9.6% (7/73) 3.6% (1/28)

pupa pupa pupa pupa pupa pupa pupa pupa pupa cocoon cocoon pupa pupa cocoon cocoon pupa pupa

22.2% (4/18) 23.8% (5/21) 5.9% (1/17) 7.4% (2/27) 11.8% (2/17) -25.9% (7/27) 5.5% (3/55) -7.7% (2/26) 17.4% (4/23) --1.6% (1/63) 27.3% (3/11) ---

ENCYRTIDAE 19

Copidosoma floridanum (Ashmead) A. tiara?

20

Nesolynx phaeosoma (Waterston)

larva

larva

EULOPHIDAE

A. sagax Apanteles spp. X. aliena Aleiodes sp. M. laphygmarum S. derogata

21

Pediobius ston)

amaurocoelus

(Water-

Apanteles spp.

cocoon cocoon pupa mummified larva larva

3.2% (1/31) 20.6% (13/63) ---

cocoon pupa

--

cocoon

15.4% (4/26)

PARASITOIDS OF LEPIDOPTEROUS PESTS OF COT'TON IN B U R K I N A FASO

Parasitoids

Hosts

Stage attacked

Host-stage from which the parasitoid emerges

Maximum weekly parasitism rate

Apanteles sagax Brachymeria sp. S. derogata

cocoon

Apanteles spp. Apanteles sagax

cocoon cocoon

30.8% (8/26) 7.7% (4/52)

pupa

7.8% (3/38) --

ELASMIDAE 22

Elasmus flaviceps Ferri~re

23 24

TRICHOGRAMMATIDAE Trichogrammatoidea n. sp. Trichogrammatoidea lutea Girault

25 26 27

ICHNEUMONIDAE Metopius discolor Tosquinet Xanthopimpla aliena Krieger Charops sp.

28

Parania sp.

29

oidesCampt~

30

31

Echthromorpha sp. 9 Stictopisthus africanus Ferri~re

32 33 34 35

Aleiodes sp. A. dedivus (Sz6pligeti) Meteoridea testacea (Granger) Meteorus laphygmarum (Brues)

36 37 38 39 40

Apanteles sp. A. syleptae Ferfi~re A. sagax Wilkinson Dolichogenidae sp.

H. armigera H. armigera D. watersi A. flava

egg egg egg egg

egg egg egg egg

22.2% (2/9) 5.6% (1/18) 25.0% (2/8)

S. littoralis S. derogata H. armigera S. littoralis S. derogata

larva

pupa pupa larva larva pupa

13.9% (5/36) 22.7% (5/22) 0.7% (I/148) 6.5% (2/31) 12.5% (I/8)

pupa pupa larva cocoon

4.7% (3/64) --3.8% (1/26)

larva larva larva

(Hemipimpla) vipi- S. derogata? A. flava S. derogata A. flava Apanteles spp.

larva

BRACONIDAE

Microgastrinae ind6termin6

Cotesia sp. Megagathis aft. costata Brull6 Chelonus sp. 1 44 Chelonus sp. 2 45 Pentatemus striatus (Sz6pligeti) 46 Protomicroplitis sp. 41 42 43

A. flava Earias sp. S. derogata H. armigera S. littoralis? Earias sp.? H. armigera S. derogata S. derogata S. derogata Earias sp. H. armigera H. armigera S. derogata S. littoralis A. flava Earias sp. Earias sp. A. flava

larva larva larva larva larva larva larva larva larva larva larva larva larva larva larva larva

larva larva pupa larva larva larva larva larva larva larva larva larva larva larva larva pupa larva larva

17.4% (4/23) 11.1% (3/27) 32.9% (28/85) 4.2% (2/48) 5.0% (1/20) 1.3% (2/160) 8.3% (7/84) 7.3% (3/41) 16.7% (2/6) 0.7% (1/148)

4.0% (1/25) 1.4% (1/70) 2.3% (1/44)

CERAPHRONIDAE 47

48 49

Aphanogmus fijiensis (Ferri~re) PERILAMPIDAE Perilampus sp. P. microgastris Ferfi~re

cocoon

Apanteles spp. M. laphygmarum S. littoralis Apanteles spp.

10.0% (1/10)

cocoon

larva

pupa cocoon

547

10% (1/10)

548

J. C. STREITO & S. N I B O U C H E

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PARASITOIDS

OF LEPIDOPTEROUS

PESTS OF COTTON

IN BURKINA

FASO

549

TABLE 2

Parasitoids emerged from H e l i c o v e r p a a r m i g e r a larvae collected in Farako-B~ from 1991 to 1994. Annual average parasitism rates. Maximum values of the weekly parasitism rate

1991

1992

1993

1994

N u m b e r o f c o l l e c t e d larvae A n n u a l a v e r a g e p a r a s i t i s m rate M a x i m u m w e e k l y p a r a s i t i s m rate

90 0% --

435 1.4% --

541 7.4% 11.3% (18/160)

174 16.1% 3 2 . 9 % (28/85)

Meteorus laphygmarum Cotesia sp. Unidentified Microgastrinae Exorista sp.

-----

0.9% ----

5.2% 0.2% 0.6% 0.2%

16.1% ----

Unidentified parasitoids

--

0.5%

1.2%

--

PARASITOIDS OF

DIPAROPSISWATERSI

From June to September 1994, 227 eggs were collected. Only two were parasitized by Trichogrammatoidea lutea (parasitism rate 0.9%). Fifty larvae were collected. One was parasitized by Carcelia sp. During the 1993 and 1994 dry seasons (from January to May), 380 pupae were collected in the soil. None of them was parasitized.

TABLE 3

Parasitoids emerged from E a r i a s spp. larvae collected in Farako-Bd in 1992 and 1994. Annual average parasitism rates. Maximum values of the weekly parasitism rate

1992

1994

258 10.5% 2 4 . 0 % (6/25)

167 11.4% 2 6 . 1 % (6/23)

T a c h i n i d a e sp. 5

1.2% 0.8% 0.4% ---

3.6% 1.2% -3.0% 0.6%

Unidentified p a r a s i t o i d s

8.1%

3.0%

N u m b e r o f c o l l e c t e d larvae A n n u a l a v e r a g e p a r a s i t i s m rate M a x i m u m w e e k l y p a r a s i t i s m rate

Dolichogenidea sp. Meteorus laphygmarum Pratomicroplitis sp. Aleiodes dedivus

PARASITOIDS OF

SPODOPTERALITTORALIS

Of 248 larvae collected in Farako-B~ in 1994, 44 were parasitized (table4). The parasitism rate reached a maximum of 25.8%. Five species were identified. Caroelia sp. was the same species that parasitized H. armigera and D. watersi, but the other Tachinidae could not be identified. A sixth species, Chelonus sp. 1, emerged from larvae collected at

550

J. C. STREITO & S. N I B O U C H E

Farako-B~. Perilampus sp., which emerged from a pupa, was probably a secondary parasitoid. The most frequent species was Metopius discolor Tosquinet, followed by an unidentified Tachinidae and Meteorus laphygmarum. During the dry season (January 1993 and from January to May 1994), 194 pupae were collected in the soil. Seventeen M. discolor emerged from those pupae and a further 33 dead M. discolor were recorded after the dissection of pupae with no emergence. Sixty-nine pupae were collected at the end of the rainy season (October 1994); 15 of them were found to be parasitized by M. discolor. M. discolor emerged in the laboratory during the dry season from January to June. This suggests that M. discolor can survive the dry season with a pupal diapause.

TABLE 4

Parasitoids emerged from Spodoptera littoralis larvae collected in Farako-B~ in 1994. Annual average parasitism rate. Maximum value of the weekly parasitism rate

Number of collected larvae Annual average parasitism rate M a x i m u m weekly parasitism rate

Metopius discolor Meteorus laphygmarurn Charops sp. Perilampus sp. Carcelia sp.

248 17.7% 25.8% (8/31)

Tachinidae sp. 5 Tachinidae sp. 1

6.0% 2.0% 0.9% 0.4% 0.4% 2.8% 0.4%

Unidentified parasitoids

4.8%

PARASITOIDS OF SYLLEPTEDEROGATA

In 1994, 405 S. derogata larvae were collected at Farako-Bfi, with an average parasitism rate of 9.1% (table 5). Three primary parasitoid species were identified: Apanteles syleptae Ferfi~re, Apanteles sagax Wilkinson and Parania sp., which emerges from pupae. Meteoddea testacea (Granger) emerged from pupae after a collection of larvae outside Farako-B~ in 1991. Pupae of two species, Megagathis aft. costata Brull6 and Camptotypus vipioides (Brull6), were collected in cotton leaves rolled by S. derogata larvae. Apanteles spp. are the main larval parasitoids. A. sagax emerged from larvae older than those from which A. syleptae emerged. No more than one A. syleptae larva emerged from one S. derogata larva, but an average of 27 A. sagax larvae emerged from each S. derogata larva (with a maximum of 50). In 1993 and 1994, 502pupae were collected at Farako-B~ (table 5). Annual average parasitism rates were very different in the two years at 42.9% and 15.6% respectively. Nine primary parasitoid species were identified. The most important group of species belongs to the genus Brachymeria, with 71.0% of the parasitoids collected in 1993 and 47.5% in 1994. In 1993, part of the species B.feae, B. citrea et B. kassalensis were not correctly identified and are grouped under Brachymeria spp. in table 5. The Ichneumonidae Xanthopimpla aliena Krieger was hardly present at all in 1993 but formed more than a third of the

PARASITOIDS OF LEPIDOPTEROUS

PESTS OF COTTON IN BURKINA FASO

551

parasitoids collected in 1994. Four secondary parasitoids were identified. Pediobius amaurocoelus (Waterston) was the most common species (table 5).

TABLE 5

Parasitoids emerged from S y l l e p t e d e r o g a t a larvae and pupae collected in Farako-Bd in 1993 and 1994. Annual average parasitism rate. Maximum value of the weekly parasitism rate

1993

1994 405 9.1% 14.6% (6/41)

N u m b e r of collected larvae Annual average parasitism rate M a x i m u m w e e k l y parasitism rate

Apanteles sagax Apanteles syleptae Parania sp,

----

3.7% 3.2% 0.5%

Unidentified parasitoids

--

1.7%

N u m b e r of collected pupae Annual average parasitism rate M a x i m u m w e e k l y parasitism rate Primary p a r a s i t o i d s

Meteoridea testacea Brachymeria spp. B. olethria B. feae B. citrea B. kassalensis Xanthopimpla aliena Parania sp. Echthromorpha sp.

233 42.9% 61.5% (16/26)

269 15.6% 50.0% (11/22)

0.4% 17.2% 8.6% 2.1% 1.3% 1.3% 0.4% 1.7%

0.4% 0.4% 5.6% 1.1% 0.4% -4.8% -0.7%

5.6% 0.9% 0.4% -3.0%

1.5% --

Secondary parasitoids

Pediobius amaurocoelus Eurytoma lepidopterae E. syleptae Nesotynx phaeosoma Unidentified parasitoids

0,7% --

The study of secondary parasitoids attacking Apanteles spp. was performed by collecting Apanteles cocoons in the field. Isolated cocoons and mass-grouped cocoons were distinguished. Mass-grouped cocoons were exclusively A. sagax but isolated cocoons comprised A. syleptae and an unidentified Apanteles species (table 6). This unidentified Apanteles species was not obtained from S. derogata larvae reared in 1994 (table 5). Some Apanteles that emerged from isolated cocoons were unfortunately destroyed before further identification and the specimens concerned have been grouped as 'unidentified Apanteles'. For unidentified reasons, no emergence was noted from a large proportion of the cocoons (table 6). The secondary parasitism level was high in both cases at 45.3% for isolated cocoons and 43.6% for A. sagax cocoons. Elasmus flaviceps Ferri~re was the main secondary parasitoid of isolated cocoons, followed by N. phaeosoma and P. amaurocoelus

552

J. C. STREITO & S. NIBOUCHE

(table 6). The genus Eurytoma was the most important secondary parasitoid of A. sagax cocoons. Two species were present (E. syleptae and E. braconidis) but they are difficult to distinguish from each other, notably the males (some specimens are therefore grouped as Eurytoma spp.). No secondary parasitoid emerged from Apanteles cocoons obtained from rearing of S. derogata larvae. Some secondary parasitoids also attack Brachymeria spp. and X. aliena. The secondary parasitoids P. amaurocoelus and N. phaeosoma were obtained from S. derogata pupae, respectively parasitized by Brachymeria sp. and by X. aliena (identified by dissection of the pupae after emergence of the seconday parasitoids). Eurytoma lepidopterae Risbec emerged from a S. derogata pupa. This species is probably a secondary parasitoid, but its host could not be identified.

TABLE 6

Parasitoids emerged from Apanteles spp. cocoons collected in Farako-B~ in 1993. Annual average parasitism rate. Maximum value of the weekly parasitism rate

Number of collected cocoons

Isolated cocoons

Mass-grouped cocoons

148

158

Apanteles sp. Apanteles sylepiae Apanteles sagax unidentified Apanteles

4.7% 11.5%

No emergence

27.0%

53.9%

45.3% 65.4% (17/26)

43.6% 90.4% (47/52)

18.2% 10.1% 0.7% 1.4% 0.7% 1.4% 4.7% 0.7% 7.4%

2.5% 0.6% ---10.8% 18.3% 7.0% 4.4%

Average secondary parasitism rate Maximum secondary parasitism rate

--

2.5%

11.5%

Secondary parasitoids

Elasmus flaviceps Nesolynx phaeosoma Aphanogmus fijiensis Perilampus microgastris Stictopisthus africanus Eurytoma spp. Eo syleptae Eo braconidis Pediobius amaurocoelus

PARASITOIDS OF ANOMIS FLAVA

Only a few A.flava eggs were collected. Of the 14 collected, five were parasitized by T. lutea.

The parasitism level of A. flava larvae collected in Farako-Bfi in 1994 was low (table 7). The Chelonus species (sp. 2) parasitizing A. flava was different from the species parasitizing S. littoralis. Mummified A. flava larvae parasitized by Aleiodes sp. were frequently noticed on cotton leaves. Copidosoma floridanum (Ashmead) emerged from a mummified larva. However, the

PARASITOIDS OF LEPIDOPTEROUS PESTS OF C O T T O N IN B U R K I N A FASO

553

m u m m y was too deformed for it to be absolutely certain that it was an A. flava larva. A. brachymeria emerged from the pupa of a dipteran that primarily parasitized an A. flava larva. The parasitism level of A.flava pupae was higher than for larvae (table 7). Occasional collection of pupae enabled the identification of Brachymeria feae, B. kassalensis and the Tachinidae Winthemia dasyops Wiedemann. The (probably secondary) parasitoid Eurytoma lepidopterae emerged from A. flava pupae, but its host could not be identified.

TABLE 7

Parasitoids emerged from A n o m i s flava larvae and pupae collected in Farako-Bd in 1994. Annual average parasitism rate. Maximum value of the weekly parasitism rate 235 3.8% 13.3% (2/15)

Number of collected larvae Annual average parasitism rate M a x i m u m weekly parasitism rate Primary parasitoids Protomicroplitis sp. Chelonus sp. 2 Tachinidae sp. 4 Tachinidae sp. 3

0.4% 0.4% 1.3% 0.4%

Secondary parasitoids

Brachymeria sp. Stictopisthus africanus

0.4% 0.4%

Unidentified parasitoids

0.4% 85 16.5% (14) 22.2% (4/18)

Number of collected pupae Annual average parasitism rate M a x i m u m weekly parasitism rate

Echthromorpha sp. Brachymeria spp. Tachinidae sp. 2 Tachinidae sp. 3

3.5% 4.7% 3.5% 2.4%

Unidentified parasitoids

2.4%

DISCUSSION PARASITOID SPECIES OBSERVED

Eleven primary parasitoid species were obtained from H. armigera. Among them, the two unidentified species belonging to the genus Cotesia and Dolichogenidea were not mentioned by van den Berg et al. (1988) or Greathead & Girling (1989) in their reviews of natural enemies of H. armigera in Africa. The number of species attacking H. armigera in Burkina Faso is similar to previous records in cotton areas from the Afrotropical area: 12 species in South Africa (Parsons, 1940), 14 in Uganda (Coaker, 1959) and 10 in Tanzania (Nyambo, 1990). A preliminary study of egg parasitism was enough to observe a new species of Trichogrammatoidea; this indicates that more work is needed to improve the

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inventory of egg parasitoids in Burkina Faso. For example, van den Berg et al. (1993) list seven egg parasitoids species attacking H. armigera in Kenya (this included crops other than cotton). With the exception of the unidentified Protomicroplitis and the Braconidae Pentatemus striatus, all Earias spp. primary parasitoids collected in Burkina Faso have been recorded previously (Couilloud, 1987; Silvie et al., 1989; Silvie et al., 1993; Bagayoko et al., 1993). Although relatively few D. watersi were successfully reared, the diversity of parasitoids was low with only two species collected. This low level of parasitism is consistent with previous studies. Galichet (1964) listed only four primary parasitoid species in Chad, including a nematode. Pearson (1958) reviewed 10 larval primary parasitoids and two egg parasitoids attacking the genus Diparopsis, but noted that parasitism rates were generally extremely low. With the exception of Chelonus sp., all the S. littoralis parasitoids identified in Burkina Faso had been observed by other authors in different parts of the Afrotropical area (Pearson, 1958; Silvie et aL, 1989, 1993). Three parasitoids associated with S. derogata in Burkina Faso were not listed by Silvie (1990): Parania sp., Eurytoma lepidopterae and Aphanogmus fijiensis (the species Aphanogmus reticulatus was nevertheless mentioned in Chad). It should be noted that the primary parasitoid mentioned in Chad (Silvie et al., 1989) and Togo (Silvie et al., 1993) as Xanthopimpla punctata (F.) is in fact X. aliena, which is the species also identified in Burkina Faso (Delvare, pers. comm.). The list of parasitoids attacking A. flava in Burkina Faso includes several new records. Of nine species observed, five are not listed in Deguine's review (1991): the genera Chelonus and Echthromorpha, Brachymeria kassalensis and Trichogrammatoidea lutea (although the genus Brachymeria and Trichogrammatoidea are listed). It should be noted that the only known African species belonging to the genus Echthromorpha is E. agrestoria, with the subspecies variegata Brull6 for continental Africa (Townes & Townes, 1993). The Encyrtidae Copidosoma floridanum (whose status of A. flava primary parasitoid should be confirmed) was not listed by Deguine (1991). On the other hand, Nurindah & Bindra (1988) mentioned Copidosoma sp. in Indonesia. PARASITISM LEVELS

Much information is available on parasitism levels for H. armigera and S. derogata, but few results are available for the other species studied here. Parasitism rates in H. armigera in Burkina Faso showed great variability but were generally lower than 20%. Those results are similar to studies everywhere else in the Afrotropical area (Parsons & Ullyett, 1934; Parsons, 1940; Coaker, 1959; Reed, 1965; Nyambo, 1990; van den Berg et al., 1993). On the other hand, the role of Meteorus laphygmarum (which formed more than 80% of the parasitoids collected) is outstanding. Van den Berg et al. (1988) and Greathead & Girling (1989) described this species as 'rare' in reviews of works mainly carried out in Eastern and Southern Africa. The average S. derogata larval and pupal parasitism levels observed in Farako- B~ in 1994 are consistent with values reported in Chad (Silvie, 1991) and Togo (Silvie,1993). Parasitoids emerging from larvae in Burkina Faso belong mainly to the genus Apanteles, with equivalent numbers of the species sagax and syleptae. Previous work generally reported greater influence of one of the two species (Odebiyi, 1982; Silvie, 1991; Silvie, 1993). In Chad, Silvie (1991), noticed that Apanteles spp. were less common than Meteoridea testacea. Brachymeria spp. are the most common parasitoids emerging from

PARASITOIDS OF LEPIDOPTEROUS PESTS OF COTTON IN BURKINA FASO

555

pupae collected in the field. The most common Brachymeria species in Farako-B~ is B. olethria, but some care is necessary because of the large number of specimens unidentified at species level in 1993 (more than half the specimens collected). This dominance of one species was not noticed in Togo or in Chad (Silvie, 1991, 1993) where B. olethria and B.feae are found in equivalent numbers. As previously noticed by Silvie (1993) in Togo, the Ichneumonidae X. aliena was more common when S. derogata populations were high (1994) than when populations were small (1993). The high secondary parasitism levels noticed in Farako-Ba for field-collected Apanteles spp. cocoons were similar to the levels reported in Chad (46.5%) and Togo (56.4%) by Silvie (1991, 1993). The main secondary parasitoid species are the same in Burkina Faso, Chad and Togo, but there are differences in their relative proportions: N. phaeosoma is the most common on A. syleptae in Togo and Chad but less common than E.flaviceps in Burkina Faso. Average parasitism levels, as presented here cannot be used for accurate assessment of the impact of a parasitoid on the dynamics of the host population (Silvie, 1993). The peak parasitism rates given enable assessment of the potential effect of a parasitoid on its host. However, the results are biased by the calculation method. Parasitism rates were calculated by using the total number of larvae collected while most parasitoid species only attack specific instars of their host. This bias results in underestimation of parasitism rates (van den Berg et al., 1988). Moreover, all the results presented were obtained in an untreated field of very limited size (0.25 ha) in comparison with the total area under cotton receiving pesticide sprays. The parasitism effect would probably be greater if pesticide use was less intensive in the cotton growing area. While average parasitism rates observed in Farako-B~ were generally low, exceeding 20% only for S. derogata pupae in 1993, maximum weekly parasitism rates were often much higher and indicate that parasitism rates are potentially high and that parasitoids may sometimes have a s!gnificant effect on their host populations. Secondary parasitoids are mainly associated with the Apanteles spp. that parasitize S. derogata. High secondary parasitism levels decrease the (low) effectiveness of Apanteles spp. on S. derogata larvae populations. In addition, it is possible that large populations of those secondary parasitoids generated by the usually high S. derogata populations could have a significant negative influence on the populations of primary parasitoids of other pests. N. phaeosoma, P. amaurocoelus and A.fijiensis are indeed polyvalent secondary parasitoids that can parasitize M. laphygmarum, Aleiodes spp. or Brachymeria spp., which are key primary parasitoids of H. armigera or Earias spp. No systematic collection of M. laphygmarum cocoons or Aleiodes mummies was performed and the actual incidence of this secondary parasitism could not be assessed. This indicates the interest of quantitative study of trophic interactions by considering not only parasitism rates but also the population density of parasitoids and their hosts (Memmot & Godfray, 1993). ACKNOWLEDGEMENTS This study was carried out at the Programme Coton of the Institut d'Etudes et de Recherches Agricoles (INERA). Funding was provided both by INERA and by the Centre de Cooperation Intemationale en Recherche Agronomique pour le Developpement (CIRAD). The authors thank G. Delvare of the Laboratoire de Faunistique et de Taxonomie du CIRAD (CIRAD/LFT) for identifying a large proportion of the specimens. Thanks are also due to A. Delobel (ORSTOM) who identified or confirmed identification of Ichneumonidae, and to Dr. van Achterberg (Nationaal Natuurhistorisch Museum, Leiden, Netherlands) who identified some Braconidae. Insects identified in

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this study are located in the INERA Programme Coton and in the CIRAD/LFT. We thank G. Delvare and J. P. Bournier for their critical reading of the manuscript. Particular thanks go to the technical team, D. KambirE, S. SamakE~ M. YE, M. Dayamba, I. Sow, B. Yougbar6 & O. HombouE, for collection and rearing work.

RI~SUME PremiEres observations sur les parasito'fdes associEs aux 16pidopt~res dEprEdateurs de la culture cotonni~re au Burkina Faso Une Etude des parasito'ides des ravageurs du cotonnier au Burkina Faso a EtE menEe entre 1991 et 1994 sur les genres ou esp~ces de 16pidopt~res suivants: Helicoverpa armigera (Htibner), Earias spp., Diparopsis watersi (Rothschild), Spodoptera littoralis (Boisduval), Syllepte derogata (E) et Anomis flava (E). Trente-neuf parasito'fdes primaires et dix parasito'fdes secondaires ont EtE observes. Les taux de parasitisme moyens annuels sont infErieurs ~ 20%, hormis pour les chrysalides de S. derogata (42,9%). Les valeurs maximales des taux hebdomadaires de parasitisme peuvent 8tre ElevEes: 61,5% pour les chrysalides de S. derogata ou 32,9% pour les chenilles de H. armigera. Les taux maxima de parasitisme les plus ElevEs ont EtE obtenus avec Meteorus laphygmarum Brues (Braconidae) sur H. armigera; Xanthopimpla aliena Krieger (Ichneumonidae), Brachymeria olethria (Waterston) et B. citrea (Steffan) (Chalcididae) sur S. derogata; Aleiodes dedivus (SzEpligeti), Dolichogenidea sp. (Braconidae) et Brachymeria feae Masi sur Earias spp.; un Tachinidae indEterminE sur A.flava; Metopius discolor Tosquinet (Ichneumonidae) sur S. littoralis. Les parasito'ides secondaires sont essentiellement associEs aux Apanteles spp. (Braconidae) parasitant les larves de S. derogata. Parmi ces parasitoi'des secondaires, certaines esp~ces, telles que Nesolynx phaeosoma (Waterston), Pedobius amaurocoelus (Waterston) (Eulophidae) ou Aphanogmus fijiensis (Ferri~re) (Ceraphronidae), sont susceptibles de s'attaquer 6galement aux Braconidae ou aux Chalcididae parasites primaires des autres 16pidopt&es. Received: 10 February 1947; Accepted: 17 September 1997.

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