A BIOLOGICAL REVIEW OF THE GENUS EUPLECTRUS [HYM ...€¦ · A BIOLOGICAL REVIEW OF THE GENUS EUPLECTRUS [HYM.: EULOPHIDAEj WITH SPECIAL EMPHASIS ON E. LAPHYGMAE AS A PARASITE OF

A BIOLOGICAL REVIEW OF THE GENUS EUPLECTRUS[HYM.: EULOPHIDAEj WITH SPECIAL EMPHASIS

ON E. LAPHYGMAE AS A PARASITE OF SPODOPTERA LITTORALlS[LEP. : NOCTUIDAE]

Department of Zoology, The George S. Wise Centre for Life Sciences,Tel Aviv University, Israel.

The life history and behavior of Eupleclrus laphygmae FERRIERE were stLldied.The parasites paralyse the host larvae temporarily before ovipositing 1-2 eggs ontheir dorsum. Egg and larval development takes place externally in the locationof egg deposition and pupation is in a silken cocoon under the dead host. Deve-lopment lasts 11.7 days for both sexes. The eggs are attached to the host witha pedicel that is inserted under the cuticle but above the hypodermis, and whichmay have physiological and mechanical functions. The adult parasites host-feed, but do not lay on the same host. All hosts stung by parasites die, regardlesswhether oviposition has occurred, or whether host larvae develop upon them.Multiparasitism with internal parasites of Spodoplera liltoralis (BOISD.) wasobserved.

A comparison with other Eupleclrus species was made. They have a widerange of lepidopterous hosts but very similar biological characteristics. Only veryfew utilizations for biological control have been reported with this genus.

Among parasites that were introduced into Israel from East Africa during 1969-1970 in an attempt to control Spodoptera !ittora/is (BOISD.) was also Eup/ectrus /aphygmaeFERRIERE. The biology and autecology of this species as a parasite of S. !ittoraliswere studied in order to determine its potential, and to develop suitable rearing tech-niques. In general, our results resemble those of NESER (1973), who studied an unde-termined species that is close to E. /amphygmae. However, there are differences inthe host-parasite association, in the emphasis given to different parts of the research,and in some of the results. Therefore, we chose to present a short account of theparasite's life history and dwel1 on some of the biological phenomena that wereobserved.

MATERIALS AND METHODS

The parasites were reared originally from Spodoptera exempta WLK, larvae whichwere collected between June 23 and July 10, 1970 in the vicinity of Nairobi, Kenya (1).They were re ared as parasites of S. liTtoralis larvae, in screen-topped plastic Petri dishes

(I) Through the cooperation and courtesy of Mr. E. BROWN of the East African Agricultureand Forestry Research Organization.

at a temperature of 26 ± 1.5°C. The hosts used were of the 2nd and 3rd instar andwere supplied with leaves of castor bean plants, on which they fed until their death.Parasite females were kept singly in Petri dishes throughout their lives. They werefed honey that was streaked upon the walls of the dish. Hosts were replaced every24 hours, until the parasite female died. The parasitized hosts were kept in Petridishes until the new parasite adults emerged.

OVIPOSlTION

The parasite female examines the host with her antennae, and then jumps onits back. The host tries unsuccessfully to dislodge her while she inserts her ovipositorinto the integument. The host larva becomes motionless within a short ti me, andthe parasite lays her eggs and leaves. About one minute later, the host resumes itsactivity which appears to be normal. Only the first 4 of the 6 larval stages of thehost are attacked. On the 4th instar larva, the eggs are laid in small groups on theanterio-dorsum, whereas on instars 1-3, they are laid singly and may be depositedanywhere from the head to the anal segment, on the dorsal aspect of the abdominalsegments.

The parasitized host larvae usually do not molt again. In exceptional cases,partial moulting took place, and the old larval skin remained attached to the host atthe oviposition sites.

DEVELOPME T

The eggs become black 24 hours after oviposition, and hatch 24 hours later.The parasite eggs hatch in situ and the whole larval development takes place at

the same location. We observed 4 larval instars, each of which split the exuviumof his predecessor in the mid-dorsal line before commencing to feed. The 4th instarhas its posterior 3 segments extended into a tail-like portion through which it exudesthe silken material which is used for cocoon spinning. The material itself originatesin modified malpighian tubules (THOMSEN, 1927). Developmental duration was:egg 2 days, larva 3.4 ± 0,02 days, pupa 6.3 ± 0,04 days, averaging a total of 11.7 days(n = 580).

The eggs are attached to the host with a pedicel. According to NESER (1973),the pedicel of the egg in E. Hr. laphygmae is inserted into the integument of the host.Our studies confirmed this observation for E. laphygmae. Moreover, our sectionsshow c1arly that the egg is held in place by a plug that is inserted between the cuticleand the epidermal layer (fig. I). We tried to determine whether the pedicel is a mereanchoring device, or if it has additional functions. For this purpose the pedicels ofeggs were cut at different stages of their development. Thereafter, the eggs werereplaced on top of the same host from which they have been removed. Care wastaken that the eggs would not be dislodged in the absence of the anchoring device.Invariably, the eggs failed to hatch and their development was arrested, (as judgedby the lack of color changes of the chorion). This may have been caused by mecha-nical damage and/or infection; additionally, the pedicel may have served in the trans-port of materials from the host to the parasite egg.

CAUSE OF HOST MORTALITY

As mentioned, the hosts resume apparently normal activity about I minute afterthe parasites complete oviposition. However, their activity diminishes during thenext days and they stop feeding within 2-8 days after oviposition. In order to deter-

mine whether host mortality is caused by parasite feeding, we removed the parasiteeggs and larvae from the hosts at different developmental stages, and followed thebehavior and fate of the hosts. The observations showed that the larvae of S. littoralisalways stopped feeding and died, whether or not living parasites were feeding uponthem. The death-inducing factor is apparently injected by the parasite female whenshe attacks the host, and acts independently of the parasite larvae. However, it ispossible that the speed at which the hosts die is modified by the number of the parasitelarvae feeding upon it.

FIG. I. Egg of E. laphygmae imbedded in the integument of an S. lilforalis larv~.FIG. 2. An egg of E. laphygmae attached to a larva of E. laphygmae. a. egg, b. pedicel, c. larva, d. previous

molting skin of the larva.

HYPERPARASITISM, SUPERPARASITISM AND MULTIPARASITISM

As a rule, E. laphygmae was a primary parasite of S. littoralis. However, thereadiness of the parasite female to oviposit upon hosts already parasitized, causedher to lay her eggs also on other larvae of E. laphygmae (fig. 2). We attributed thisphenomenon to the laboratory conditions in which the host was confined with theparasites in a small chamber.

Superparasitism occurs whenever more parasites attack a host than it is able tosustain, and the result is that both and parasites die. The usual egg complement on2nd or 3rd instar larvae of S. littoralis was or 2 per host, but under laboratory condi-tions, the parasites continued to oviposit also on hosts that already bore parasite eggsand larvae. In this fashion, we observed as many as 18 eggs per host larva. On4th instar S. littoralis larvae, we obtained successful development of up to 12 parasites,whereas on younger ones only 4 or less were able to develop successfully. However,the individuals that managed to complete their development under crowded condi-tions were often much smaller than normal ones.

NESER (1973) observed multiparasitism by E. nr. laphygmae and the internalparasites Microplitis sp., Meteorus laphygmorum BRUES, and Copidosoma sp. Wedid not offer to E. laphygmae in the laboratory any hosts that have been previouslyparasitised, as NESER did. However, 1 larva of S. littoralis, that had been collectedin the field, bore eggs of E. laphygmae and also produced a larvae of Microphetis rufi-ventris KOK. All of the parasites pupated but only a male E. laphygmae emerged.

HOST RANGE

Our stock material was collected from S. exempta in Kenya. We also obtainedmaterial from S. littoralis larvae, and Plusia sp. feeding on groundnuts in Uganda.The parasites attacked S. littoralis readily in our laboratory. They also oviposited

on 29 of 120 larvae of S. exigua HB . that were presented to them. Oviposition wassuccessful on Heliothis sp. but the host larvae died invariably before the parasites weresufficiently developed. Larvae of Acrocercops conjlua MEYR and Aporophyla sp.(Lep., Noctuidae) were also oviposited upon. However, the latter were always super-parasitized and both host and parasites died. Two unidentified pterophorid larvaewere also laid upon, a total of 7 eggs of which only I hatched. The rest remained whiteand did not develop, whereas the host larvae reacted by forming a melanized spotupon the locus of oviposition.

When a male encounters a female, he faces her and starts to wave his wings upand down rapidly. If the female is receptive, she will almost immediately stand quietlyand elevate the tip of her abdomen somewhat, whereupon the male will mount her.Mating lasts up to 2 seconds <:fter which the male returns to his original position andresumes the wing-flapping. The female does not respond again, and no second matingswere observed. After a few minutes (average 7, maximum 15), the female leaves andthe male stops the courting behavior. The males exhibit their excited behavior onalmost all encounters with females and may mate several times during their life.

In order to learn more about the attraction of the males to females, we confrontedmated and unmated males with separate body parts of females. The separate heads,thoraxes, abdomens, and an ethanol extract of heads and thoraxes were placed infront of the males and the presence and duration of their courting dance were registered.The males did not respond to the abdomens, but danced for periods varying from I to11 minutes in front of the other options (table I). It was the attraction to the thoraxthat was the strongest, but the tests were insufficient to determine if the pheromoneoriginated in the head, thorax, or both.

TABLEI"Dancing " response of males of E. laphygmae to female body parIs

Part tested : Whole Head Headless Thorax Abdomen Ethanolfemale female extrac:t (a)

Duration ofresponse (min.) 3-8 2-7 2-5 5-11 0 1-3Average 6.4 3.8 3 9 0 2n 5 5 5 4 5 3

(a) Extract of heads anel thoraxes presented as a drop on a glass plate

Number ol eggsThe egg complement of 31 females was examined, and their daily ovipositions

were recorded. The females laid an average of 165 ± 18 (32-415) eggs during theirlife of 34 ± 2 (32-38) days, or an average of 4.6 ± 0,3 eggs per female per day. Wecalculated the daily average percentage of eggs laid by the females, and plotted itagainst time. The results (fig. 3) gave 2 regression lines which indicate that averageoviposition rose from the first to the 5th day of the female's life, and then declinedslowly till her death. The Ilumber of eggs laid per host larva was tested on 2071 young(instar 2-3) hosts, in most cases I (540) or 2 (827) eggs were laid on each host (fig. 4).This was in contrast with the field collected material that was received from Kenya.In the latter, S. exempla larvae usually bore 4 or more parasites per host.

y>-0 15"0

3{;0ill

"0 100

'"C1'C1' 5CIJ

'0~

0

~ 900 [

~ 700

.'.. , ....

10 20 30 ';0 50 x

Age of female ( DaY5)

"0ill

'".~ 500oL.

oa.. 300

'0ci 100Z

111211o 2 .; 6 8 10 12 1'; 16 18 20

>-

1001

5 ~ 800'0ii 60CIJ ';00E~ 20

~ 10 t-~-~-~-~-~----'---'--

10 15 20 25 30 35 40Age- of female- (DaY5)

FIG. 3. Percent of daily oviposition, as a function of female's age.FIG. 4. Number of S. lilforalis larvae parasitized by E. laphygmae, as a function of the number of

eggs per host.FIG. 5. The sex ratio of progeny of mated E. laphygmae females, as a function of their age.FIG. 6. Mortality of the developing stages of the parasites, as a function of the number of eggs per

host.

3

#e-gg5/ho5t

Sex determination and parthenogenesis were tested by recording the sex ratioof the progeny of 31 females, and then dissecting the mothers in order to determineif they have been fertilized. We found that most of the females were arrhenotokous,i.e. only mated females gave rise to female progeny. In 2 cases, we found deutotoky,since female progeny were produced by unfertilized mothers. The sex ratio in thesecases was 1/45 and 1/72 in favor of the males.

The overall sex ratio of the progeny of mated, females, averaged 55 % females(l187 out of 2121 progeny), and the ratio per ovipositing female did not change signi-ficantly throughout her life (fig. 5). The sex ratio per host varied with the numberof eggs laid. Sixty-eight percent (75 out of 109) of the cases of single eggs per hostproduced males, all of the 27 hosts that bore 2 eggs produced I male and 1 female;whereas the 7 cases of 3 eggs per host produced I male and 2 females each. Largeregg batches produced usually a few parasites of each sex.

A group of 103 males and a group of 46 females, were kept in glass vials withhoney, and their longevity was tested. Both sexes were allowed to mate freely but

no hosts were made available for oviposition by the females. The males lived anaverage of 29.1 ± 1.8 days and the females 45 ± 1.8 days.

Mortality of the developmental stages was examined both as a function of thestage in which the parasite was, and as a function of the number of parasites per host.The results were, that an average of 60.4 % of 3356 eggs gave rise to adults, and thatpupal mortality accounted only for 4.1 % of this amount. Egg and larval mortalityaccount, therefore, for 35.5 % mortality of the developing progeny, or 92.4 % of thetotal mortality. An examination of mortality as a function of number of eggs perhost (fig. 6) shows clearly that mortality rises sharply with the number of eggs laidon each host, being some 30 % at 1 egg per host, and 46 % at 7 eggs per host.

DISCUSSION

So far, some 55 species of Euplectrus have been recorded and catalogued in theliterature. These insects occur in all continents and include tropical species asE. laphygmae, subtropical ones as E. agaristae and E. nr. laphygmae, and temperateones as E. bicolor and E. platyhypenae. Only a few species have been studied in detail,these include E. r.rgaristae, E. bicolor, E. parvulus, E. platyhypenae, E. nr. laphygmae,and E. laphygmae. These studies, together with the scattered observations that arereported in association with other described species, allow us to summarize the presentknowledge about this biologically unique genus.

Euplectrus species are external parasites of lepidopterous larvae. Few recordsof other hosts exists, gall midges (SILVESTRI, 1911) and Lecanium (CHAIRMONTE, 1933).These host records should be reexamined. Within the Lepidoptera, the host rangeis very wide, and includes mainly Heterocera. The recorded families are :arctiids, coleophorids, gelechiids, gcometrids, hesperiids, hyspids, limacodids,Iymantriids, noctuids, papiJionids, phycitids, pterophorids, sphingids, tortricids, andzygaenids. Most of the Euplectrus species are reported from I host only. However,the few species on which biological data exist, are all known to be oligophagous orpolyphagous. The host range of E. platyhypenae includes over 13 noctuid speciesbelonging to 10 different genera, and E. laphygmae has been reared from 5 noctuidspecies belonging to 3 genera and from I pterophorid. E. bicolor also has an extensivehost list; but more than I parasite species may be involved (BoucEK, 1970).

The eggs of the parasite are laid on the thorax and anterior abdominal segmentsof the host-larva, as in E. nr. laphygmae, (NESER, 1973) and E. platyhypenae (WELL& BERBERET, 1974), or anywhere on the host (CHATTERGEE, 1945). In E. laphygmaethe eggs are laid anywhere on the dorsum of young hosts; but on older hosts, ovipo-sition is limited to the dorsal aspect of the thorax and fore-abdomen. This ovipo-sition pattern is apparently correlated with the greater agility of older larvae and theirability to remove parasite eggs from posterior segments.

Oviposition is accompanied by temporary paralysis of the host by E. nr. laphygmae(NESER, 1973) in E. laphygmae and in E. parvulus (CHATTERGEE,1945), whereas E. pla-tyhypenae, (CLAUSEN, 1950), and E. agaristae (NOBLE, 1938) do not induce paralysis.Additionally, eggs of the 2 former species darken greatly before hatching, whereasthose of the latter species do not.

The number of eggs laid per host is variable and depends upon the host size, thespecies of the parasite and of the host, and oviposition pressure in the female parasite.E. agaristae, laid up to 60 eggs, E. bicolor, and E. platyhypenae each laid up to about37 eggs per host, the number in E. bicolor varying with the host size (BISCHOFF, 1929).E. nr. laphygmae laid an average of 16 eggs on medium, and 25 eggs on large hosts,

whereas E. laphygmae laid on S. littoralis only 2 eggs per host, and on E. eXl'mpfa upto 8 or 10 eggs. Maxima of over 100 eggs per host were reached in some of the species;but these were due to artificial laboratory conditions and included many supernumeraryeggs.

Eggs of all species are fastened to the host's integument. CHATTERGEE(1945)reported that the eggs of E. parvulus are glued on with a host-originating fluid. Allother authors point to a pedicel as the anchoring device. The structure of the pedicelwas found to be similar in E. nr. laphygmae (NESER, 1973) and E. laphygmae, whereit has a bulbous shape and reaches below the epidermis. The egg does not surviveif the pedicel is cut, if the host reacts by forming a melanized area under the egg, orif the pedicel is not inserted into the host during oviposition; therefore, it is possiblethat the pedicel has physiological as well as mechanical functions. The eggs ofE. parvulus, that are presumably devoid of a pedicel are the only ones that can beshaken off the host.

Larval development occurs totally at the oviposition site. When moulting, thelarval exuviae are split along the dorsal midline. Once the larvae finish feeding theyleave the dorsum of the host for its venter, under which they pupate. The remnantof the egg chorion and the larval exuviae are left behind. NOBLE (1938) reported3 larval instars, THOMSEN(1927) and we found 4 instars, and NESER (1973) found 5.

When larvae are ready to pupate they spin a cocoon with which they fastenthemselves under the dead host to the host and substrate. The loose cocoon is spunthrough the anal opening with material that originates in modified malphighian tubules.The host always stops feeding some ti me after the parasite's oviposition, and dies thereafter.The exact time of death varies within the same species (NESER, 1973; WELL & BERBERT,1974) and was shown by NESER (1973) to depend upon the number of parasite larvaefeeding upon the host. The same author also showed that the host of E. nr. luphygmaeis destined to die once oviposition by the parasite has occurred, regardless of parasitesurvival and feeding upon it. Similar results were obtained by us for E. laphygmae.

The developmental cycle of the parasites is rapid; and the pupal stage is reachedin a week or less under most conditions. Development from egg to adult is longestfor E. bieolor in Russia (ZIMIN, 1930), where it required 26-35 days. In other warmerregions, the life cycle averaged some 2 weeks or less. The parasites usually did notattack the first instar larvae of their host~, neither were they found on the last instars;all of the authors recorded preference for the intermediate instars (E. agl1rislue : 3 and 4,E. laphygmae : 2-4, E. nr. laphygmae : 2-5, E. parvulus : 2, and E. plafyhypenae 3 and 4).Since different lepidopterous species show different degrees of aggressiveness, andbecause Eupleelrus species are not monophagous, it is probable that the same parasitespecies may prefer different instars of different hosts.

The adults may either spend their life actively or hibernate. In the first case,their life spans from 14 to 54 days for the females and from 12 to 30 days for the males.Overwintering females may live for several months. The number of eggs that a femalelays during her life-time was recorded to exceed 100 in E. laphygmae and E. playhypenae,however, for E. nr. laphygmae, only a maximum of 38 eggs per female were recorded(NESER, 1973).

Several variations in mating behavior were reported. E. parvulus emerges firstand "courts the female" for some 30 minutes. E. laphygmae and E. nr. laphygmaeexhibit elaborate mating dances by the males, which emerge contemporaneously withthe females. In the other species on which reports exist, the males emerge beforethe females and wait for the latter to emerge, once that happens, mating takes placeimmediately. Females were never reported to mate more than once.

The sex ratio varies greatly, but is always in favor of the females. In fieldcollected material, WILSON (1933) reported 60 % females in the third generation and90 % females in the 6th generation of E. platyhypenae. NOBLE(1938) observed 94.98 %females for E. agaristae and NESER (1973) reported between 54 and 83 % females forE. nr. laphygmae. The sex ratios for the latter were similar also in the laboratory,whereas we obtained a somewhat lower, 54 % female average in our laboratory cul-tures of E. laphygmae. All of the sex-ratio studies report that at least I male emergesfrom each oviposition, and accordingly, the ratio of females increases with the numberof eggs per host.

Host feeding has been reported for E. parvulus (CHATTERGEE,1945), E. nr. laphygmae(NESER, 1973), and E. laphygmae. It is conceivable that the other species in the genusare also synovigenic and require host-originated proteins for egg development undernatural conditions. The hosts are killed or badly injured by the feeding process,and become unsuitable for parasite development. E. nr. laphygmae did not hostfeed during the first 6 days of her adult life, a period during which she probably stillutilized eggs or proteins with which she emerged from the pupa. Thereafter, host-feeding was a prerequisite for oviposition and was performed readily. One feedingfor each female usually sufficed.

Stinging of the host before oviposition apparently does not enable the parasitefemale to determine if the host has previously been parasitized, since multiple para-sitism was reported several ti meso We reared a larva ofMicroplitis rujiventris from a larvaof S. lit/oraUs infested by E. laphygmae. NESER (1973) obtained Microplitis sp. andMeteorus laphygmarum from hosts that were infested by E. nr. laphygmae; the parasitesalso oviposited on hosts that were parasitized by Copidosoma sp., but multiple pnra-si tism did not occur since the latter failed to develop. CHATTERGEE (1945) hadE. parvulus lay but fail to develop, on larvae of Plecoptera reflexa GUEN. that had theinternal parasites Rhogas plecopterae CHAT., Microgaster plecopterae WLKN., andApanteles sp. developing within them. The success of multiple parasitism involvingthe braconids Meteorus and MicropUtis may be correlated with the fact that theseinternal parasites are blood feeders which do not kill the host during their larval deve-lopment, and that they were already mature larvae when the EupleClrus females ovi-posited upon the host.

The numerous records in which Euplectrus species have been mentioned in connec-tion with the biological control of lepidopterous pests will not be dealt with in thepresent review. However, it is noteworthy that only few successes either in naturalcontrol or by man-mediated biological control have been recorded. The best recordedcontrol works concern E. platyhypenae. It was reported to reach 20 % p3.rasitizationof the lepidopterous pests attacking alfalfa in Kansas during June and July (SMITH,1927). It has also been introduced from the continental U.S.A. into Hawaii originallyagainst Spodoptera mauritia BOISD., and once there, it was mass-reared and releasedagainst Cirphis latuiscula H.S. and C. unipuncta HAW. E. platyhypenae was statedto have been established in all of the sugar-cane areas of Hawaii (MUlR & SWEZEY,1924, 1927). MATHUR (1942) reported the release of E. parvulus agai nst Plecopterareflexa in the Punjab, but no long term results of establishment and control were given.

We wish to thank the staff and students of the Entomology group of Tel Aviv University for theirhelp during this study. Special thanks are due to Mrs. R. COHEN and Mrs. R. SUZIN for the graphicillustrations, Mr. A. Shoub for the photography and to Mrs. T. ORtON for the histological preparations.

Rcvue biologique du genre Eupleclrus [Hym. Eulophidae] avec interet particulierpour E. laphygmae, parasite de Spodoplera lilforalis [Lep. Nocluidae]

L 'evolution et Ie comportement de Euplectrus laphygn;ae FERRI ERE ont ete etudies. Les parasitesparalysent les larves-hotes provisoirement avant 10. ponte d 'un ou deux a:ufs sur leur face dorsale.Le developpement de I'a:uf et de 10.chenille a lieu a I'emplacement de 10.ponte et de I'incubation dansun cocon de soie en-dessous de 10. chenille morte.

La duree du developpement est de ] 1,7 jours pour les deux sexes. Les a:ufs som attaches it 10.chenillepar un peoicule entre 10. cuticule et I'hypocerme. II pourrait subir des phenomenes mecaniques ainsique physiologiques.

Les parasites se nourrissent de larves-hotes mais ne pondent pas sur les memes larves. Toutes leschenilles piquees par les parasites meLII'ent sans aucun rapport avec la ponte ou Ie developpementd 'une larve-parasite au-dessus des hotes. On remarque un multiparasitisme des parasites internes deS. lilforalis. Une comparaison entre differentes especes d'Eupleclrus a ete etablie. lis comptent un grandnombre d'hotes Lepidopteres; cependant leurs caracteres biologiques sont tres semblables.

Euplectrus a ete tres peu utilise dans 10. lutte biologique contre les insectes nuisibles.

BISCHOFF, H. - 1929. Zur biologie der Euplectrus bicolor. - Swed Z. Wiss. Insektenbiologie, 24,78-82.BoucEK, Z. - 1970. Contribution to the knowledge of Italian Chalcidoidea, based mainly on a study,

at the Institute of Entomology in Turin, with descriptions of some new European species. -Mem. Soc. Entomol. Ital., 49, 35-102.

CHAIRMONTE, A. - 1933. Considerazioni entomologiche sullo. coltura delle pi ante do. frutto nellaSomalia Italiano.. - Agric. Colon., 27, 383-385. (Rev. Appl. El1Iomol., 21, 584, 1934).

CHATTERGEE, P. N. - 1945. On the biology and morphology of Euplectrus parvlllus FERR. [Hymenoptera,Eulophidae]. - Ind. J. Entomol., 6, 95-101.

CLAUSEN, C. P. - 1940. Entomophagous Insects. - McGraw-Hili, New York, 688 pp.

MATHUR, R. N. - 1942. On the biology of the shisham defoliators in the Punjab plantations. - Ind.For. Rec. (N.S.), 7, 9-65.

MUIR, F. & SWEZEY, O. H. - 1924. Entomology. - Reporl of Hawaiian Sugar Planters' Assoc. Exp.Stn., 25, 12-23.- 1927. Entomology. - Report of Hawaiian Sugar Planters' Assoc. Exp. Stn., 26, 16-29.

NEsER, S. - 1973. Biology and behavior of Ellplectrus species near laphygmae FERRI ERE (Hymenoptera:Eulophidae]. - Entol1lol. Mem. Depl. Agric. Tech. Serl'. SOlllh Africa, 32, 31 pp.

NOBLE, N. S. - 1938. Eupleclrus agaristae CROW. A parasitc of the grape vine moth. - Depl. Agric.New South Wales, 63, 5-27.

SILVESTRI, F. - 19] I. Contribuzioni alia conscenza degli insetti danosi elora simbionti. 11 PllIsiagamma - Boll. Lab. Zool. Gen. Agric. PO/·tici, 5, 308-311.

SMITH, R.C. _. 1927. Observations on EllpleClrus plalyhypenae a parasite of noctuid larvae. - Bull.Brooklyn El1Io 1110 I. Soc., 22, ] 28-134.

THOMSEN, M. - 1927. Some observations on the biology and anatomy of a cocoonmaking chalcidlarva, Ellplectrtls bicolor SWED. - Saerl. Vid. Medd. DansIe Nalllrh. Foren., 84, 73-90.

WELL, R. & BERBERET, R. C. - 1974. The life cycle of Ellpleclrlls plalyhypenae, a gregarious externalparasitoid of peanut foliage feeders in Oklahoma. - Environ. Enlomol., 3, 744-746.

WILSON, J. W. - 1933. The biology of parasites and predators of Laphygma exigua HB., reared duringthe season 1932. - Fla. Entomol., 17, 1-15.

ZIMIN, Yu. S. - 1930. On the biology of Euplectrus bicolor SWED. as a parasite of noctuid larvae. -Bull. W. Callcas. Plal1l Prot. Stn., 6-7, 99-106 (in Russian).

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Le prix de I'abonnement annuel est de 150 FF par volume de 4 fascicules(environ 450 pages) a souscrire pres de votre librairie ou directementpres de I'editeur :

which is the official periodical of the International Organization for BiologicalControl of noxious animals and plants (l.o.B.C.).

This scientific jou rnal founded in 1956 pu blishes origi nal papersdealing with fundamental or applied research, studies of systematics andbiology of natural enemies (parasites, predators, pathogens) which areor may be used in biological control.

Manuscripts are published in one of the following five languages:English, French, German, Italian. Spanish.

The subscription price is FF 150 per volume of 4 issues (ca 450 pages).Orders may be placed with your bookseller or directly with the publisher