AN ANNOTATED LIST OF HYMENOPTEROUS PARASITES

OF CITRUS SOFT SCALES IN ISRAEL*

BY

DAVID R O S E N

I. Introduction

Efforts have recently been made in Israel to integrate chemical and biological control methods of citrus pests. Any such programme of integrated control should take into account all the natural enomies of the pests ill question. A considerable amount of information on the enemies of citrus pests has been accumulated in Israel ( B O D E N H E I -

MER, 1951). tIowever, no systematic, country-wide survey of the parasites of these pests has ever been conducted, and very little has been added to their knowledge in recent years.

An extensive monthly survey was therefore started in the winter of 1960/1961. The survey covered the coastal plain, which is the main citrus growing region of Israel, and also the interior valleys. The various pests were brought into the laboratory, where parasites were reared from them. Occasionally the same pests were collected also on other host plants.

This work certainly would have not been able to proceed without the invaluable help rendered by Drs. Ch. FERttlI~RE, V. DELUCCHI and G. DOMENICtIINI of the C.I.L.B. and Mr. I-I. COMPERE of the Universi ty of California in kindly identifying many t tymenopterous specimens.

II. Host Insects

Of the soft scales (Hemiptera, Coccidae) four species are known as citrus pests in Israel. The most important of them is the Florida wax scale, Ceroplastes floridensis COW, ST. I t was found the whole year round. Being very rare on citrus in the Jordan valley, it was collected on ornamentals (Hedera Helix 5., Laurus nobilis n.) in tha t region.

* This invest igat ion was supported by a grant from the Citrus Market ing Board o[ Israel.

~-IgTOMOPIIAGA TOME VII~ N ~ ,{, 4 e TRIMESTRE I 9 6 2

3 5 0 DAVID ROSEN

The soft brown scale, Coccus hesperidum L., increased in high numbers at the beginning of the summer, but disappeared later - - presumably mainly through the action of parasites - - and reappeared in the autumn. I t was found occasionally on citrus in the Jordan valley, and was collected there on ornamentals.

The black scale, Saissetia oleae (BERN.), was found in many citrus groves in the coastal plain. I t develops apparent ly a single annual generation on citrus (HARPAZ, 1961), the first-instar larvae undergoing an aestivation period. On olive this pest seems to have a different annual cycle, and some parasite rearings were made from its populations on this host plant.

The fig wax scale, Ceroplastes rusci L., is rare on citrus, and was collected on rare occasions only.

III. Parasites

Following is a list of the species hitherto identified, along with some notes on their phenology and distribution in Israel (the dates pertain to collection of host insects).

Aphelinidae :

1. Coccophagus bivittatus COMPERE.

Coccophagus bivittatus COMPERE, 1931, Proc. U.S. Nat. Mus., 78 (% ~1.

Hos t : Coccus hesperidum L. This African species is very rare in Israel. A few specimens

were obtained in the northern coastal plain (Rosh Haniqra, III , V. 1961; Gesher ~aziv , III , V. 1961).

2. Coccophagus cowperi GIRAULT.

Coccophagus cowperi GIRAULT, 1917, Descriptiones Stellarum Novarum, p. 1.

Hosts: Coccus hesperidum L., Ceroplastcs floridensis COMST.

Females of this species were quite abundant ly reared from C. hesperidum populations. They seem to prefer dense colonies of the scale, but were obtained occasionally also from low infestations. This species seems to be the dominant among the Coccophagus spp. at tacking the soft brown scale in Israel. I t was reared from samples of this host collected throughout the coastal plain during December through June, and in the interior valleys (Geva, IV-VI. 1961; Kinne- reth, VIII . 1961, III . 1962).

Females of Coccophagus cowperi were twice reared from C. flori- densis in the coastal plain (Mikveh Israel, VIII . 1961; Ashqelon, IX.

PARASITES OF CITRUS SCALES IN ISRAEL 351

1961). This seems to indicate an alternate host in which the parasite might pass the summer in the absence of C. hesperidum.

Males of a Coccophagus species belonging to t.he lecanii group were very abundant in populations of C. hesperidum. Their identi ty has not yet been determined.

3. Coccophagus scutellaris (DALMAN).

Entedon scutellaris I)ALMAN, 1825, Svensk. vet. Akad. Handl., 46, 365.

Host: Coccus hesperidum L. BODENHEIMER (1951) considered this cosmopolitan species to be

a common parasite of C. hesperidum and C. floridensis in Palestine. In the present survey it was obtained only from C. hesperidum, on which it is less abundant than Coccophagus cowperi. I t was reared only from dense colonies of the host.

C. scutellaris was found in the coastal plain (Rehovot, II. 1961; Ashqelon, IV. 1961; Mikveh-Israel, V. 1961; Matsuva, VI. 1961), in the Jezreel valley (Geva, IV-VI. 1961), and on ornamentals in the Jordan valley (Gesher, VIII . 1961-III. 1962).

4. Marietta exitiosa COMPERE. Marietta exitiosa COMPERE, 1936, Univ. Califi Pub. Ent., 6

(12), 312. Hosts: Ceroplastes floridensis COMST., Saissetia oleae (BERN.).

This South-African hyperparasite is very rare in Israel. I t was reared once from C. floridensis collected in the Jezreel valley (2 ~ , 1 6, Geva, IX. 1961), and once from olive-infesting S. oleae in the southern coastal plain (1 ~, 1 6, Ein-Tsurim, XII . 1961).

5. Prospaltella sp. Hos t : Coccus hesperidum L.

Males of a Prospaltella species were reared from C. hesperidum during April through June 1961. They were found in the coastal plain (Rosh-Haniqra, Kabri, Matsuva, Ashqelon), and in the interior valleys (Geva, Heftsiba), bu t quite rarely. They are certainly less abundant than the species of Coccophagus.

Ency rtidae :

6. Bothriophryne fuscicornis COMPERE. Bothriophryne ]uscicornis COMPERE, 1989, Bull. Ent. Res.,

30 (1), 21. Host: Ceroplastes floridensis COMST.

This Afriean parasite was reared in small numbers during Sep- tember and October 1961. I t was found throughout the coastal

352 DAVID ROSEN

plain and in the western Jezreel valley, but is apparent ly of little economic importance.

7. Che i loneurus paral ia (WALKER).

Encyrtus paralia WALKER, 1837, Ent. Mag., 4, 446.

Hosts: Coccus hesperidum L., Ceroplastes floridensis COMST.

This species was reared during May and June, 1961 from C. hespe- ridum throughout the coastal plain. I t is generally rare, and only once were more than a few specimens reared (Kfar-Bilu, VI. 1961). Occasionally it was obtained also from C. floridensis (Tirah, IX. 1961; Ra 'anana, IX. 1961; Kfar Hess, IX, X. 1961). The species is believed to be hyperparasitic.

8. Divers inervus elegans SILVESTRI.

Divcrsinervus elegans SILVESTRI, 1914, Boll. Lab. Zool. Portici, 9, 303-305.

t[osts: Saissctia oleac (BERN.), Ccroplastcs floridensis COMST.

This species was reared by RIVNAY (1944) from C. floridensis and by BODENIIEIMER (1951) from C. hesperidum. BODENHEIMER stated tha t it was rarc in Palcstine.

In the prcsent survcy D. clegans was repeatedly reared from its typical host, S. oleae, of which it seems to be the most important parasite in Israel. I t seems to dcvclop on citrus the whole year round, as it was obtained from S. oleac collected from May through August, and from C. floridensis collected from August through December. I t was obtained from olive-infesting S. olcae also during Ju ly through January .

D. elegans occurs in many localities in the coastal plain. Though reared many times from C. floridensis it is not an important parasite of this pest in Israel. C. floridensis seems to serve as an alternate host, when susceptible stages of the preferred host - - S. oleae - - are absent on citrus.

9. Encyr tus l ecan iorum (MAYR),

Comys lecaniorum MAYR, 1875, Verh. Zool. Bot. Ges., Wien, 740-741.

Host: Coccus hesperidum L.

RIVNAY (1944) and BODENHEIMER (1951) considered this species to be the most abundant , and apparently the dominant, parasite of C. hesperidum. In the present survey it was obtained only 9 times,

PARASITES OF CITRUS SCALES IN ISRAEL 353

and rarely were there more than single specimens reared. I t seems to be now of very little economic importance.

E. lecaniorum was found in the coastal plain, especially north of Acre, and also in Geva, Jezreel valley. Emergence occurred during all seasons.

10. Metaphycus flavus (HOWARD).

.4phycus flavus HOWARD, 1881, Rep. Ent. U.S. Dept. Agric., p. 365.

Hosts: Coccus hesperidum L., Saissetia oleae (BERN.). This parasite was reared by RIVNAY (1944) from C. hesperidum,

bu t was then very rare. In the present survey it was obtained more than any other parasite of this pest, and seems to be the first of impor- tance among its parasites. I t has an apparent ly excellent searching capacity: it was obtained even from extremely sparse populations of the scale, when only few scales could be detected in an orchard.

M. flavus was reared from C. hesperidum populations collected throughout the coastal plain from November through Augalst. The host could not bc found on citrus in the coastal plain during September and October, but it seems certain tha t M. ]tavus is able to survive in citrus orchards also during these months, on sporadic scales.

In tile interior valleys the species was obtained whenever C. hespe- ridum was found to infest citrus, or ornamentals, the whole year round.

Only once was a single female reared from a larva of S. oleae (Kfar ]3ilu, II. 1962).

11. Metaphycus zebratus MERCET.

Aphycus (Mctaphycus) zebratus MERCET, 1916, Bol. Soc. Esp. Hist. Nat., 16, 138.

Host: Ceroplastcs floridensis co~sT. This species, or a form very close to it, is very rare in Israel.

Only 4 rearings have been recorded, all of them through September and October, 1961. The parasite was found in the northern coastal plain (2 ~ , Kabri, IX. 1961; 1 ~, Kabri, X. 1961; 1 ~, 1 ~, Nahariya, IX. 1961) and in the Jezreel valley (4 ~ , 3 c~c~, Geva, IX. 1961).

12. Microterys frontatus (MERCET). Encyrtus [rontatus MERCET, 1921, Himenopteros, Fam. Encir-

tidos, Mus. Nac. Cien. Nat., Madrid, pp. 413-415. Hosts: Coccus hesperidum L., Ceroplastes floridensis COMST.

This species was reported by RIVNAY (1944) from the southern par t of the coastal plain of Palestine. In the present survey it was

3 5 4 DAVID ROSEN

found throughout the coastal plain and in the interior valleys. M. ]rontatus is very abundant , and was obtained the whole year

round. I t seems to prefer C. hesperidum as a host, and is second only to Metaphycus [lavus on it. I t was found in sparse populations of this scale, as well as in dense colonies. C. ~oridensis serves as an alternate host, and is parasitized to a much lower extent than C. hesperidum, but still M. ]rontatus is one of its more important parasites.

In the coastal plain of Israel this species was obtained from C. hesperidum collected during November through August, and from C. l~oridensis collected during April through October. In the interior valleys it was reared from C. hesperidum collected on citrus during March and April, and on Hedera Helix during October to February. I t was once obtained from C. ]toridensis in the western Jezreel valley (Mishmar t ta 'emeq, X. 1961).

13. Microterys sp.

Hosts: Coccus hesperidum L., Ceroplastes floridensis COMST. Males of a Microterys spccics were reared during May and June

1961 from C. hesperidum collected in the coastal plain. In the absence of females, the species could not be determined. They were generally rare, and only occasionally were obtained in considerable numbers (Kfar Bilu, VI. 1961).

Males of seemingly the same specics were reared on 2 occasions from C. floridensis collectcd in the coastal plain (Ra'anana, IX. 1961; Kfar Hcss, X. 1961).

Eulophidae:

14. Tetrast ichus spp.

Hosts: Ceroplastes floridensis COMST., Ceroplastes rusci L., Coccus hesperidum L.

At least three species of Tetrastichus were reared from soft scales during the present survey. Their ident i ty has not been determined yet, and therefore they will be dealt with here together.

Tetrastichus spp. were the most common parasites reared from C. ]~oridensis, and on many occasions were the only parasites obtained from populations of this scale. They were reared from this host throughout the coastal plain the whole year round. Two specimens were obtained in the Jezreel valley (Geva, XI. 1961 ; Mishmar I-Ia'emeq, XII . 1961).

Specimens of Tetrastichus spp. were obtained also from C. rusci, collected occasionally on citrus in the northern coastal plain (Kabri, I I I . 1961; Gesher I-Iaziv, XI. 1961).

RIVNAY (1944) mentioned a Tetrastichus sp. tha t was obtained

PARASITES OF CITRUS SCALES IN ISRAEL ~55

from C. hesperidum. In the present survey one female was recorded from this host (Kabri, VI. 1961).

A further s tudy is needed to determine the relationship between these abundant parasites and the soft scales.

P t e r o m a l i d a e :

15. Pachyneuron s i cu lum DELUCCHI.

Pachyneuron siculum DELt:CCHI, 1955, Z. ang. Ent., 38, 135. Host: Coccus hesperidum L.

Dr. DELUCCHI examined some of our specimens and designated them as Pachyneuron pr. siculum, observing that they are probably the true siculum, but this is difficult to establish without comparison with the type (DELuCCHI, 1961, personal communication).

This species, which is possibly hyperparasitic, was obtained from C. hesperidum throughout the coastal plain during May, June and July. I t was occasionally reared in considerable numbers.

A single male was obtained from the Jezreel valley (Geva, IV. 1961).

16. Scutel l is ta cyanea MOTSCH.

Scutellista cyanea MOTSCHULSKY, 1859, Etud. Entom., 8, 171- 173.

Hosts: Ceroplastes floridensis COMST., Saissetia oleae (BERN.), Ceroplastes rusci L.

The first to record this well-known egg-predator and eetoparasite from Israel was apparent ly George CO~PERE, who found it at Jaffa (SMITH & COMPERE, 1928). BODENHEIMER (1951) listed the three above-mentioned hosts, as well as Saissetia hemisphaerica (TARG.) and Coccus hesperidum L. as hosts of this parasite in Israel.

In the present survey, S. cyanea was obtained from C. floridensis ha the coastal plain the whole year round. I t is certainly the most abundant parasite of this pest in Israel, with the exception of Tetrasti- chus spp. In the interior valleys it was reared from C. floridensis collected on citrus and ornamentals during July, Augalst and September.

S. cyanea was reared from Saissetia oleae collected on citrus during June and July, and on olive also during November, December and January . I t seems to be an important parasite of this pest, though less abundant than the Diversinervus.

Many specimens of S. cyanea were obtained from a sample of C. rusci collected on a fig tree near Jerusalem (Ein Karem, VIII . 1961, Leg. I. IYARPAZ).

The typical, clear-winged form is dominant in Israel. Scutellista

356 DAVID ROSEN

cyanea obscurata SILVESTRI (1914, Boll. Lab. Zool., Port ici , 9, 240-334) was ob ta ined v e r y r a re ly f rom C. floridensis (Gan Y av n eh , VII . 1961; Ashqelon , X. 1961). Many specimens of this v a r i e t y were found a mong the S. cyanea t h a t were reared f rom the above -men t ioned sample of C. rusci.

IV. Conclusion

The paras i tes ob t a ined f rom the var ious soft scales in the presen t su rvey are l is ted below according to the i r re la t ive abundance .

HOST PARASITES

Ceroplastes floridensis (CO~IST.) Tetrastichus spp. Scutellista cyanea MOTSEHULSKY lVlicroterys frontatus (MERC~T) Diversinervus elegans SILVESTRI Bothriophryne fuscicornis COMPERE Metaphycus zebratus MERCET Cheiloneurus paralia (WALKER) Coccophagus cowperi GIBAULT ~Iicroterys sp. ~'Vlarietta exitiosa COMI'ERE

Coccus hesperidum i,.

Saissetia oleae (BERN.)

Ceroplastes rusci L.

Metaphycus flavus (aOWAaD) l~/Iicroterys frontatus (MERCET) Coccophagus cowperi 6mAULT Pachyneuron siculum DEr.trccm Coccophagus scutellaris (DALMAN) Cheiloneurus paralia (WALKER) Encyrtus lecaniorum (~IAYB) Prospaltella sp. Microterys sp. Coccophagus bivittatus COMPERE Tetrastichus sp.

Diversinervus elegans SILVESTRI Scutellista cyanea MOTSCHULSKY Marietta exitiosa COMPERE Metaphycus flavus (HOWARD)

Scutellista cyanea MOTSCHULSKY Tetrastichus spp.

C. hesperidum was paras i t ized to a v e r y high degree, especially a t the beginning of the summer . Paras i t i za t ion of C. floridensis was neve r so high, a t t a in ing its peak a t the beginning of the summer and fall ing sharp ly dur ing the winter . Mature females of S. oleae were para- si t ized to a considerable ex t en t a t the beginning of the summer , b u t a lmos t no paras i tes were ob ta ined f rom developing larvae.

Two genera, n a m e l y Bothriophryne COMPERE and Mariet ta ~OT-

PARASITES OF CITRUS SCALES IN ISRAEL 357

SCHULSKY, are recorded here for the first t ime from Israel. Seven species and one var ie ty are new to the fauna of Israel. These are: Bothriophryne ]uscicornis COMPERE, Cheiloneurus paralia (WALKER), Coccophagus bivittatus COMPERE, Coccophagus cowperi GIRAULT, Marietta exitiosa COMPERE, Metaphycus zebratus ~.RCET, Pachyneuron siculum DELUCCHI, and Scutellista cyanea obscurata SlLVESTRI.

Considerable changes must have taken place in the populations of Coccidophagous parasites on citrus in Israel during the last twenty years or so. The most impor tant of these seem to be as follows: Metaphycus flavus and Tetrastiehus spp., which were apparent ly of no economic importance, have risen recently to a dominant position. Encyrtus lecaniorum, which was considered to be first of importance among the parasites of the soft brown scale, is now rare and of no economic value. Diversinervus elegans is here recorded for the first t ime from the black scale, and it seems to be the most impor tant para- site of this pest.

A C K N O W L E D G E M E N T S

T h e a u t h o r is g ra te fu l to Prof . Z. AVIDOV, u n d e r whose gu idance t h i s work was done , a n d to Dr . I. ttARPAZ for r e ad ing t h e m a n u s c r i p t a n d offering m a n y he lp fu l suggest ions .

T h a n k s are l ikewise due to t h e s taff of t h e A g r o t e c h n i c a l Div is ion of t h e Ci t rus M a r k e t i n g B o a r d of Israel , a n d i ts D i r ec to r Agr. I . CO~IEN, for t h e i r k i n d co-opera t ion .

T h e t e c h n i c a l a ss i s t ance of Mr. A. KON~:N is also g ra t e fu l ly acknowledged .

R~SUM~

U n e enqu~te en tomolog ique effectu6e sur t o u t lc t e r r i t o i r e d ' I s ra~ l nous a p c r m i s : 1 ~ de d o n n e r une l is te des H y m ~ n o p t 6 r e s pa r a s i t e s des cocheni l les de la fami l le des Coccidae des Ci t rus ; 2 ~ de pr~ciser leur phonolog ic e t leur d i s t r i bu t i on .

N o u s avons a ins i o b t c n u 11 esp6ces de Coccus hesper idum L., 10 de Cero- plastes f lor idensis COMST., 4 de Saissct ia olcar ( B E R N . ) , et 2 de Ceroplastes 7usci L. 2 genres , 7 esp6ces e t 1 var i6 t6 son t n o u v e a u x d a n s ]a f aune d ' Is ra~l . I1 semble que des c h a n g e m e n t s cons id6rablcs on t cu l ieu dans la f a u n e des pa ra s i t e s des cochcni l les des Ci t rus d ' I s ra~l dcpuis les p u b l i c a t i o n s de RIVNAY e t de BOI)EN- HEIMER.

B I B L I O G R A P H Y

BODENHEIMER, F. S. - - t951. Citrus entomology in the Middle East. - - ~V. Junk , The Hague, 663 p.

HAaPAZ, I. - - 1961. Coccoidea, p. 126-175. In Z. AvlDOV, Pests o[ the cu l t iva tedp lan t s of Israel. - - The Magnes Press, Jerusalem.

RIVNAY, E. - - 194~. The economic s ta tus of Coccus hesperidum L. and its parasi tes in Palestine. - - J. Ent. Soc. S. Africa, 7, 73-8t.

SMITH, n . S. & H. COMPERE. - - 1928. A prel iminary report on the insect parasites of the black scale, Saissetia oleae (nERNARD). - - Univ. Calif. Pub. Ent., 4 (9), 231-33/~.

(The Hebrew University, Faculty o/Agriculture, Rehovot, Israel.)