Proc. Indian Acad. Sci. (Anirn. Sci.), Vol. 96, No. 5, September 1987, pp. 587-611.

(D Printed in India.

Biosystematics of Tingidae on the basis of the biology and micro­morphology of their eggs*

DA YID LIYINGSTONE and M H S YACOOBDivision of Entomology, Bharathiar University, Coimbatore 641 046, India

Abstract. The biology and micromorphology of the eggs of 40 species belonging to 26genera and two subfamilies of Tingidae from southern India have been studied andconsidered for an assessment of their biosystematics. The oviposition strategy is intimatelycorrelated with the selection of oviposition site on the host plant, determined by the shapeand size of the egg and accomplished by appropriately developed ovipositing mechanisminvolving the structural features of the first gonapophyses. The oviposition pattern isaccordingly classified and the eggs are classified on the basis of the nature of development ofthe chorionic collar cum opercular apparatus. Characterization of the eggs and assessmentof their systematic importance ha ve been linked with the origin and evolution of adaptiveradiation of oviposition strategies of their egg parasitoids as well. Production of seasonoriented dimorphic eggs is common among species that oviposit their long operculate eggsvertically in clusters, either into stems or rachis or pistil. Lamina ovipositors preferentiallyoviposit into the mesophyll horizontally. without cluster formation, on the undersurface ofthe leaves and the significant reduction in the number of aeropyles of such oval, shortoperculate eggs could be correlated with thc abundance of oxygen supply of the ambient air.More elongate, long operculate eggs in Tingidae, characterized by their multiplicity ofaeropyles and vertical oviposition in clusters into stems, rachis and pistil, signifyprimitiveness, as observed in Cantacaderinae and some large sized Tinginae, Micropyles areabsent in tingid eggs, as fertilization occurs before chorion formation and a truespermatheca is wanting.

Keywords. Tingidae; oviposition strategies; opercular diversities; evolutionary trend;biosystematics.

I. Introduction

The pioneering contribution of Southwood (1956) on the classification of TerrestrialHeteroptera on the basis of egg structure and the classic monograph of Cobben(1968) on the evolutionary trends in Heteroptera on the basis of the micromorpho­logy of the eggs, continue to challenge those who try to venture on the biosystema­tics of any particular family of Heteroptera. Unfortunately, the posthumouslypublished 3 volume treatise of Hinton (198 I) on the biology of the insect eggs, but forthe third volume comprising of the bibliography, has nothing substantial to offer onthe biology of the eggs of Heteroptera. Nevertheless, the contributions of Salkeld(1972) and Haridass (1985a, b, 1986a, b) on the ultrastructure of reduviid eggs haveenormously enhanced the scope of future attempts on the biosystematics of Cimico­morpha in general on the basis of the biology and micromorphology of their eggs.

The Tingidae, constituting a minor family of Heteroptera, ever since Johnson(1936) published the first elaborate account of the biology of the Rhododendron lacebug. Leptobvcrsa rhododendri, has been steadily registering its importance as a

'Contribution No. 44.

SR7

588 David Livingstone and M H S Yacoob

weed control agent, as a potential vector of coconut wilt and as a rare example offloral gallmaker. The biology and micromorphology of the eggs of Tingidae has beenconsidered in specific cases of biological studies, attempted by Roonwal (1952) onTeleonemia scrupulosa: Stusak (1961, 1968), on Monanthia symphyti; M. rotundata;Acalypta marginata; A. parvula; A. corynata; Elasmotropis testacea: Catoplatus

[abricit; Physatocheila dumetorum; Deryphysia foliacea; D. catoplatus; Tinqisauriculata; T. reticulata and T. stachydis, Livingstcne (1959, 1962a, b, 1967a, 1968,1976) on Urent ius euonymus; M onosteira minutula; Cadmilos retiarius; Tinqisbuddleiae and Dasytingis rudis and Livingstone and his eo-workers (Livingstone et al1981; Livingstone and Yacoob 1983a, b, 1986) on Pontanus puerilis, Agramma spp.and A. hupehanum. The more recent publications of Yaccoob and Livingstone (1983)and Livingstone and Yacoob (1983a, b, 1986) on the egg Parasitoids of a miscellanyof Tingidae of southern India provide adequate informations for placing emphasison the biology of the eggs as a significant aspect of biosystematics. In the presentpaper, the micromorphology and biology of the eggs of 40 species of Tingidaebelonging to 26 genera and two subfamilies of southern India provide the bases forassessing the biosystematics of this family.

2. Oviposition site selection and oviposition strategy

Tingidae are by and large species specific in their host selection (Livingstone 1977).They feed and oviposit on the same host plant. But each species selects its ownoviposition site and accordingly their strategies of oviposition vary. All species ofsouthern India whose biologies are known are multivoltine. Even the exotic speciesT. scrupulosa, the Lantana lace bug, which is known to be bivoltine in northern India(Khan 1945; Roonwal 1952), is multivoltine in southern India, breeding all round theyear, producing more than 12 generations (Livingstone et al 1980). Most Europeanspecies of tingids are known to be bivoltine (Drake and Ruhoff 1965). The Britishthistle lace bugs, Tinqis ampliata and T. cardui are reported to be univoltine.However, their overwintering phenomenon is not well understood (Eguagie 1972a, b,1973, 1974a, b).

All the 4 known species of the subfamily Vianaidinae are reported to bemyrmecophilous and but for a meagre fragmentary information on the micromorpho­logy of the ovariolar egg of one species (Cobben 1968) their biologies are not known.The gallicolous species of Copium and Paracopium are anthophagous and theyoviposit into the corolla by rotating their eggs in their oviduct at 180°, so that whileovipositing, the operculum could be directed to the interior of the flower bud. Thenymphs that hatch enter the space beneath the corolla and make the monothalamusfloral cecidium (Darke and Davis 1960; Darke and Ruhoff 1965). This uniquerotatory mechanism of the eggs in these bugs is not even vaguely understood fromthe reports of Fischer (1956), Monad and Carayon (1958), Abraham and Abraham(1971) and Jaeger (1976).

Specificity in oviposition site selection on the host plant is strongly indicated asrevealed in table 1 and the manner of oviposition is determined by the ovipositionsite. as indicated in table 2. The manner of oviposition is further indicated by thespecialization of the ovipositor (figure 5). Such specializations become species specificand such an explorative study provides valuable information on the biosysternatics,

Biosystematics of Tinqidae 589

inter-specific relationships and adaptive radiation of this or any other group ofinsects.

2.1 Lamina oviposition

Depending on the thickness and architecture of the lamina or the calyx, the eggs areinserted either parallel (horizontal) to the leaf surface as in all the grass tingids suchas Aconchus urbanus, Agramma spp. and other monocot tingids such as Stephanitisspp. or slantingly into the mesophyll as in the majority of lamina ovipositing species(figure 3J). The degree of obliquity is directly related to the relative thickness of thelamina. Tingids of the verbenaceous plants tend to insert their eggs near to verticalposition, similar to those that insert their eggs into stems and pistils. Horizontaldeposition in monocot lamina invariably occurs in between parallel veins.

In lamina oviposition, since the eggs are inserted into the substance of [he leaf, theupper and lower epidermis turn transparent, and the site of oviposition becomesdechlorophylled, betraying the presence of the egg. All the lamina depositors showvarying degrees of preference to specific sites such as dorsal surface, ventral surface,leaf margin and leaf tips (table I) and majority of them prefer the ventral surface, forsafety and protection from direct exposure to sun light. It has also the advantage ofthe safety of the nymphs from predators and from being directly exposed toinsecticides. The first gonapophysis of the lamina ovipositors can be readilyrecognized by the arrangement of serrations, especially in the grass tingids, forfacilitating insertion into the flaccid blades (figure 5 J-Nl.

2.2 Rachis/petiole/vein oviposition

Considerable variations occur in the degree of obliquity of oviposition, depending onthe thickness of the substrate. When the eggs are deposited into the midrib they arecloser to vertical insertion as in Pontanus puerilis (figure 3G) and Perissonemiaecmeles (figure 3E).

2.3 Floral parts oviposition

There is specificity in the selection of floral parts also. C. retiarius selects the calyx(Livingstone 1962b). D. rudis (Livingstone 1976), D. semota and Ammianus ravanusspecifically select tender pistil and oviposit in clusters of 3-8 eggs. The eggs hatchbefore the pistil matures since mature fruits always carry shells .01' hatched eggs.

2.4 Stem oviposition

This is characteristically found in C. bullita, inserting its eggs vertically in batches ofmore than IQ eggs per batch into the tender stems of Ocimum spp. Laminaoviposition is also not uncommon in this species, as reported by Samuel (1939) andSharga (1953). Phatnoma costalis alone has been found ovipositing exclusively intothe tender stems of Hibiscus. In C. retiarius, a polyphagous species of north Indiahas Helianthus as its primary host in which it oviposits on the sepals and lamina. But

V1

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Site

ofeg

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posi

tion

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Flo

ral

.... 0D

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ter

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gid

spec

ies

surf

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surf

ace

tipm

argi

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veno

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sC

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Pist

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:

Aco

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2;:A

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mm

aq

ram

inii

-+

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AiJ

ram

ma

hupe

hanu

m-

+-

++

-::z:

:A

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tin

qi:

p/u

lllu

elii

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+-

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C/J

AlI

llllia

llu.l

raV

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l.l-

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lI1Ii/

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++

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ry/l

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0-

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Cys

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Biosystematics of Tinqidae

1 + 1

1 + 1

591

I + I

1 + I + + 1

I + 1

1 + I

1 ++++11+1

1 +

+ + 1

+++1++1

1 + 1

1 + + 1 + + + +

1+++1++1++1+

1++11+11+11+

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+++1 +++ 11+++++++++++

1 + 1 1 + +

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592 David Livingstone and M H S Yacoob

Table 2. Mode of egg deposition in Tingidae.

Solitary

ACO/lclllls urbanusAqramma qraminii

Aqramma hupelw/11ImCoryrhauma ayyariCysteochila jatensisDusytinqis rudisDasytinqis semotaDictyla karnaticaDulinius conchatusHabrochila laetaHaedus qrewiiHaedus yacobiiLasiacancha justiciaiiLasiacantha peristrophiiLasiacant ha ruelliiNaochila minulaPerissonemia ecmelesPhatnoma costalisPhaenotropis cleopatraAmmianus ravanusPhysatocheila asiaticaPoncanus puerilisStephanitis cinnamomiiStephanitis charieisSuphanitis macranchaiiStephanitis typicaTeleonemia scrupulosaTinqis tomentosiiUrentius euonymusUrentius hystricellus

Batches

Cochlochila bullita (30)Dusytinois rudis (3-6)Dasytinqis sp.mota (3-5)Duiinius conchatlls (2-3)Eteoneus cinchonii (5-10)Lasiacantha peristrophii (2-3)Ammianus ravanus (2-5)Physatocheilu asiatica (2-3)Perissonemia ecmeles (2--4)POll/anus pueriiis (2-4)

Cork formation

Corythauma ayyariDusytinqis rudisDas)'lingis semotaEteoneus cinchoniiPhatnoma costalisAmmianus raranusPoncanus puerilisSteplJanitis cinnamomiiStephanitis macranthaiiStephanitis typicaTeleonemia scrupulosaTinqis tomentosiiUrentius euonymusUrentius hvstricellus

Smearing of faecal matter

Corythauma qibbossaDietyla karnaticaHabrochila laetaNaochila minutaPhaenotropis cleopatraStephanitis t ypicuStephanitis cinnamomii

during rainy season it oviposits also into the tender stems of other selected annuals(Livingstone 1962b). Dictyla karnatica also has been observed to oviposit in thetender stems as well as lamina.

2.5 Comments

In the case of lamina deposition, the operculum of the egg remains in flush with thesurface whereas in the other types where the eggs are inserted vertically,perpendicular to the surface, the operculum and part of the neck of the eggs stick outat varying heights, especially in the case of the long operculate eggs of P. ecmeles,D. rudis, D. semota, A. ravanus, P. puerilis, Eteoneus cinqonii, T. scrupulosa and C.bullita.

Southwood (1956) recognized 4 types of oviposition in Heteroptera-{i) exposed,(ii) semi embedded. (iii) embedded in dead plants and (iv) embedded in live planttissue. Later, Cobben (1968) summarised these 4 types into (i) lateral superficial,(ii) embedded position and (iii) upright position. He considered the first type as themost general method of oviposition in Heteroptera and the upright vertical placingof ~ggs has been regarded as the most economical spatial usuage of substrate. This is

Biosystematics of Tinqidae 593

often indicated in cluster or clutch formation, as characteristically found in the pistiland stem deposition types in Tingidae and all such eggs are invariably long operculateand elongate. The first gonapophysis of the pistil. stem and rachis depositors aremore elongate and spike like with minute serrations facilitating oviposition of suchelongate eggs in clusters by piercing the tender substrate (figure 50-R).

Vertical oviposition in clusters is associated with parental care (Cobben 1968) andin Tingidae only in C. bullita, in which maximum number of eggs per cluster ofvertically deposited eggs in the stem has been found, the females are observedperiodically inspecting (guarding) the eggs.

Vertical oviposition and cluster formation are considered as indications ofprimitiveness, an approach towards formation of ootheca and according to Cobben(1968) more advanced type of egg deposition is indicated by eggs being depositedsingly, slantingly and haphazardly. It was also suggested that a shift from horizontalto vertical position allows greater dependence on atmospheric air and escape fromparasitoids and predators. In Tingidae, though the upright position may rendergreater dependence on atmospheric air it may not render them any immunity againstparasitoid attack, since the egg parasitoids have been observed to oviposit throughthe operculum and parasitisation of eggs occurs irrespective of the position ofoviposition (Livingstone and Yacoob 1986).

Smearing of faecal matter around the exposed opercular surface of the depositedegg, as reported in Leptoypha mutica (Dickerson and Weiss 1916) and Dictyle stiff/ate(Livingstone 1962b) occurs in a number of species (table 2). It appears to be a featurecharacteristic to the lamina ovipositing genera Dietylu and Naochila. Such smearingserves as a sealing device, protecting the egq;s from desiccation and damping but notas a deterrent against parasitcids. It can be readily washed away with water. Thoughfungus does not attack the material smeared around freshly deposited eggs, there is adense growth of fungus around the site of oviposition, after the eggs are hatched.

Cork formation around the oviposited eggs (figure 3H) by the plant tissue byreacting with the secretory material of either accessory gland or oviduct, ischaracteristically met with in long operculate eggs, oviposited either vertically orslantingly into stems, pistil and rachis and in a few lamina ovipositors such asCorythauma ayyari, Stephanitis spp. and Urentius spp. In the case of P. ecmelesspecialized warty concrescences (figure 4S) have been observed at the concave(dorsal) surface at the collar base. Such materials are found to have been spread onthe leaf surface serving as anchoring device as in the case of chorionic serrationsreported in P. puerilis (figure SA) (Livingstone et al 1981) as well as in Haedusyacoobii (figure 5B).

Since oviposition site selection is species specific, such a specificity is indicated bythe specialized development of the ovipositor. Thus a lamina ovipositor is recognizedby the highly serrated, broad blade like ovipositor and the pistil, rachis and stemovipositor is recognized by the much elongate, sharply pointed, finely serrated spikelike ovipositor. Morphometric analysis by Livingstone and Yacoob (1986) on theeggs of 23 species of Tingidae and their egg parasitoids iLathromeromvia (L.) tinqi­phaqa; Erythmelus empoascae; Epolygosita (E) duliniae, Lathromeromyia sp. andParallellaptera polyphaqas has provided evidence of variations in the length of theovipositor of these parasitoids (figure 5 H, l) determined by the relative height of thechorionic collar cum opercular apparatus. It is an example of reproductive poly­morphism (ecotypic/biotypic) of a parasitoid species being determined by the height

594 David Livingstone and M H S Yacoob

of the chorionic collar of the eggs of a wide range of host species, throwing challengeto a biosystematist. A mastery over species determination on the basis of morpho­logical characters therefore is recognized as a necessary adjunct to its biosystematics,placing the sovereignty of taxonomy and integrity of the taxonomist in a highlyexalted position.

3. Micromorphology of the eggs

Tingid eggs are known from the accounts of Heidmann (1911), Steer (1929) andLeston (1954). Ovariolar eggs as well as oviposited eggs extricated from the planttissues were mounted in cavity slides either directly in polyvenyl lactophenol orsoftened in 5% KOH for an hour and cleared in cellosolve (2-ethoxy ethanol) beforemounting. Since it is difficult to extricate eggs from grass, the blades carrying eggs(figure 3J) were treated in 5% KOH for a few hours and cleared in cellosolve andmounted. Treated eggs were dissected in lactic acid and mounted in pieces in DPXfor micromorphological studies.

The tingid egg (figure I) is clearly divisible into the body, the chorionic collar andthe operculum.

3.1 Body of the egg

The body of the egg is invariably smooth, the hexagonal sculpturations not verydistinct, with rare exceptions such as H aedus spp. In P. puerilis (figure 5A) aridH. yacoobii (figure 5B) the neck region, mostly along the indented side, for a shortdistance, develops posteriorly directed serrations which according to Livingstone(1976) enable the egg to gain firm grip inside the plant tissue. Such serrations havebeen reported in the inner surface of the exochorion of T. buddleiae also, which hasbeen explained to serve the function of gripping the endochorion which is likely to bepulled out at eclosion and in that event eclosion will not be possible (Livingstone1967a). In the case of P. ecmeles, the occurrence of warty materials at the neck region,mostly on the indented surface, is significant. With a few exceptions, the chorion islight yellowish and in the case of C. bullita, D. karnatica and P. cleopatra even theovariolar eggs are darkly pigmented. The caudal end of the eggs is rounded in stemand pistil depositors (figure 3P) whereas in most of the lamina depositors it isslightly oblong, permitting easy penetration into the mesophyll (figure 3L).

3.2 The chorionic collar

The chorionic rim is the cephalic end of the body of the egg and the chorionic collaris defined as the extension of the cephalic end of the egg beyond the chorionic rim.The junction of the two is the mouth of the egg (figure I), beyond which the endo­chorion does not extend. Therefore, the chorionic collar (,limbus chorioni' of Stusak1961 and 'rim collar' of Cobben 1968) is essentially an extension of the exochorionbeyond the mouth of the egg, circumscribing it, as well as the operculum that formsits lid. The chorionic collar is invariably a spongy. reticulate mesh work, traversed bythe aeropyles and the height of the collar varies considerably in different species. The

Biosystematics of Tingidae

Acanchus urbanus

:r ••. • _•• . • ... .~

595

- - · • • _Ie

Staphanit is chari~iJ

...... . -...

-----Ie

Pontanus p-uarilis

Cochlochila bull it a

Figure l. Types of collar-operculum (diagrammatic).

height of the collar is invariably correlated with the height of the opercular crest, butthe collar, though intimately associated with the opercular crest, does not fuse as iscommonly reported in similar type of eggs of harpactorine reduviids (Cobben 1968;Salkeld 1972; Haridass 1986a). On the basis of the nature of development of thecollar cum operculum, tingid eggs could be classified as follows.

3.2a Short spongy type: Typically, the chorionic collar here is reduced as areticulate (spongy) lining of the chorionic rim and the operculum remaining as a lid(figure 3L) without any outgrowth. This type is characteristically found in the eggs ofall grass tingids and in all the other lamina ovipositing species the collar, thoughshort, shows different grades of development (table 3). The collar is also plain andspongy as in all the grass tingids as well as C. ayyari: Dulinius conchatus, D. karnatica,Phaenotropis cleopatra, Stephanitis macranthaii and both species of Urentius. It isfinely punctate in all species of Haedus and Laciacantha justiciaii (figure 58). Theaeropyles open to the exterior at the junction of the collar lining and the chorionicrim.

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Tab

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Egg

sof

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(ill

mm

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spec

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32

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80

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598 Daoid Lioinqstone and M H S Yacoob

3.2b Elongate reticulate type: The collar, when elongated, is invariably diffe­rentiated into a basal, more tough and punctate region that gradually differen­tiates apically into a more elaborate, reticulate and more brittle region which getseasily mutilated at the slightest touch. This apical brittle region corresponds to theproblemmatic structureless tissue (Roonwal 1952), net work region (Southwood andScudder 1956a, b), spongy region (Livingstone 1962a, b, 1967b, 1976) and gas con­taining mesh work (Hinton 1981). The aeropyles develop apically as definite numberof shallow grooves along the reticulate region of the collar and as they proceedbasally the grooves become deeper and narrower at the punctate region. As theyenter the chorionic rim they become tubes (figure SF) formed in between the endo­chorion and exochorion.

3.2c Elonqately frilled type: The chorionic collar is elongately divided into adefinite number of filamentous frills of reticulate texture. It is characteristicallydeveloped in C. bullita, T. scrupulosa (figure 50) and P. ecmeles (figure 3F). InC. bullita each frill filament is fusiform, the middle enlarged region is dark, punctateand slightly bulged outward, appearing as circular dark band of the collar (figure5C). Apically, each frill filament is punctate and an aeropyle in each frill filament ischaracteristically found. In T. scrupulosa, each frill filament is uniformly reticulatethroughout its length and the aeropyles characteristically develop, one in betweentwo frill filaments (figure 50) as grooves along the basal reticulate region of thecollar. In P. ecmeles, the reticulate apical region of the collar is more elongate andfrilled and the frill filaments are often found spread out conspicuously (figure 3F)exposing the long collumn of the operculum sticking out from the centre of the egg.In freshly laid eggs the frill filaments are held together enveloping the collumn (figure3E). The aeropyles develop from the reticulate basal region of the collar below thelevel of the frills (figure 4S).

3.2d The fringe type: The collar, along with the opercular flange, rolls back onitself circumscribing the chorionic rim (figure 1). This type is characteristically foundin all species of Stephanitis.. In S. cinnamomii and S. macranthaii the fringe thusformed is compactly invested with the cork that is formed around this region alone(figure 31). The aeropyles that develop on the collar also follow its course andtherefore remain curved.

3.3 Operculum

The operculum, forming the lid of the mouth of the egg and being sealed at the baseof the chorionic rim by the membrane commonly known as the sealing bar, protectthe egg from desiccation and rotting. The operculum can be distinctly described as aplate ('discus operculi' of Stusak 1961) that develops around its rim posteriorly aflange called the sealing bar and on its outer surface it may either be smooth or maydevelop certain outgrowths. While the sealing bar is consistent in its struc­ture, the outgrowths vary in their structure from species to species. These out­growths when developed around the rim (periphery) as elongate reticulate tube(figure 3 N-R), is designated as the anterior flange or collumn ('limbus operculi' ofStusak 1968) and when the plate on its outer (anterior) surface develops similar

Biosystematics of Tinqidae 599

outgrowths, circumscribed by the collumn, such outgrowths remain as central reti­culate pillar, designated as columella (figure 4T). When the columella and thecollumn are clearly defined, the latter as an outer tube circumscribing the former asthe reticulate pillar and both together remaining perceptibly elongate, such an egg isdescribed as long operculate egg. When such outgrowths are not well defined theyare described as short operculate eggs. Long operculate eggs invariably have equallyelongate collar and when both the collumn and the collar are juxtaposed, as in thecase of most of the long operculate eggs, they jointly function as efficient air store.When the collumn and the columella are relatively short and both together remaininseparably fused, it is called opercular crest. On the basis of the relative develop­ment of the outgrowths of the opercular plate on its exterior, the eggs of Tingidae areclassified as given below.

3.3a Short operculate type: This type constitutes the majority of the eggs examinedand with a very few exceptions such as C. bullita and P. costalis, all are depositedeither in the rachis or petiole or lamina. Here, the operculum is characterized by ashort anterior flange (corresponding position of the collumn of the long operculateeggs) traversed by definite number of canals. This flange may be smooth in all grasstingids (figure 4A) and in a few other lamina ovipositors such as Urentius spp. In allspecies of Stephanitis (figure 4F), P. costalia (figure 4N) and in all species ofLasiacantha (figure 4C), the flange is highly reticulose and remains juxtaposed withthe corresponding collar. In S. cinnamomii (figure 4G) the flange is lobulated.

The outer surface of the opercular plate may also show varying degrees of deve­lopment of sculpturations in the short operculate eggs.

3.3b Smooth or plain plate: The entire surface is smooth as in all species of Aqramma(figure 4A) or a few rows of hexagonal calls may border it as in A. urbanus, Afrotinqisphanuelii; Belenus dentatus; D. conchatus and Lasiacantha spp. (figure 4D).

3.3c Sculptured plate: The entire outer surface of the plate is distinctly puncturedby hexagonal sculpturations, as seen in Urantius spp. (figure 4E). N aochila nigra,Agramma spp., C. ayyari, C. qibbosa, Lasiacantha ruelii, P. cleopatra and Stephanitiscinnamomii. The outermost whorl of sculpturations are more conspicuous as indi­cation of differential sclerotization of the plate.

3.3d Tuberculate plate: Each hexagon of the plate develops either hairy outgrowthsas in Tinqis tomentosii (figure 4N), P. costa lis, Physatocheila asiatica and Cysteochilajavensis (figure 40) or certain central hexagons develop digitate tubercularoutgrowths as in L. justiciaii and Stephanitis charieis (figure 4H). In the former casethese outgrowths camouflage with the tomentose surface of the lamina and make thedetection of the eggs at the oviposition site difficult.

3.3e Crested plate: The outgrowths from the plate (both flange and columella) asreticulate meshwork, form a compact crest or crown, often traversed by definitenumber of longitudinal grooves, comparable to the 'Prolatio disci' of Stusak (1961,1968). In Haedus qrewii (figure 4M), Abdastartus atrus, D. karnatica and T. scrupulosa(figure 4P) the crest is in the form of meshwork with the grooves running along theperiphery. These grooves however, do not open into the interior but since the collar

600 David Livingstone and M H S Yacoob

also is closely juxtaposed with the crest, these grooves remain associated with thecorresponding grooves of the collar in the formation of the aeropyles. Stusak (1961,1968) in Tingis st achydis and several other species described the tubes of the crest tobe communicating with one another at the base of the crest but not opening into theegg. The number of grooves present on the crest approximates the number of aero­pylar grooves of the collar. Thus the grooves on the opercular crest, by their position,are formed on the anterior flange developed from the rim of the opercular plate andthe main mass of the reticulate mesh work of the crest is formed from the body of theplate and therefore the flange corresponds to the collumn and the mesh work to thecolumella of the long operculate eggs. Livingstone (1962b), while describing similaropercular crest in C. retiarius, suggested that this structural feature of the crest is anadaptation for humidity regulation. During rainy season the crest appears distendedexposing fully the peripheral grooves while during drought it remains collapsed,shrunkan and hard.

All the 4 species of Haedus present 4 different types of opercular crest. In the caseof Haedus ruthii (figure 4L) and H. manii, the crest like a crown of hexagonal cellswith the chorionic collar encrusting at its base. In H. qrewii (figure 4K) the crestreveals the peripheral grooves of the flange. An unique type of opercular crest amongTingidae has been found in H. yacoohi. Here, the columella is drawn out in the formof a compactly formed hook and the collumn (flange) with the grooves forming thebase around it (figure 5B).

The more reticulate type of opercular crest of T. scrupulosa, C. hill/ita and D. kar­natica appears intermediate between short and long operculate types, correspondingstructure has been termed as 'prolatio disci' by Stusak (1961, 1968) in lVI. symphvti.

3.3f Long operculate type: It is characteristically found in all those eggs with tallchorionic collar. They include A. racanus, D. rudis, D. semota, P. acmeles and P. pue­rilis. In Eteoneus cinchouii it is moderately elongate as in T. scrupulosa, but structu­rally both are different. By circumscribing the elongate collumn of the operculum,the chorionic collar encloses a periopercular space (figure I). In the case of D. rudis,D. semota, A. raranus and P. puerilis the collumn circumscribes the columella as aperiopercular cylinder (Livingstone 1976) almost up to the tip and throughout itslength it establishes, at regular intervals, transverse septal connections with the latter,as indicated externally by the ribs (figure 4T). By this, a honeycomb pattern of airstore is thus established.

The columella is not clearly defined in P. ecmeles (figure 4S) and in E. cinchonii(figure 4R). In the latter, both the collumn and the columella together expandapically and remain transparent. In all these long operculate eggs, especially inP. ecmeles, the collumn is narrow, often constricted basally (figure 4S) thus increa­sing the area of the periopercular space.

In P. puerilis, D. rudis and D. semota it has been observed that the operculum andthe collar together are variable in height, exhibiting seasonal dimorphism(Livingstone et al 1981). The eggs oviposited during February are short operculateand those oviposited during October are long operculate. Both types of eggs areinserted vertically, but the former is less exposed, being more deeply buried in thetissue than the latter. Dissections of gravid females of these insects reveal (figure 3C)that the eggs that are ovulated earlier are invariably long operculate whereas those

Biosystematics of Tinqidae 601

ovulated subsequently are consequentially short operculate. Consequently, the eggsthat are ovipusited at the termination of oviposition cycle are always short opercu­late, thus presenting a typical example of dimorphic eggs. However, the relevance ofthe production of such dimorphic eggs by these multivoltine species needs furtherinvestigation.

The long operculate eggs of Tingidae are comparable to the eggs of Harpacto­rinae, the chorionic collar of the former and the vail of the latter exhibiting structuraland functional similarities. Both have well established periopercular space andcomparable opercular elements. In both the cases, eggs are oviposited vertically inclusters. Whereas, in Harpactorinae they are glued to the substratum (leaves, barks.stones and soil) by means of the spumaline secreted by the subrectal glands (Cobben1968; Hinton 1981), the tingids bury their eggs into the plant tissue and for thatreason the ovipositor of Tingidae, especially their first gonapophyses, are moreelongate and variously serrated. In Harpactorinae and in all other subfamilies ofReduviidae shortening of gonapophysis is characterised. Though the paired acce­ssory glands are well formed in these tingid species the characteristic cork formationaround the inserted egg into the plant tissue due to reaction with the secretedmaterial, necessitates further confirmatory evidences.

3.4 Respiratory apparatus

The close juxtaposition of the collar and the opercular flange (collumn), whether highor low, creates an efficient air storing mesh work and the development of the colu­mella from the plate in the crested and long operculate eggs enhances the efficacy ofthe air storing device, comparable to the plastron of the eggs of terrestrial Hetero­ptera (Hinton 1981). The creation of the periopercular space in the long operculateeggs, comparable to the 'long double walled respiratory cylinder with fine reticula­tions' of Cobben (1968), further increases the area of air storage.

Subsequent to the report documented by Carayon (1954) that tingid eggs werefertilized after chorion formation, Southwood (1956) by his cobalt injection techni­que concluded that the canals that are established by the juxtaposition of exochorionand operculum were micropyles. Later, Stausak (1961, 1968) further emphasised thatall the canals of the reticulate collar were micropyles. According to Bearnent's (1946)definition, all canals that do not have definite opening to the exterior are'pseudornicropyles', corresponding to the 'Leukart's canals' which are respiratory infunction. The 'true micropy1es' according to him have definite opening to the exteriorand therefore they alone are responsible for sperm transport. The pseudomicropylesare in fact the aeropyles opening into the ;:;:''' containing meshwork (Hinton 1981) orthe aerostatic layer (Cobben 1968) of the exochorion and gaseous exchange with theambient air is accomplished by these canals. When the periopercular space is presentit maintains communication with the ambient air. The fact that the grooves of theopercular flange (collumn) do not communicate with the egg but associated with thecorresponding grooves of the collar to form definite canals at the chorionic rim,confirms the formation of aeropyles by the juxtaposition of the collar and flange.

In Tingidae, Cobben (1968) reported to have observed both aeropyles and micro­pyles. One of the criteria for classification of Terrestrial Heteroptera was the

602 David Liuinqstone and M H S Yacoob

functional organization of these two canal systems and Southwood (1956) includedTingidae under Cimicomorpha as he considered that both aeropyles and micropylesare present as independent functional entities in their eggs. Hinton (1981) contendedthat all species of tingids have two micropyles, one on either side (right and left) inall, except in Cantacader infuscata in which the two are arranged close to each otheron the ventral side.

A micropyle is recognized from the aeropyle by its sharp curve beneath the inner. surface of the shell, to open more anteriorly in the shell. In the aberrent myrmeco­philous tingid, Anommatocoris, a few aeropyles also have been reported to curve intothe air containing mesh work in a similar fashion as the micropyles (Cobben 1968).But none of these authors have recognized a distinct opening of the so called micro­pyle to the exterior at the chorionic rim. Southwood and Scudder (1956a, b) andStusak (1961,1968) considered all the visible canals as micropyles and for that reasonthey failed to recognize any aeropyle in the eggs of a number of species of tingidsthey examined.

A close examination of the chorionic architecture, collar and operculum of all the40 species of Tingidae examined does not provide any conclusive evidence of theexistence of a canal identical to the micropyle. It is also conclusively established thatthe curvature of the tube as a diagnostic feature of micropyle is not only arbitrarybut also not tenable in Tingidae, since curvature of aeropyles is met withinAnommatocoris as well as in almost all the long operculate eggs (figure 5F).

True micropyles are reported to be absent in Anthocoridae and Cimicidae and inthese two families fertilization took place before chorion formation (Cobben 1968).Livingstone (1967a, b) provided histological evidences in favour of fertilization takingplace in Tingidae before chorion formation. In T. buddleiae he has confirmed thatthe paired accessory gland opening into the bursa does not receive sperms, as againstthe pseudospermatica notion maintained by several workers (Carayon 1950;Southwood 1956; Pendargrast 1957; Draka and Davis 1960) and that the sper­matozoa in this polygamous insect are received first in the expanded region of thetwo lateral oviducts that act as 'primary receptaculum semenis' and from thence theyare transported to all the 7 pedicels on each side that act as 7 'accessory spermreservoirs'. Similar histological evidence has been provided by sections of theovarioles of Habrochila laeta also (figure 3D). Whenever sperms are found either inthe pedicels or in the oviducts, the follicular epithelium of the basal oocytes, havingclear ooplasm, are found to have not even initiated vitellogenesis. This may also leadto the suggestion that the entire physiology of vitellogenesis and chorion formation,occur as a succession of events following fertilization. Earlier, Kullenburg (1946,1947) reported that in mirids sperms are stored in the pedicels much earlier to theformation of chorion. Miridae are known to be closely related to Tingidae in severalrespects especially in the biology of their eggs (Darke and Davis 1960; Cobben 1968).

Regarding the nature of the aeropyles, considerable variations exist in Tingidae.Branching of the aeropyles inside the egg has been reported in L. rhododendri(Johnson 1936) and T. scrupulosa (Roonwal 1952). Such branching has beenconsidered as 'extension canals' by Livingstone (1976) in D. rudis and by Livingstoneet al (1981) in P. puerilis. They are in fact extension grooves (figure 5F) and notcanals. In A. rupanus also they are present but not in P. ecmeles. Therefore, suchextension canals commonly occur among long operculate eggs. However, theaccessory reservoir on the chorionic rim as part of the aeropyle, as reported in

Biosystematics of Tingidae 603

T. buddieiae by Livingstone (196 7a), has been traced only in T. tomentosii, suggestingthat this is a characteristic feature of the genus Tinqis.

Variations in the length of the aeropyles in an egg itself in the long operculate eggshave been reported in D. rudis (Livingstone 1976) and P. puerilis (Livingstone et at1981), the more elongate principal aeropyles (APP) reaching almost the full length ofthe collar and the short accessory aeropyles (A PA) stopping at the basal punctateregion of the collar. But in the aerostatic layer of the chorion both short and longaeropyles show the usual curvature.

The number of aeropyles vary considerably in tingid eggs (figure 2) and issignificantly numerous in the long operculate eggs. In the short operculate eggs theyare less than 20 and in all the grass tingids they are significantly not more than 6, notdistributed at equidistance around the chorionic rim, as they are in most otherspecies. It is also significant that in most of the long operculate eggs the aeropyles arearranged in groups of 3-6. In T. scrupulosa and C. bullita their number correspond tothe number of collar frill filaments.

In Tingidae the aeropyles in all the species, whether with or without extensiongrooves, terminate in the aerostatic layer inside the egg shell.

3.5 Sealing bar

The term sealing bar, representing the posterior flange of the opercular plate, that

S.NO TlNGIO SPECIES 5NUMBER OF AEROPVLES

10 15 20 lS )0 35

1,~Qlrus -

2 I~~ -·3 I Agramma grominii -4 I Agramma hupel'lanum -I5 · Atrotingis phanuelii -6

,~~ --I

7 I Bel.nus~ -,8 ~bullitQ -9

,CorythQuma~ -,

10 ,Corythouma gibboua -,

11 I Cysteochila JQvensis -12 · Dasytingis~ -I13 Oosylingis semoto --'4 Ql;!I!.g karngticQ -15 ~ conchctus --'6 Eteoneus cinchonii -17 Ha,brochila~ -18 ~~ -'9 ,~~ -20 Haedu5 ruthl! -21 : Ha.dus yacobii -22 I LQsiacantha justiciai! -23 : La siocantha perlstrophii -24

·~ruellii -

25 : NaochilQ~ -26 I ~~ -27 : Perissonemia ecmeln -28 : ~costalis --29 : Physalocheila osiotice -30 Phaenotropis c1eopqtra -31 : ~pUltrili5 -32 Stephanitis~ -33 Stephanitis ,innamomii - I34 : 51ephanitis mac(Qnthaii . I35 , Stephanitis~ -36

I I!!!9!!~ -37 ·~ scrupulosa --38 UrentiU5 euonymus -39

IUr.ntiu5 Iwstrieellus -,

Figure 2. Eggs of Tingjdae-c-nume rica] distribution of aeropyles.

604 David Liuinqstone and M H S Yacoob

o

seals the plate to the base of the chorionic rim, was first coined by Beament (1946)and subsequently by Southwood (1956) and Southwood and Scudder (1956a, b). InTingidae, Stusak (1961, 1968) described the sealing bar to be composed of twocomponents, the opercular posterior flange proper named as 'basis operculi' and thechorionic component named as the 'claustrum'. At the time of eclosion, theoperculum along with the basis operculi has been reported to snap off from theclaustrum. Roonwal (1952) and Livingstone (1967a, b, 1976) indicated a line ofweakness or suture, corresponding to the junction of the 'basis operculi' and

Biosystematics of Tingidae 605

Figure 4. Operculum of a few selected species of Tingidae. A. A. hupehanum. B. U. euo­nymus. C. Lasiacantha peristrophii. D. L. justiciaii. E. Urentius hvstricellus. F. Ste­phanitis typica. G. S. cinnamomii. H. S. cherieis. I. L. ruellii. J. S. macranthaii. K. C.ayyari. L. H. ruthii. M. H. qrewii. N. T. tomentosii. O. C. [avensis. P. T. seru­pulosa. Q. P. asiatica. R. E. cinchonii. S. P. ecmeles with the warty concrescences atthe neck. T. A. ravanus with the columella protruding.

'claustrum' of Stusak. In all the 40 species of Tingidae examined, the sealing bar(figure 1) has been found to be the fusion product of the posterior flange of theopercular plate with the anteriorly directed short, more thick flange of the chorionon its inner surface, developing at the base of the chorionic rim. By this fusion,a notch is formed at the base of the chorionic flange in between the rim and theflange which was earlier considered as the place of fusion of the sealing bar

606 David Livingstone and M H S Yacoob

Figure 5.

R

Biosystematics of Tingidae 607

(Livingstone 1967a, b, 1976). At the time of eclosion, the opercular component of thescaling bar detached itself from the chorionic component and therefore the termsuture (SUT) of the sealing bar was found more appropriate to designate the junc­tion of the two components.

.... Biosystematic considerations

Leston et al (1954) and Drake and Davis (1960) confirmed Pruthis (1925) conclusionthat the male genitalia of Tingidae is bipartite, resembling that of the Reduviidae andplaced both these families closer under Cimicomorpha. Carayon (1954) andPendergrast (1957) on the basis of the occurrence of 'pseudosperrnatheca' concludedthat Tingid.,e, Nabidae and Reduviidae are closely related. Southwood (1956) on thebasis of the arrangement of the aeropyles and micropyles included Tingidae amongCimicomorpha. Following these earlier revelations Cobben (1968) and Hinton (1981)had taken for granted that Tingidae as a cimicomorph. However, Livingstone (1967)in T. buddleiae categorically maintained that the male genitalia is tripartite (acondition declared by Pruthi (1925) as primitive) and a pseudospermatheca is non­existant. The total absence of micropyles, consequential to fertilization taking placebefore chorion formation, alienates Tingidae from most other families ofCimicomorpha, including Reduviidae that retain both micropyles and aeropyles.

But the absence of micropyles alone does not justify the creation of Tingidae as amajor systematic group along with Anthocoridae, Cimicidae and Miridae becauseseveral other characters, especially of the cephalic end of the eggs, Tingidae and

Figure 5. A and B. Neck region of the egg showing serrations of exochorion. A. P.puerilis. B. H. yucoobii. C. C. bullita. Cephalic end of the egg shell showing the centraldarkly pigmented bulging of the collar frill filaments. D. T. scrupll[osa. Cephalic end of theegg showing collar frill filaments. opercular crest and aeropyles. E. D. rudis. Shortoperculum showing collumn and the columella. F. P. puerilis. Cephalic end of the eggshell showing bundles of principal (long) and accessory (short and slender) aeropyles andtheir extension grooves entering the aerostatic layer of the egg. G. P. cleopatra cephalicend of the egg showing aeropyles. H. P. polvphaqu. A mymarid egg parasitoid showingreproductive polymorphism. Here a biotype parasitoid of D. rudis showing very slender andmore elongate ovipositor. I. P. po/yphll!JCI. The ovipositor of anuther biotype parasitoidthat parasitises the short operculate egg of Cysteochila jaoensis. J-R. Nature of first

gonapophysis of various species according to the oviposition site. J and K. Grass tingidsA. urbanus and A. hupehanum showing highly serrated. blade like tirst gonapophysis (GC,.Gonocoxu; GO. gonoplac; GP,. gonapophysis. R. ramus). L-N. S. charieis, A. phanueliiand P. cleopatra-all are lamina ovipositors. o-R. Stem, pistil and rachis ovipositorsshowing tinely serrated more elongate spike like first gonapophysis. O. P. costalis. P.C. bullita. Q. P. puerilis. R. A. ra1'l1llus.

(Ahhreviation.~: AP. Aeropyles; APA. accessory aeropyle; APP, principal aeropyle; B, bodyof the egg; BU. Bursa copulatrix; C, cork; COL, collumn; CM, columella; CH. chorion;CHF, chorionic collar frill filament; EC and ECH, exochorion; ENCH, endochorion; EXG.extension groove; L. leaf. M, mouth of egg; OC. ocelli; OcT, oocyte; OM, compound eye ofthe parasitoid; OPC. opercular crest; OPF, opercular flange; OPP, opercular plate; PED.pedicel; PEH. parasitoid emergence hole; POP and POS, periupercular space; PUN.punciations of the aerostatic layer of the chorion: R. rib: SB. sealing bar: SER. serrations:sr. sperm bundle; SUT, suture; TB. tubcrcular process; W. warty concrescence).

608 David Lioinqstone and M H S Yacoob

Reduviidae share in common. The basis of classification of the eggs into long andshort operculate types; the structural similarities of the chorionic collar and itsassociation with the collumn (flange) of the opercular plate and in the creation of aperiopercular space; the pattern of distribution and arrangement of the aeropyles;vertical oviposition of eggs in clusters and multiplicity of the aeropyles in longoperculate eggs etc could be considered as major such characters that both Tingidaeand Reduviidae share in common.

One of the remarkable features, apart from the shape of the eggs, that could becorrelated with the systematics and evolution of eggs in Tingidae is the reduction inthe number of aeropyles corresponding with the reduction in the height of thechorionic collar which is in turn correlated with the relative obliquity of oviposition,depending on the texture of the host tissue. Long operculate eggs that are verticallydeposited in clusters invariably have more spherical caudal end and their cephalic end,almost upto the base of the chorionic rim, protruding far above the site ofoviposition. These eggs are characterized not only by the higher numerical density oftheir aeropyles opening into the periopercular space but also by their dimorphiccondition (principal and accessory aeropyles), in marked contrast with the eggs of theshort operculate lamina oviposition type. Drastic reduction in the number showing atendency towards asymmetrical arrangement of the aeropyles on the chorionic rim,with the emanipation of the collar from the operculum, could be correlated with thedirect exposure of the aeropyles to the ambient air, close to the surface of the leavesthat are actively engaged in photosynthetic process. In the majority of such cases, theunder surface of the leaves is preferred.

Interestingly, P. costa/is, a representative of Cantacaderinae, inspite of the fact thatits opercular height is quite insignificant, when compared with the long operculateeggs, the number of aeropyles is significantly higher when compared with all othereggs having similar type of operculum. It is also seen that the aeropyles in P. costalisare arranged uniformly spaced around the chorionic rim while in most other verticaldepositing species they are grouped in bundles. In the other intermediate types suchas C. bullite and T. scrupulosa their number corresponds with the number of frillfilaments.

Drake and Ruhoff (1965) considered Cantacaderinae as a homogeneous group,having more number of fossil species and with a combination of characters thatdistinctly set them apart from other subfamilies. It is suggested that P. costalisrepresents a more generalized condition of egg types in Tingidae, characterized byvertical oviposition in the stem, with cork formation around the collar and withnumerous long aeropyles, showing no trace of alignment into groups. The longoperculate type of eggs of non-lamina ovipositors, with the formation ofperiopercular space and grouping of aeropyles and their differentiation into principaland accessory types could be therefore considered as a specialization in verticaloviposition. The lamina ovipositors, having a tendency to oviposit horizontally intothe mesophyll, with their sharply serrated ovipositor, could be considered as moreevolved. as it is further evidenced by the drastic reduction in the number of aeropyles.The grass tingids of the genera Aconchus and Aqramma are therefore more highlyevolved among the lamina ovipositors. Thus the Cantacaderinae constitutes theprimitive subfamily of Tingidae from which the various genera of the subfamilyTinginae have derived specializations in their egg micromorphology and ovipositionstrategy. Intermediate conditions are found in various genera of Tingidae (scheme 1).

Biosystematics of Tinqidae

TingidaeOviposition strategy-evolutionary trend

609

Transilientovipositing -- --­(gall makers)

('1)---- Lamina/sepalovipositing

(horizontal)

iRachis/petiole/veins ovipositing

(slanting)

iPistil ovipositing

(vertical)

iStem ovipositing

(vertical)

Ovipositorhighly serratedshort operculate eggs

Intermediate

Long operculate eggsOvipositor elongately

pointed

Scheme I. Progressive reduction in the number of aeropyles,

Acknowledgements

The authors are extremely grateful to the Indian Council of Agricultural Research,New Delhi for financial support and the authorities of the University of Madras andBharathiar University for providing the available facilities for the work. The seniorauthor records his deep sense of gratitude to Prof. T N Ananthakrishnan,Entomology Research Institute, Loyola College, Madras for providing the requiredencouragement to this kind of studies.

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Ins. Eco!. and Resource Munaqe. (ed.) S C Goel S.D. College. MuzalTarnagar pp 247-252

Figure 3. A. H. laeta the Barleria tingis. Copulating pair. B. P. ecmeles. Ovariolar eggswith accessory glands arising from the bursa. C. D. rudis. Ovarioles showing dimorphiceggs: proximal long operculate eggs and distal short operculate eggs. D. H. laeta L.S ofovarioles showing basal oocyte with clear cytoplasm and sperm bundle in thepedicel. E. P. ecmeles. Ovipositcd egg (vertical) showing chorionic frill filamentsfolded. F. P. ecmeles. Oviposited egg showing the frill filaments spread out exposing thecollumn of the operculum. G. P puerilis. Two oviposited eggs in the rachis of teakleaf. H. P. costalis. Oviposited egg with cork formed around the chorionic collar andrim. I. S. cinnamomii. Ovipositcd egg showing fringe type of chorionic collar. J. P. cleo­

patra. Eggs oviposited horizontally in the mesophyll. The opening in each egg is thcemergence pore of the egg parasitoid. K. A. hupehanum la grass tingid). Short operculateegg (parasitised). L A. urbanus egg, a grass tingid. M. H. yacoobi. An oviposited eggshowing the opercular crest (Columella) being drawn out in the form of a hook. N. C. bul­

lita. A hatched egg showing the frill filaments of the chorionic collar, O. P. ecmeles. Anentire egg (long operculate). P. A. rl/vamls. An example of long operculate egg. Q. P. pue­

rilis. Two deposited eggs. R. D. rIlllis. A short operculate egg. S. E. cincll(mii. A batch of 3ovulated eggs.