ENTO,~IOPHAGA, I8 (3), I973, ~I~-~22

SYSTEMATICS, MORPHOLOGY

AND BIOLOGICAL CONTROL (*)

BY

David ROSEN (1) & Paul DEBacH (2)

(t) The Hebrew University, Faculty of Agriculture, Rehovot, Israel (2) Division of Biological Control, University of California, Riverside, U.S.A.

Accurate systematics is the foundation on which all meaningful research in biology is based. The importance of sound systematics to practical biological control is illustrated by results from several projects on biological control of coccid pests. Correct identification of the pest species or their natural enemies, and reco- gnition of cryptic species or infraspeeific entities, have been of utmost importance to the success of many projects.

Accurate morphology is the basis of reliable systematics. Unfortunately, basic morphology of the parasitic Hymenoptera is still imperfectly understood and that which is known often is inadequately used. The scanning electron microscope is a valuable tool for comparative morphological research that will go far toward solving these problems. The taxonomic validity of morphological characters, and the extent of intraspecific variation, should be determined by a detailed'biometrical study of large series of cultured specimens whenever possible. This approach is illustrated with results obtained in our recent revision of the species of Aphytis, important parasites of diaspine scale insects. Comparative morphology of develop- mental stages of parasitic Ilymenoptera is recognized as an important approach to the study of cryptic species needing much more emphasis.

Accurate systematics is the basis on which all meaningful research in biology is based. In the words of the late F. S. BODENII~cr~ER (1959) : " I t is essential that every zoologist - - and certainly every ecologist - - acquire good knowledge of some special animal group, no mat te r how small. Any inquiry into a branch of biology can be reliably conducted only on the basis of accurate taxonomy... Basic taxonomic information on any group gives the biologist the Dos moi po sto of A~CHI~IEDES, the point from which he may manipulate the lever for any biological problem. A zoologist is definitely not a man who does not know any animal."

Sound Systematies is especially important to the success of bio- logical control projects. When" natural enemies are being sought or are transferred from one region to another in order to bring about

(*) This pape r is a cont r ibu t ion of the IBP project on Biological Control of Armored Scale Insects . Financial suppo r t was furnished by NSF grants GB-74&4 and GB-17829.

216 D. ROSEN ~5 P. DEBACtt

biological control of an arthropod pest, the correct identification of both pest and natural enemy species and the recognition of cryptic species or infraspecific entities may, of course, be of utmost importance. This has been illustrated time and again by the failures or successes of projects aimed at the biological control of many serious pests. We shall restrict this discussion to our field of speciality - - biological control of coccid pests. Needless to say, these illustrations apply broadly to the entire field of biological control.

Correct identification of the pest species

This is of supreme importance in biological control. A survey of successful projects in biological control shows that most effective natural enemies either are virtually monophagous or only narrowly oligophagous. When established exotic pest species are misidentified the search will be conducted for natural enemies of the wrong host or prey insect with the result tha t these natural enemies, if at all specific, will probably fail to become established in the new habitat . Time and efforts of biological control workers have thus often: be6~iuselessly wasted due to inadequate systematic knowledge ~ f ~ ~ s t species. Unfortunately, popular j udgemen t in such eases is likely to be that biological control has been tried and failed.

Inabil i ty to distinguish between etosely related pest species was o n e of the main causes of repeated early failures in efforts to achieve biological control of the California red scale, Aonidiella aura~tii (MASKELL) (Homoptera: Diaspididae), in California. Ear ly in the present century, several a t tempts were made to introduce natural enemies of tha t serious pest of citrus from the Far Eas t into California. However, yellow scale, Aonidiella citrina (CoQuILImTT), and various other species of Aonidiella were at that time misidentified as California red scale, and their parasites repeatedly failed to become established in California because they were not adapted to that pest. These repeated importat ion failures led to the commonly held erroneous conclusion in the 1930's tha t no effective parasites of California red scale were present in the Orient. 0 nly after a thorough taxonomic revision by ~[cKENzlE (1937) provided the means for correct identification of California red scale, were researchers eventually able to discover effective parasites of tha t pest in the Far Eas t (CoMPERE, 1961; :Dv.BACH, ROSEN & KENNETT, 1971).

Adequate systematics may help in directing biological control workers to the area of origin of a pest. Thus, the misclassification of California red scale as a species of Chrysomphalus, a genus once believed to be of South American origin, misdirected the at tent ion of researchers toward that continent. A futile search for natural enemies was conducted in South America in 1934-1935, resulting in

~IORPHOLOGY AND BIOLOGICAL CONTROL 217"

yet another waste of effort. Only after California red scale was correctly recognized as a species of Aonididla, a genus of Oriental origin, was attention focused again on the Far East, where efficient natural enemies were indeed present and eventually discovered and imported.

Another demonstration of the crucial importance of correct speci- fic identification of an insect pest was provided by the successful biolo- gical control of the coffee mealybug, Planococcus kenyae (L]~ P]gLLEY} (Ilomoptera ." Pseudococcidae), in Kenya. That serious pest apparently invaded Kenya about 1923, spread rapidly and caused severe damage to coffee and various native food crops. It was at first misidentified as the citrus mealybug, Planococcus citri (RIsso), then as the cacao mealybug, Planococcus lilacinus (Coc~:]~F, LL), and numerous unsuccess- ful attempts were made to control it by the introduction of predators and parasites of those species from four different continents. One whole year was spent on a fruitless search through the Pacific area. Only after the pest was correctly identified as an undescribed species, known only from East Africa, was a search for its parasites conducted in neighboling Uganda and Tanganyika. Several effective parasites of the coffee mealybug were then discovered and introduced into Kenya with resulting completely sueeessfnl control of the pest (LE PEL~.EY, 1943).

Correct identification of natural enemies

This is as essential to the success of biological control projects as correct identification of the pest. Some good examples are furnished by eetoparasites of the genus Aphytis (Hymenoptera: Aphelinidae) which are generally by far the most effective natural enemies of armored scale insects (Homoptera: Diaspididae). Unfortunately, specific identification of these minute aphelinid wasps is extremely difficult even to today's skilled specialist. A few years ago misiden- tifieation was probably the rule rather than the exception. As a mat ter of fact, potential success in the biological control of California red scale in California was delayed for over half a century, because various species of Aphytis attacking that pest in the Orient were misidentified as A. chrysomphali (MERCET), a relatively inefficient parasite already present in California. For several decades repeated at tempts were made to discover and import endoparasites of the pest, whereas species of Aphytie were largely ignored or, ironically, actually eliminated from cultures as unwanted contaminants. The present two most efficient natural enemies of California red scale, A. lingnanensis COMPETE and A. melinus DF~BAcH, were not recognized as distinct species until 194,8 and 1956, respectively, and were then

218 D. ROSEN & P. DEBACH

successfully introduced from the Orient into California, and sub- sequently also into other countries (RosEN & DEBAcH, 1973).

Another species of Aphytis may serve as a further example. A. holoxanthus DEBaclI, currently known as the most efficient natural enemy of Florida red scale, Chrysomphalus aonidum (L.), was appa- rently first reared from that host near the turn of the century, bu t was then forgotten due to its misidentification as another species. Many years later, that important parasite was introduced into Israel against the Florida red scale under the assumption that it was a form of A.flngnanensis that a t tacked that scale. I t soon brought about complete biological control of Florida red scale. Its true identity was subsequent ly revealed in a biosystematic s tudy carried out as late as 1960. Needless to say, this effective weapon might have been available in the arsenal of biological control for decades, had it been recognized as a distinct species much earlier (DEBACH, 1960; DEBACH, ROSEN & KENNETT, 1971).

Cryptic or sibling species of natural enemies may play an important role in biological control, and their recognit.ion on biological grounds may provide the key to ultimate success. Thus, outstanding success in the biological control of the olive scale, Parlatoria oleae (CoLv~E), was achieved in California when a so-called "biparental strain" of Aphytis maculicornis (~L~sl) --apparently a sibling species- intro- duced from Iran, was recognized as biologically distinct from several other morphologically indistinguishable "strains", imported from other countries. When released in California, the "Persian Aphytis" soon became a major factor in the control of that serious pest of olive and deciduous fruit trees (DEBACH, ROSEX & K_ENNETT, 1971). Obviously, "biological control workers should never consider, a priori, t h a t two similarly appearing populations in different geographical areas represent the same species... I t is bet ter to err on the safe side, than it is to fail to import a natural enemy because it is considered to be already present" (I)EBAcH, 1969).

The role of the taxonomist is not limited to the early exploratory stages of a biological control project. Lack of taxonomic awareness among economic entomologists may lead to inexcusable failure of otherwise promising projects. ~[ass cultures of natural enemies, especially minute parasitic t tymenoptera , may be readily contami- nated by unwanted species. Unless continuous collaboration with a taxonomist is maintained, such contamination may n o t be noticed for long periods. This apparently happened in the intensive project of biological control of San J o s e scale, Quadraspidiotus perniciosus (CoMsTOCK) (Homoptera: Diaspididae) in Europe. Mass cultures of an imported parasite, Prospaltella per~dciosi Tow>m (Hymenoptera: Aphelinidae), were apparent ly invaded in Germany by a related, ineffective species, P. /asciata ?VlaL~NOTTI, which however was the

MORPHOLOGY AND BIOLOGICAL CONTROL 219

most effective under insectary conditions. Some four million indi- viduals of P. /asciata were mistakenly released as P. perniciosi in the Ileidelberg region during 1956-58, before the true identity of the species was determined by taxonomists. P. /asciata never became established in Germany (Ros]~N & DEBAcH, 1973).

Finally, collaboration with a taxonomist may be an absolute necessity also during the post-colonization stages of a biological control project. Correct identification of natural enemies is obviously necessary in order to ascertain their establishment and progress in a new habitat and to assign credit where credit is due. Several years ago we imported Aphytis hispanicus (M~CET) into California and colonized it in an incipient outbreak of the newly invading chaff scale, Parlatoria pergandii COMSTOCK. A year or so later the scale was reduced to very low levels by Aphytis activity and A. hispanicus was credited with the victory. I t was not until a year or so later tha t detailed microscopic comparisons revealed tha t A. hispanicus was not even established and tha t the control had resulted from the fortuitous establishment of a very similar appearing species - - a form of A. maculicornis. To this day we do not know the origin of this form because hybridization tests show it to be distinct although indistinguishable from the Persian A. maculicornis also present in California. This is the first record of a form of A. maculicornis from the chaff scale and this makes another species available for use against the chaff scale elsewhere.

Morphology as the main basis for taxonomic research

Ever since the advent of the so-called "new systematics", most taxonomists have been more or less aware of the importance of biosystematics and the need to recognize biological differences between closely related entities. This need is all the more apparent in applied biological control. As pointed out by DzBicH (1969), "from the standpoint of practical biological control, we are vitally interested in whether natural enemies differ from one another, regardless of our ability to tell them apart morphologically. All grades of specific or sub-specific genetically based difference may be important" . Never- theless, for obvious practical reasons, most taxonomic research still has to rely upon the morphological s tudy of dead, preserved specimens. Not many entomologists are in the position to maintain cultures of several to many species. Sound morphology therefore is, and is likely to remain, an essential part of any systematic investigation. Thus, "in applied biological control, sound planning depends in many cases on systematics tha t reflect phylogenetic relationships. The planning may be no more sound than the systematics on which it is based. In turn, the systematics may be no more sound than the morphology

2 2 0 D. R O S E N & P. D E B A C H

on which it is based" (Co~PERE & ROSEN, 1970). Yet, in spite of the obvious need for a firm morphological foundation, scarcely more than a beginning has been made in a comparative morphological study of even such highly important groups as the parasitic Hymenop- tera.

Adequate equipment is, of course, essential for reliable morpho- logical research. Unfortunately, until relatively recently, researchers had to contend with generally poor optical equipment, and knowledge of arthropod morphology was therefore often inadequate. With the introduction of improved equipment and the adoption of more sophisti- cated procedures for the preparation of specimens for microscopic examination, the quali ty of morphological research has been greatly improved. Whereas in the past taxonomic research was usually confined to the examination of dry, pinned specimens under a low- power stereoscopic microscope, taxonomists are now able to s tudy cleared, dissected, slide-mounted specimens under the high-power phase-contras t microscope, with far better results even without staining. Even more important, the recent advent of the scanning electron microscope has placed a powerful, revolutionary toel in the hands of morphologists and has opened new dimensions for systematic research. The nature and detailed structure of minute organs are now being discovered, and new morphological characters are being recognized, thus enabling the taxonomist to separate closely-related species on the basis of better, more accurate morphological criteria.

However, no technique is free of its problems and inherent dangers, and scanning electron microscopy is no exception. For various techni- cal reasons, it is much easier to concentrate on a detailed s tudy of a few specimens, ra ther than to conduct a comparative s tudy of numerous individuals. Thus, the scanning electron microscope, with its unsur- passed clarity even at very high magnifications, may tend to overem- phasize individual rather than specific differences.

INTRA-SPECIIr VARIATION. - - Researchers adhering to the "classical", typological approach to taxonomy have often paid very little at tention to intra-specific variation in morphological characters. As a result, specimens exhibiting insignificant variations of s tructure or coloration have often been inadvertent ly described as distinct species, whereas valid diagnostic characters have been overlooked. Any serious taxonomic study of a group of living organisms should be preceded whenever possible by a comparative biometrical investi- gation of large series of cultured specimens which are known for certain to belong to one species,, in order to determine the extent of intra-specific variation and evaluate the validity of diagnostic characters used for the separation of species. With better understan- ding of intra-specific variation, more so-called cryptic or sibling species will eventually be separated on a reliable morphological basis.

MORPIIOLOGY AND BIOLOGICAL CONTP~OL 221.

In a yet unpublished revision of the genus Aphytis, conducted recently by the authors, a detailed study of intra-speeific variation in several species has revealed that some of the characters that had been commonly used in classification, such as the number and relative length of certain setae, tend to vary considerably with the size of specimens , hence are of l i t t le d iagnost ic value, iV[inure spec imens h a v e a longer marg ina l fr inge on the forewing and fewer se tae on t h e m a r g i n a l vein and m e s o c u t u m t h a n do la rger spec imens of the s ame species. On the o the r hand, a s table, va l id c h a r a c t e r such as t h e p a t t e r n of p i g m e n t a t i o n was of ten ignored in the pas t . Numerous . species of Aphytis had to be redefined, and severa l h a v e been recogn ized as new, on t h a t basis.

ID:ENTIFICATION OF DEV]BLOPlYlENTAL ST.~_G:ES. - - Recogn i t ion o f differences be tween a n y g iven d e v e l o p m e n t a l s tage of na tu r a l enemies m a y be of g rea t p rac t ica l i m p o r t a n c e in biological contro l pro jec ts . F ie ld-col lec ted samples of pests usua l ly con ta in some d e v e l o p m e n t a l s tages of n a t u r a l enemies, and it is o f ten r a t h e r difficult to rea r t h e m to m a t u r i t y in the l abo ra to ry . Yet , a l t hough the d e v e l o p m e n t a l s tages of n u m e r o u s species h a v e been occas ional ly descr ibed (CLAuSEN, 19~0), r e l a t ive ly li t t le use has so fa r been m a d e of such i n fo rma t ion in the ac tua l ident i f ica t ion of c ryp t i c specics. The sys t ema t i c s o f paras i t i c t t y m e n o p t e r a , for ins tance, is a lmos t en t i re ly based on morpho log ica l charac ter i s t ics of adu l t wasps . P u p a l p i g m e n t a t i o n has been used to some ex t en t for the d e t e r m i n a t i o n of cer ta in species of Aphytis (I)EBAcH, 1959). A c o m p a r a t i v e mprpholog ica l s t u d y o f l a rva l and pupa l charac te r s of paras i t ic H y m e n o p t e r a m a y p rov ide new tools for the separa t ion of c ryp t i c species in t h a t difficult b u t economica l ly i m p o r t a n t group.

R]~SUM]~

Syst~matique, morphologie et lutte biologique Une syst~matique precise constitue la base de toute recherche valable en

biologic. L'importance de solides connaissances en systdmatique pour la raise en oeuvre de la lutte biologique est illustr~e par les r~sultats de plusieurs projets concernant ta lutte biologique contre des cochenilles nuisibles. Une identification correcte des ravageurs et de leurs ennemis naturels, ainsi que la reconnaissance d'esp~ces occultes ou d'entit~s infrasp~cifiques, ont ~t~ d'une extreme importance pour le succ~s de beaucoup de ces projets.

La connaissance exacte de la morphologie est le fondement d'une syst~ma- fique sdrieuse. Malheureusement la morphologie des Hym~nopt~res parasites est encore imparfaitement connue et ce qu'on en connait est souvent real utilis~. Le microscope ~lectronique k balayage est un appareil prdcieux pour les ~tudes de morphologie compar~e qui permettra de grands progr~s dans la solution de ces probl~mes. La valeur taxonomique des caract~res morphologiques et l'~tendue de la variation intrasp~cifique peuvent ~tre d~termin~es par une ~tude biom~trique d~taill~e d'une grande s~rie de specimens d'~levage, ehaque fois que e'est possible.

222 D. ROSEN ~ P. DEBACH

Les r~sul ta ts ob tenus au cours de no t re r6eente r~vision des esp~ces d'Aphytis, paras i tes des Diaspines , en sont une i l lustrat ion. La morphologie compar~e des diff~rents s tades de ddve loppement des Hym~nopt~res paras i tes appa ra i t ~tre une i m p o r t a n t e voie d'acc~s h l '6 tude d 'esp~ees occultes, qui d eman d e ~ 8tre b e a u c o u p plus d~velopp~e.

REFERENCES

BODENtIEIMER, F . S . - - 1959. A biologist in Israel. - - Biological Studies, Publn., Jerusalem, 492 pp.

CLAUSEN, C .P . - - 1940. Entomophagous Insects. - - McGraw Hill, New York & London, 688 pp.

COMPERE, H . - - t96 t . The red scale and its insect enemies. - - Hilgardia, 31, 173-272. COMPERE, H. & ROSEN, D. - - 1970. The prescutum in Hymenoptera . - - Proc. roy.

ent. Soc. Lond. (A)., 45, 9t-97. DEBAcH, P. - - 1959. New species and strains of Aphytis [Hymenoptera, Eulophidae]

parasitic on the California red scale) Aonidiella aurantii (M~s K.), in the Orient. - - Ann. ent. Soc. Am., 52, 354-362. - - t960. The importance of t axonomy to biological control as il lustrated by the cryptic history of Aphytis holoxanthus n. sp. [Hymenoptera : Aphelinidae], a parasite of Chrysomphahts aonidum, and Aphytis coheni n. sp., a parasite of Aonidiella aurantii. - - Ann. ent. Soc. Am.., 53, 70t-705. - - 1969. Uniparental, sibling and semi-species in relation to taxonomy and biological control. - - Israel J. Ent., 4, i i -28.

DEBAc~I, P., ROSEN, D. & K E N N E T T , C. E. - - 1971. Biological control of coccids by introduced natural enemies. Chapter 7. In : Biological Control (C. B. HUFFAKER, ed.). - - Plenum Press, New York & London, pp. 165-194.

LE PELLEY, R . H . - - 1943. The biological control of a mealy bug on coffee and other crops in Kenya. - - Empire J. exp. Agric., 11, 78-88.

~[cKE~XZlE, H . L . - - 1937. Morphological differences distinguishing California red scale, yellow scale, and related species. - - Univ. Calif. Publn. Ent., 6, 323-336.

RosEr~, D. & DEBAcH, P. - - 1973. Diaspididae. In : Introduced Parasites and Predators of Arthropod Pests and Weeds : A World Review (C. P. CLAUSEr% ed.). - - U.S. Dept. Agric. (In press).