WAGENINGEN AGRICULTURAL UNIVERSITY PAPERS 91-5 (1991)
Structure ofth edigestiv e systemo f aphids,i nparticula r Hyalopterusan d Coloradoa, and itsbearin g on the evolution offilterchambers i n the Aphidoidea
M.B.Ponse n Laboratory of Virology, Agricultural University Wageningen, The Netherlands
Wageningen mm Agricultural University
5h ssi^gs BIBLIOTHEEK LtfJDBOUWUNlVERSinU KAGENlN&Ett
Cip-data Koninklijke Bibliotheek,De nHaa g
ISBN90-6754-198- 2 NUGI83 5 ISSN016 934 5 X
© Agricultural UniversityWageningen ,th eNetherlands . 1992
No part of this publication, apart from abstract, bibliographic and brief quo tations embodied incritica l reviews,ma y bereproduced , recorded or published inan yfor m includingprint ,photocopy ,microform , electronico relectromagne ticrecor dwithou t writtenpermissio n from thepublishe r Agricultural Universi ty,P.O.Bo x9101 ,670 0H BWageningen ,th eNetherlands .
Printedi nth eNetherland sb yVeenma nDrukker sB.V. ,Wageninge n Contents
Introduction 3 Materialsan dmethod s 3 Pharynx 10 Foregut 10 Cuticularlinin g 10 Stomach 11 Tubularintestin e 16 Rectification 17 Caecalintestin ean d filtersystem 23 Rectum 35 Discussion 40 Foregut 40 Tripletcell s 40 Filtersystem 40 Rectum 43 Analopenin g 43 Phylogeny 46 Mycetomean d oenocytes 56 Summary 57 Acknowledgements 58 References 58 Abbreviationsuse di n figures 61 Keywords :Aphids ,histology ,alimentar y tractfiltersystem,, phylogeny . Introduction
The genera Hyalopterus and Coloradoa belong to the family Aphididae sensu Borner(1952) .Withi n thegenu sHyalopterus therear etw ospecies ,viz .th emeal y peach aphid, Hyalopterus amygdali (Blanchard), and the mealy plum aphid, H. pruni (Geoffroy). Detailed studies carried out by Basky (1978) and Basky and Szalay-Marszó (1987)reveale d nomorphologica l features for separating thesespecies ,neverthe less, they are distinct species as they can not live on each other's primary hosts, and the males do not copulate with females of the other species. According to Spampinato et al. (1988) there are electrophoretically three different species within the genus Hyalopterus, which are correlated with their primary host- plants: H.pruni on plum and apricot trees,H. amygdali A on almond and more rarely peach trees, while the opposite is true for H. amygdali B;i n summer the three species migrate to the secondary host, Phragmites australis. The primary and secondary hostplants of Hyalopterus are listed in Table 9. Descriptions of allmorph s ofH. pruni are given by Smith (1936)an d Stroyan (1984). The digestive system of//, pruni feeding on Prunus domestica and Phragmites communis (= Phragmites australis) consists of a foregut, a dilated stomach, a tubular intestine, and a hindgut (Janiszewska, 1932),bu t lacks a filterchamber (Kunkel and Kloft, 1977). An investigation of the anatomy of the digestive system of Hyalopterus and Coloradoa was carried out as dissections of aphids of these genera revealed the presence of a filtersystem in some specimens. Within the family Aphididae only three genera are known to have a filtersystem, viz. Acaudinum, Capitophorus, and Cryptomyzus (Borner, 1938;Ponsen , 1977).
Materials and methods
Specimens of the species listed in Table 1, 10, and 13,wer e collected from the hostplants and put in Duboscq- Brasil's fluid. After fixation the aphids were dehydrated ina grade d serieso fethano l and inmethy l benzoate, stored in methyl benzoate celluidin (2%) for three days or longer, and then in toluene and finally embedded in paraplast. Serial sections, 8/m i thick, were stained in 1% methyl- green aqueous solution, rinsed in tap-water, dehydrated in methanol and in methyl benzoate, cleared in xylene, and finally mounted in xylene-dammar. The sections were examined under a Wild phase microscope. The drawings were made with help of a Wild drawing tube. The morphology of a digestive system was reconstructed from the drawings of serial sections of a whole larva viewed at a magnification of 600 times. The
WageningenAgric. Univ.Papers 91-5 (1991) 3 Table 1. A listo fHyalopterus specimens studied, their hostplant, and relevant locality data.
Hostplant Locality
Prunus amygdalus Koutouloufari, Crete (Greece), 29.IV.198 9 Prunusamygdalus var.dulcis Passo Martino, Sicilia (Italy), 19.VI.1989 Prunus armeniaca Festos, Crete (Greece), 10.V.1989 Prunus domestica Wageningen, 29.V.1983 Wageningen, 30.V.198 8 Hódmezövasarhely (Hungary), V.198 8 Cannizzaro, Sicilia (Italy), 19.VI.1989 Wageningen,X .198 9 Prunus insititia Ede, 10.VI.1989 Prunusper sica Bennekom,6.VII.1983 Carcavelos, Cascais (Portugal), 18.V.1988 Ami, Ibaraki (Japan), 20.V.1988 Canchipur (India), IV.198 9 Trecastagni, Sicilia (Italy), 19.VI.1989 Wageningen, 5.X.198 9 Prunusspinosa Mehren, Eifel (Germany), 22.VII.198 6 Heudicourt, Champagne (France), 21.VII.1987 Wageningen, 5.VIII.198 7 Arundo donax Mâlia, Crete (Greece), 8.V.198 9 Molinia caerulea Culture Department of Entomology, Wageningen, 1989-1990 Phragmites australis Wageningen, 12.VII.198 2 Wageningen,X .198 7 Wageningen, X.198 8 Lyme Regis, Dorset (England), 18.VII.198 3 Hastière (Belgium), 11.VII.1987 Saint-Mihiel,Champagn e (France), 20.VII.1987 Billy-s/s-le sCôtes , Champagne (France), 24.VII.1987 Tihany, Balaton (Hungary), 9.VIII.1987 Tidbinbilla, ACT (Australia), 10.IV.1988 Passo Martino, Sicilia (Italy), 19.VI.1989 Phragmites karka Canchipur (India),IV .198 9 Phragmites mauritianus Gisenye, Lake Kivu (Rwanda, Central Africa), V.198 8 Kisosi (Burundi, Central Africa), V.1988 Phragmites sp. Long Beach, Calvert County, Maryland (U.S.A.), 16.IX.198 9 Typha latifolia Ede, 24.VII .198 9
number of nuclei with their conspicuous big nucleoli,whic h correspond to the number of cells,wer ecounte d at a magnification of 1500times . The length of the aphid and that of the digestive system was calculated by multiplying the number ofseria lsection sb yth ethicknes so feac hsection ,8 /x m(Tabl e8) . Theinvestigatio nwa smainl ydon eo nyoun glarva eth emorp ho fwhic hcoul d onlyb edetermine d after microscopicalexaminatio n ofth esections . In order to dissect the digestive system, aphids were placed on double sided self-adhesive tape attached to a black plastic plate. Under a dissecting micro scopeeac h aphid wascovere d with adro p of Levysolutio n and dissected using
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Univ.Papers 91-5 (1991) Table 5. Number of dissected specimens of Hyalopterus with (+ ) and without (— )a filtersystem. The green apterous viviparous offspring is produced by green apterous viviparous females (funda- trix) on Prunus domestica (1-10) and on Prunus spinosa (11-20) (Wageningen, V.1990) . Each female lays from two to four eggs(Willcocks , 1916). No. of fundatrix Filtersystem Total number Apterous viviparae of offspring Filtersystem + - 1 15 3 12 2 — 10 0 10 3 - 9 1 8 4 - 15 5 10 5 — 24 9 15 6 + 17 1 16 7 - 11 2 9 8 - 13 1 12 9 — 20 5 15 10 — 25 1 24 11 — 12 3 9 12 - 13 2 11 13 - 10 3 7 14 — 15 7 8 15 — 13 3 10 16 — 10 4 6 17 - 14 1 13 18 + 14 2 12 19 + 14 4 10 20 - 15 6 9 watchmakersforcep s (Table3-7) . Hyalopterus were collected (29.VI.1989) from Prunus domestica growing in theDemonstratio n Garden for Plant Diseasesa tWageningen . Theaphid swer e reared continuously on field collected Moliniacoerulea in a greenhouse at 20 ± 3° Cwit ha photoperio d of 16hour san da relativ ehumidit yo f70-80 %(Tabl e 1-3). Specimens of the species listed in Table 12 were collected from their host plants.Unde r astereomicroscop e theywer epu t oneb yon ei n96 %ethano l for 10 seconds to extract the air-bubbles from the surface of the cuticle and out of the tracheal system. Thereafter they were transferred to 0.1 M cacodylate buffered (pH 7.4) glutaraldehyde (3%) for 2t o 4hour s and then prepared for electronmicroscopica l studyfollowin g Ponsen(1972) . WageningenAgric. Univ.Papers 91-5 (1991) Table 6. Number of dissected specimens of Hyalopterus with (+ ) and without (— )a filtersystem. The apterous viviparous offspring is produced by green alate viviparous females (spring migrants) on Phragmites australis. These females originated from Prunus domestica in the direct neighbour hood of Phragmites australis in the Demonstration Garden for Plant Diseases (Wageningen, VI.1988). No. of spring Filtersystem Total number Colour of apterous viviparae of offspring green pink Filtersystem Filtersystem + — + — 1 16 7 3 3 3 2 — 18 7 9 0 2 3 — 24 4 6 5 9 4 + 8 3 0 2 3 5 — 8 3 0 0 5 6 + 24 9 0 5 10 7 + 21 10 5 0 6 8 — 21 0 2 6 13 9 — 20 12 5 1 2 10 — 14 4 3 1 6 11 — 13 5 8 12 — 14 2 7 1 4 13 + 19 2 1 5 11 58% 28% Table 7. Number of dissected specimens of Hyalopterus with (+ ) and without (— )a filtersystem. The green apterous oviparous offspring is produced by green and pink alate viviparous females (gynoparae) on Prunus domestica in the orchard of the Plant Protection Centre (Wageningen, X.1989) . Each gynopara produces an average of 9.8 oviparous females (Smith, 1936). No. of gynopara Colour Filtersystem Total number Apterous oviparae of offspring Filtersystem 1 green + 0 6 2 + 0 8 3 + 0 6 4 + 0 7 5 0 8 6 1 5 7 pink 0 5 8 + 1 8 9 + 0 9 10 + 0 9 11 + 1 8 12 + 0 9 WageningenAgric. Univ.Papers 91-5 (1991) Pharynx Thealimentar y tract startswit hth efoo d canaltha ti sforme d byth einterlocke d maxillary stylets. This food canal leads into the pharyngeal duct, formed by theepipharyn xan dth ehypopharyn x lip.Th epharyngea lduc ti sseparate d from the pharyngeal pump by a valve, of which both the dorsal and ventral walls aremarke db ytw ocuticula rdome-shape dprominences .Th eepipharyngea lgus tatory organ has 14s e illary pores, of which eight are arranged in a row in the epipharynx of the pharyngeal duct. Six sensillary pores are located in the dorsal wall of the pharyngeal valve, three on each side of the two insertions ofth ecuticula rtendon st owhic hth edivaricato rmuscle so fth epharyngea lvalv e are attached. The hypopharyngeal gustatory organ has four sensillary pores: two in the hypopharynx of the pharyngeal ductjus t anterior to the valve and the other two at the foot of the salivary pumpstem. Both the structure of the pharynx, including the muscles of the valve and the pump, and the structure ofth egustator yorga nar eidentica lt othos eof Aphis specie s(Ponsen , 1990b) . Foregut Theforegu t (oesophagus)run sposteria d from thetentorium ,betwee n thesaliv aryglands ,alon gth emedia ndorsa lfurro w ofth esuboesophagea l ganglion and terminates in the oesophageal valve (Figure 1).I n transverse sections the uni form thin tubeconsist so f2- 4squamou s cellso fwhic hth eirregular-shape d nu clei protrude into the lumen (Figure 2F). Just before the stomach the foregut is supplied by a branch of the medial dorsal nerve, which runs alongside the dorsalvessel . The oesophageal valve is an invagination of the foregut into the lumen of the stomach. It consists of two layers of non muscular epithelium, which form anintravalvula r space(Figur e2F) .Th einne rlaye ri sa continuatio n ofth efore gut,wherea sth eoute rlaye ri sbuil tu po fcuboida lcells ,eac hcontainin ga spheri cal,relativel ylarg enucleus .Th eepithelia lcell so fbot hth eforegu t andth eoute r layero fth evalv esecret ea chitinou sintima . Cuticular lining Thecuticula rlinin go fth eepidermi sconsist so fa ninne rachromati cstructureles s layer,the na laye ro fa darkl ycoloure d substance,an da delicat ever ydar klayer , respectivelyth eendo- ,exo- ,an depicuticle .Durin gmoultin gth eol dcuticl econ sists of only the last two layers and it is quite separate from the new cuticle of which the two layers are already distinctly present. Inside the achromatic structureless endocuticle there are many waxy droplets (Figure IIB, 12, 13D and 181),whic hpresumabl yar eresponsibl efo rth erathe rheav ycoatin go fmeal y wax on Hyalopterus aphids.Th e waxy droplets originate from fat cellsan d are 10 WageningenAgric. Univ.Papers 91-5 (1991) scattered in the haemolymph throughout the body cavity. In phase microscopy the waxy droplets are recognizable by their white refractive appearance. They are soluble in acetone,chloroform , and ether, but not in alcohol (Ponsen, 1972). The cuticular lining or intima of the foregut and the oesophageal valve is an achromatic structureless mass with on the luminal surface a delicate dark line (Figure 2F, 14B, 17B,an d 18B).Althoug h the intima of the foregut is very narrow and that of the valve relatively voluminous extending far into the stom ach lumen, waxy droplets are never observed inside the endocuticle. Ultrathin sections of some aphid species (Table 12) show that the intima of the foregut consists of an endocuticle and an exocuticle, but lacks an epicuticle (Figure 5Aan d 19A-B).Th eendocuticl ecompletel y dissolves,an d the exocuticle remains in the lumen of the foregut. The exocuticle of the outer layer of the valve disintegrates into fragments. The integument of 'mature' embryo's in a nine days old viviparous Myzus persicae larva secrete a cuticle. This embryonic cuticle soon separates from the epidermis and the first instar cuticle is laid down in its place. The embryonic cuticle is not shed and remains round the embryo until its birth (as well as in the egg of Adelges (Dreyfusia) nordmannianae). After birth the embryo is enclosed in a delicate membranous structure, the embryonic exocuticle, from which the first stage larva emerges within five minutes. This is a critical phase in the life cycle of the aphid because under field conditions a large proportion of the aphids fail to emerge from the embryonic exocuticle, especially in dry, hot summers. Hyalopterus pruni (Smith, 1973),M. persicae (Ponsen, 1969), and many other aphid speciescomplet e four instars within about 10day s at a mean temperature of 20°C , so that in an imaginai aphid five exocuticles remain inside the foregut, namely one embryonic and four larval. These five exocuticles inside the foregut are presumably not a barrier for the sap flow from the pharyngeal pump to the stomach or to prevent regurgitation. Stomach The stomach begins in the mesothorax or metathorax, and joins the intestine inth e first, second, or third abdominal segment (Figure 1).I t has adilate d struc ture and lies centrally in the dorsal region of the aphid and dorsal to the caecal intestine. The maximum diameter of the stomach is situated beyond the end of the oesophageal valve; in Hyalopterus on its primary hostplants it consists of 17-23 cells and on the secondary ones 13-18 cells. In C. tanacetina the maxi mum diameter of the stomach consists of 11-13 cells. The epithelium of the stomach of Hyalopterus consists of two forms of cells: in the anterior region triangular cells with more or less spherical nuclei (Figure 2A), and in the posterior region of the stomach cuboidal cells with oval nuclei (Figure 2B). Both cell forms contain small vacuoles and granules, and the basal cell membranes are strongly invaginated. The apical cell membrane presents WageningenAgric. Univ.Papers 91-5 (1991) 11 Figure I.A. Dorsal view of the digestive system of an apterous viviparous female of Hyalopterus from Phragmites australis, reconstructed from serial transverse sections. 1-2, meso- and metathoracic spiracles; 3-9, abdominal spiracles. The siphunculi (co) are situated on the sixth abdominal tergite. Bar represents 30 urn. B. Schematic impression of the transition from the crenated opaque intestine to the smooth transparent caecal intestine. Note the position of thefilterchambe r cells. For list of abbreviations seepag e61 . 12 WageningenAgric. Univ.Papers 91-5 (1991) I 1 Figure 2. Transverse section of the filtersystem showing encapsulation of the anterior region of the stomach by the anterior region of the caecal intestine (A), the posterior region of the stomach (B), the first (C) and second region of the crenated intestine (D), the second region of the crenated intestine with triplet cells (E), the oesophageal valve (F), and the rectum (G) of Hyalopterus. (H). Transverse section of the stomach, the second region of the crenated intestine, and the anterior region of the caecal intestine of Coloradoa tanacetina. For list of abbreviations see page 61. Bar represents 10/«n . WageningenAgric. Univ.Papers 91-5 (1991) 13 Figure 3.Semi-schemati c representation ofth egu t ofspecimen s ofHyalopterus with (A)an d without a filtersystem (B).Th e transverse serial sections 1-7 are from theregio n of the stomach and illustrate the relationship between the stomach and caecal intestine in those specimens that have (A) and lack a filtersystem (B).Fo r list of abbreviations seepag e61 . 14 WageningenAgric. Univ.Papers 91-5 (1991) Figure 4.Transvers e sections of theanterio r region ofth ecaeca l intestine of which the filterchamber cells are situated on the side of the stomach and the caecal intestine cells on the opposite wall. A. Hyalopterus sp.;B . Metopolophium dirhodum;C . Uroleuconsonchi; D. Acyrthosiphon caraganae; E. Macrosiphum albifrons (Table 10). F. In Phloeomyzus passerinii (Signoret) the intestinal cells end abruptly, and thecaeca l intestinecell sbegin . For listo f abbreviations seepag e 61. Bar represents 10 pm. WageningenAgric. Univ.Papers 91-5 (1991) 15 a labyrinthine system of closely packed irregular invaginations of different di mensions (Figure 5Ban d 19C-D) and itslumina l surface isline d with extracellu lar microtubules (seepag e 22). The triangular cells produce an apocrine secretion, which is discharged together with parts of theapica lcytoplas m which gradually dissolve inth e stom ach lumen. The cuboidal cells produce a merocrine secretion; in ultrathin sec tions of Myzus persicae involve breaking off of parts of the labyrinthine system, which dissolve in the stomach lumen forming an amorphous threadlike mass (Figure 5Ban d 19C-D).Th e stomach cells secrete continuously throughout lar val and adult life. Theanterio r region ofth estomac h lumen isnearl y completelyfilled wit h solid material and the posterior region with fine-grained material (Figure 2A and B).I ndissections ,thi si sclearl y seeni na numbe r ofspecimens ,wher eth eposteri or region of the opaque stomach isles sdens e than the anterior region. Probably there isn o mixing occurring between both luminal secretory products asa result of the very slow peristaltic movements. These products are strictly limited to the lumen of the stomach and do not occur in the intestinal lumen which shows a clear appearance. The stomach ofC. tanacetinaconsist s of only triangular cellswit h a merocrine secretion (Figure 2H). In very young specimens the lumen is filled with fine grained material and small thread-like structures, but in older specimens the stomach cells are more flattened and the lumen is completely filled with very big thread-like structures. The presence oftw otype so fglan d cellsi nth e stomach of Hyalopterus (Figure 2A and B) indicates that this species belongs to the polyphagous aphids which arabl et o feed onplant si nman y different families (Table 1 and 9).Thi s phenom enon hasalread y beendiscusse d (Ponsen, 1990b) .Th e stomach ofth e monopha- gous aphid C. tanacetina consists of only one type of gland cells,viz . merocrine cells. Tubular intestine In dissections of living aphids the foregut, stomach, and tubular intestine are opaque structures which show slow peristaltic movements generated by circular muscles. The tubular intestine has over its entire length a crenated structure (Figure 1B) and its posterior region shows some distinct white dots which are the triplets. Histologically the tubular intestine consists of two distinct regions (Figure 1).Th e first region of the intestine (small crenated intestine) runs from the stom ach to the abdominal loop situated in the fifth, sixth, or seventh abdominal segment. From there it passes gradually into a broader one, forming the second region of the intestine (large crenated intestine), which terminates at the caecal intestine. Both in Hyalopterus on Prunus, and in Coloradoa the second region of the intestine forms one or two additional loops situated between the mesoth- 16 WageningenAgric. Univ.Papers 91-5 (1991) orax and the fourth abdominal segment; in Hyalopterus feeding on Arundo, Molinia, Phragmites, and Typha there occur mainly two additional loops (Table 2). The number of additional loops is independent of the morph, and the pres enceo fa filtersystem . Within the specimens the first region of theintestin e bends either to the right or to the left of the caecal intestine and the transition from the stomach to the intestine is marked by a sharp loop. The intestinal loops are closely applied to the side of the stomach. The voluminous abdominal loop isconnecte d with a branch of the main abdominal nerve. In the second region of the intestine the cells and nuclei are bigger, and the cytoplasm more vacuolated than in the first region of the intestine. The apical cell membranes of the triangular intestinal cells are distinctly striated. In ultrathin sections (Table 12)the ypresen t alabyrinthin e system ofclosel y packed irregular invaginations ofdifferen t dimensions (Figure 6C and 20F). Transverse sections of the entire tubular intestine of both Hyalopterus and Coloradoa con sists of 3-5 triangular cells forming a more or less stellate lumen (Figure 2C and D). The second region of the intestine is characterized by the presence of 6-8 groups of three conical-shaped cells (triplet). They occur mainly in the second half ofth e second region ofth e intestineincludin g the additional loops at irregu lar intervals among the triangular intestinal cells. The majority of the triplets occur singly. Occasionaly, however, two triplets or rarely three triplets occur together. The middle cell of each triplet is very large with a large nucleus, and the other two are very small each with a relatively small nucleus. The cytoplasm contains numerous minute vacuoles; the apical cell membrane has a small striated zone (Figure 19E) and the basal cell membrane is strongly invaginated. The radial cell membranes of the triplet cells are about twice as long as those of the intestinal cells(Figur e 2E). Rectification Histologically there are two types of hindgut in thedigestiv e system oîSubsaltu- saphis ornata (Theobald) (Figure 9). The first type of hindgut is an extension ofth e ascending intestine and consists oftriangula r cellswhic hpresen t a striated border on their luminal surface closely resembling the striated border of the ascending intestine (Figure 20). This is the endodermal hindgut or descending intestine. The second type is a blindly ending evagination of the rectum and for this structure the term ectodermal hindgut was introduced by the presence of a delicate intima lining the apical cell membrane of the squamous cells. In dissections both types of hindgut have a smooth transparent structure showing vigorous peristaltic movements generated by circular and longitudinal muscles, although the cellular structure of both typesi squit e different (Ponsen, 1979). In ultrathin sections of the digestive system of Rhopalosiphum maidis, S. ornata, and Uroleuconsonchi (Tabl e 12),i tappear s that adistinc tcuticula r lining or intima, such as that present in the foregut and the rectum (Figure 5A, 81, WageningenAgric. Univ.Papers 91-5 (1991) 17 Figure 5.A. Apical cell membrane of the foregut of Myzus persicae. Note the plaques at the tips of the irregular fingerlike evaginations of the apical cell membrane and the non-lamellate structure of the endocuticle .B. Apical cell membrane of the stomach of Myzus persicae. Arrows breaking off of parts of the labyrinthine system (merocrine secretion). For list of abbreviations see page61 . Bar represents 0.5(im . u WageningenAgric. Univ.Papers 91-5 (1991) w "••••* % Figure 6. Apical cell membrane of the small crenated intestine of Rhopalosiphum maidis (C), and the descending intestine of Drepanosiphumplatanoidis (D) and Subsaltusaphis omata (E). Note the extracellular microtubules (see arrow). For list of abbreviations see page 61. Bar represents 0.5 Aim. WageningenAgric. Univ.Papers 91-5 (1991) 19 Figure 7. Apical cell membrane of the descending intestine of Adelges (Dreyfusia) nordmannianae (F) and of the caecal intestine of Rhopalosiphum maidis (G). Note the extracellular microtubules (seearrow) . For list of abbreviations seepag e 61. Bar represents 1 ßra. 20 WageningenAgric. Univ.Papers 91-5 (1991) *i laf ' *• Är"^.-"!*!! g^^y^&'jfi Ai. ••-*;.«•;; ' • •• •• iff.,.^ Figure 8. Apical cell membrane of the caecal intestine of Subsaltusaphis ornata (H), the rectum of Uroleuconsonchi wit h an old and newexocuticl e(I) , and theepiderma l invagination oiDrepanosi- phumplatanoidis (J)showin g thelamellat e structure of theendocuticl e (seearrow) .Fo r list of abbre viations seepag e 61. Bar represents 0.5 /im. WageningenAgric. Univ.Papers 91-5 (1991) 21 19 and 20),i sabsen t in their respective 'ectodermal hindgut'. On the other hand, theapica lcel lmembran e ofth e'ectoderma l hindgut', presentingirregula r finger likeevagination s inwhic h occursmal loblon g mitochondria, isline dwit ha single row of extracellular microtubulelike structures (Figure 7G and 8H). The term extracellular microtubules wasintroduce d by O'Loughlin and Chambers (1972) lying along the luminal surface of the intestinal and hindgut cells of Acyrthosi- phon solani(Kaltenbach ) (= Aulacorthum solani(Kaltenbach) , Aphis craccivora (Koch), Hyperomyzus lactucae (Linnaeus), Macrosiphum euphorbiae (Thomas), and Myzuspersicae (Sulzer).Late r on these structures were also observed facing the hindgut cells of Rhopalosiphum padi (Linnaeus) (Gildow, 1985). In the coc- cid, Planococcus citriRisso ,identica l extracellular microtubules occur along the luminal surface of the intestinal cells(Foldi , 1973). The apical cell membrane of the endodermal hindgut or descending intestine of S. ornata (Figure 6E) as well as of Drepanosiphum platanoidis and Adelges (Dreyfusia) nordmannianae (Figure 6D and 7F; Table 12) presents a labyrin thine system of closely packed irregular invaginations of different dimensions (Figure 20). Such a labyrinthine system of the apical cellmembran e occurs also in the cells of the stomach and the crenated intestine of the above mentioned species,includin gM. persicae (Forbes, 1964). Since electron microscopic examination revealed the absence of a cuticular intima inth e blindly ending evagination of therectu m or 'ectodermal hindgut'of S. ornata, it follows that the term 'ectodermal hindgut' is wrong and has to be replaced by the term caecal intestine being a part of the midgut. Moreover, as the hindgut in insects isline d by a cuticular layer the term 'endodermal hind gut' isn o longer applicable. Within the families Adelgidae (Figure 17), Mindaridae (Figure 18), Thelaxi- dae, Chaitophoridae, Greenideidae, Drepanosiphidae without a filtersystem, Anoeciidae, and the genera Anuraphis, Aphis, Brachycaudus, Plocamaphis, and Pterocomma, the midgut consists of a stomach, a tubular crenated intestine, and a smooth transparent descending intestine (Figure 10A). Species of Drepa nosiphidae with a filtersystem (Table 4 in Ponsen, 1990 a) have two smooth transparent intestines (Figure 9): the descending intestine which is a continua tion of the ascending intestine, and the caecal intestine which isa blindly ending evagination ofth erectu m (Figure 10B). Both transparent intestinesfor m a filter- system: a concentric filtersystem in which the stomach is encapsulated by the caecal intestine (previously named the 'ectodermal hindgut') (Figure 9B) and a parallel filtersystem in which the anterior region of the ascending intestine isfuse d with the posterior region of the descending intestine (previously named the 'endodermal hindgut') (Figure 9C).However , within the families Phylloxeri- dae (Figure 14), Phloeomyzidae, Lachnidae, and Aphididae (Table 10), the transparent descending intestine is completely lost and replaced by the caecal intestine (Figure IOC). In this group of aphid species the midgut consists of a stomach, a tubular crenated intestine, and a smooth transparent caecal intes tine. 22 WageningenAgric. Univ.Papers 91-5 (1991) Caecalintestin e and fîltersystem The caecal intestine of Hyalopterus and C. tanacetina starts in the meso - or metathorax and runs directly caudad ventrally of the stomach and dorsally of the voluminous abdominal loop of intestine to open into the rectum (Figure 1).It s simple epithelium consists of long squamous cellswit h elliptic nuclei. The long axis of the nucleus is parallel to the main axis of the cell and the short axis protrudes into the lumen (Figure 2 and 4). The long cells contain granules and irregular membraneless 'vesicles' (Figure 7G)i nwhic h occur waxy droplets. Thewaxy droplets originate from fat cellsan d are scattered throughout the body cavity from which they are released by the caecal intestinal cells into the lumen. The irregular apical cell membrane presents minute projections (Figure 201). Halfway, on its ventral side, the caecal intestine is connected with a branch of the main abdominal nerve. In dissections of living aphids the caecal intestine is a smooth transparent structure that shows vigorous peristaltic movements generated by circular mus clesan d about eleven longitudinal muscles; the latter are external to the circular muscles.A sa result ofth evigorou s peristalsis thecaeca l intestineca n take sever alforms , from themos t contractileconditio n to themos t dilated condition form ing a more or less spherical structure to the most bizarre irregular ones (Figure 21). In the most dilated condition the caecal intestine can attain a volume of about 6 times its original one; the cells are very flat and the elliptic nuclei are situated against the basal cell membrane. In a number of specimens the anterior region of the stomach is completely encapsulated by the anterior region of the caecal intestine forming a concentric fîltersystem (Figure 2A and 3A). On the other hand, there are specimens of which thestomac h isno tencapsulate d byth ecaeca lintestine ; thecaeca l intestine is completely separate from the stomach showing a kidney-shaped to a more or less spherical structure (Figure 2H). Moreover, there occur intermediate forms of which the caecal intestine is partly fused with the stomach. In dissec tions the two parts of the fîltersystem are so intimately fused that they cannot be separated easely from each other. In ultrathin sections of Subsaltusaphis ornata the opposite basal cell membranes of both filtersystems are anchored to each other by the basal lamina which extends into irregular invaginations of the opposite epithelial cells (Figure 8H). The segment of the caecal intestine which envelopes the stomach is the filter- chamber (Figure 2A). The length of the filterchamber is about two fifths of that of the stomach (Figure 3A). The filterchamber is lined with both filter- chamber cells and caecal intestine cells but so arranged that the filterchamber cells are situated on the side adjacent to the stomach and the squamous caecal intestine cells on the opposite wall of the filterchamber. The filterchamber cells in the filterchamber are acontinuatio n of those of the second region of theintes tine. By the bending of the filterchamber around the stomach the filterchamber cells loose their triangular structure and transform to a more or less cuboidal WageningenAgric. Univ.Papers 91-5 (1991) 23 w • Figure 9. Semi-schematic representation of the digestive system of Subsaltusaphis ornata recon structed from serial transverse sections. Bar represents 30 fim. Schematic transverse sections of the concentric filtersystem (B) of which the stomach is encapsulated by the caecal intestine and the parallel filtersystem (C) of which the ascending intestine and the descending intestine are fused together. For list of abbreviations seepag e61 . 24 Wageningen Agric. Univ.Papers 91-5 (1991) Figure 10. General impression of the digestive system of an aphid with a descending intestine (A), an aphid with both a descending intestine and a caecal intestine (blindly ending intestine) (B, see Figure 9), and an aphid in which during evolution the descending intestine disappeared and was replaced byth ecaeca l intestine (C).Th e transverse sectionscorrespon d with thesevera l subdivisions of thedigestiv e system. For list of abbreviations seepag e61 . WageningenAgric. Univ.Papers 91-5 (1991) 25 form (Figure 2A). In some specimens they have less vacuoles in their cytoplasm than those in the second region of the intestine. In transverse serial sections they start as a ring of cells adjacent to the stomach, after which the number of filterchamber cells gradually decreases until the caecal intestine consists of only squamous cells (Figure 3A, 1-7). The part of the filterchamber with the filterchamber cellsi sopaqu e and only enveloped bycircula r muscles.Th e oppo sitepar t of the filterchamber istransparen t and has both circular and longitudi nal muscles as well as the entire caecal intestine. As a result of the transparent structure ofth ecaeca lintestine , the filterchamber cellsar eclearl y seen especially when after dissection a drop of saturated picric acid or Duboscq-Brasil's fluid isadde d to the Levy solution (Figure 1B). Inth e specimenswher eth estomac h isno tencapsulate d byth ecaeca l intestine, the epithelial lining of the anterior region of the caecal intestine is identical to that ofth especimen swit h a filtersystem (Figure 3).Althoug h thecaeca l intestine iscompletel y separate from the stomach and has a more or less spherical struc ture, the filterchamber cells are situated on the side of the stomach with the squamous caecal intestine cells on the opposite wall (Figure 2H and 4A-E). In dissections, the region of the caecal intestine with the filterchamber cells shows anopaqu ecrenate d structure similar toth eentir ecrenate d intestine;th e opposite wall of the caecal intestine with the squamous cells shows a smooth transparent structure like the rest of the caecal intestine (Figure IB). Thepercentag e of specimens ofHyalopterus with afiltersyste m is significantly higher on Phragmites than on Prunus, Molinia, and Typha (Table 4; G-test,P < 0.0001). However, there isn o difference between the percentages of apterous viviparous females with a filtersystem feeding on Prunus, Molinia, and Typha, although the latter two are secondary hostplants (Table 4). On Prunus the per centage of apterous viviparous females with a filtersystem is higher than for alate viviparous females, but there is no difference in percentage between alate viviparous females and apterous oviparous females (Table 4). In the first gene ration on Phragmites the percentage of the green apterous viviparous females with a filtersystem ishighe r than for thepin k apterous viviparous females (Table 6), although in the subsequent generations there is no difference (Table 2 and 3). On Phragmites the percentage of apterous viviparae with a filtersystem is higher than for alate viviparae (Table 3) as on Prunus, while it is higher for alate viviparae than for alatemale s (Table 4).Adult s with or without a filtersys tem can produce both progeny with a filtersystem and progeny without a filter- system (Table 5-7). In Coloradoa26 %o fth especimen shav ea filtersyste m (Table2 )wic hi ssimila r to the percentage of Hyalopterus feeding on Prunus, Molinia, and Typha (Table 4). The caecal intestine is about half as long as the aphid (Table 8) and the total number ofcell svarie sfro m 96t o 113fo r Hyalopterus, and 58t o 67fo r Coloradoa. There is no difference in length and total number of cells in the caecal intestine in specimens with or without a filtersystem, or from different hostplants. After birth cell division in the digestive system ceases and during larval growth the 26 WageningenAgric. Univ.Papers 91-5 (1991) •3 a 3 ^ — H •g II •^•\0(NOc»Tj-ooooot~-fNooTrfN^Dfn-Hoa>'—i en oo r> (N M ÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖÖ <3 S O O O O O oooooooooooooooo o o o o o O o mot(NWTto-o\nNm^oor)0^^\c\o-Hntoo^ioooooooooooooooooooooooooon M ^ 3 °c — o &'Eö -5 u O c O O '> '? o CJ u M I- O O O O O O CD en en e» '> '> M '> ca en (-1 en hfl *-t CO 'M "M '> M M M M M M Ö CD 3 3 3 3 3 c/i c/) '? 3 3 3 & C/5 '> & O. Ü •Û & O O O O O 3 3 3 '> O O O g. a JZ 3 1-H S- 'M 'M O O V o O •> •> CD Ë > ca ca ca M ca s s '> O '> '> M '> '> M M '5 '> cd Q. U M eu eu eu CU O) O. O. •> S C Ä > c a & g. « '>C« & '>W5 '>en '>CA '>t/i ec« Cfl •> •> O. D. 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Univ.Papers 91-5 (1991) o o 5 Z ca 5 'pi 2 ' Ë °* M 2's ' X a S en o "-1 f- :0 :E •« —• ca o S O) « « 2: cfi — S£ «"J — s^o g — •OT322 « 2 °* ON ' rt u e ~« ' •-* ~* ^H J3 ca 3 « .O O G O ' *3 « O ü M 3 U U -C g O J3 00 1/3 fS M £ t« m H o o J3 CA 00 3e 2 S •a ^ o •— C3 3 vinifera a latifolia usprunoph us salicina us spinosa s communis i a angustifo iculum vuig i .H •> •> a: ^ 3c c3 s3: as -Ci «>, ft. S H ft, n, ft, «Cft! <% c?pi§ ^ a =; s o, •C 3 >N «H D > Wagem'ngen/Igrc'c. t/m'v.Papers 91-5 (1991) 29 _eS "ob X X c CO & •« -S ;-> ci oo 00 ' •O oo o\ 73 .S.2u P§ [^ n '—' eu 6n "> S * o .SP B»fc - « -s 3 3 a •~ -c 5 :g -S 3 eu ä 3.1I 'S 5 a .§ 5 S, a 2o S§ t û. Ci, S & S 3 - ™ » 1 Sil S. s a .S • !£.S' 3 S •§ -5 c o "1 ci L' 5) y s. s *^ -s -^: ti *- ^ ^* 5> ~ »•o o» 5^ t~c Co o TJ J3 §.3 ° S S cd ^ -O •O ü U x> T3 ._JH çd fi CU 'S M G -S u.ä • •gl.fi S S Q N•S -SN oo g a a a i ^J es SS fe' o Ö..2 S g D. C &£1 -S -S ci J< c M •-? 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Papers 91-5 (1991) 31 X e C i S gS| Ü'H flu \o ^ ^- r- E'S-S 8 ca x Ë B1TJ 3 •o s o. S c x c CA •£* 73 o,. 2 o c~ y *5 eu •* •* r- •* Tfcocninw^x^o Tf-CDTj-TtO'^-m'sO^OOO-cJ- Is H O CA .a s co .2 ^ 'S o cu u 60 s. Ö g § * cu -C S !5 O ' x 2 S -S ^ -SP -SP 's I g g -o ? 'S I'S 60 "S. ä 5 's I'S, Si « ft, cj S §i O 11 J2 H •S -S S'1 I- § & 'c 33 £3 ^ S 3 a Ê S £ !§ !§ <§ ^ CA O CU o 73 * Xi X O s ^S • fi3 X) O o ti C X £J -c -s C u § S 5 s-s c« X sCU. sC-u V. QJ CU •t S S S 5 ? Ü -s C*H S •S £ O 3 » 3 a -C -S -« -s: c c c c c « •S*-S* -•S«- >Q o o o o o o -s —T 3 •S--S- cj CJ cj Cj cj cj o XI e» o O S 3 S S 3 a ft, s s -Si -Si -Si -32 -Si -32 5> x cj cj Cj (j Ü bo X CU o, Cj o o o o o «t H o < 32 Wageningen Agric. Univ.Papers 91-5 (1991) 0^^>^^^^oo^t^^<^<^^co<^Tf^asr--oorn«rioo<^'0(Nw-irn^ooo(N ffi-H(S-i-H-H'HNNMO)HFH(snn(Nm(N--nfnri(N 3 3 3 3 3 3 3 3333 3333 OOO O OOO OOOO OOOO o .& o .&.& o o .& o o. & o .& o .£• o o .&. & o .& .9- o o o .& o .& o .& o .& -1 cd •-« cd •—" -•-* c-•-d* c dc -—d• ccdd -— cd• -— c• dc dc •-d «-— c•d -rcd •-cd« cdc •-d "-J- •I« c^d Tc-d1 *r•-«* -cd« cdcd c d ->-« cd•! — a > a > >a > a a -> o a- > a a, > a a, > > a o. «>> o «a> a a >- o >. > & > > >o. &.&.&> & > 3 . .— 3 .« .« 3 -^ 3 .« 3 •£ * .£H 3 3 -2 oor^-T}-Tj-f*i rn n ^ >o oo 't •I o 'i^l Ûi 3 tl) r_ 1 #1I I #| 1laf ! 11 si I . I H It il S!i isiif il! y l #l Il il il Hl mil rtillï i i i sis U h h ft, ^ft;^a,h o 09O -J a, ^ £ s ? s s -• Ni .5 ™ N -S S .3 S S-. w •s .s .s a -c .s s? s a e -s s; S3 'g s S .§3 S^S <5,s £ 12SS§ ^Ul S t.• §i 8f f8 f8f8 g.I 1 1§ • ?!.§•-cj-äl§ Ss S&g g i §s s : s- !•§ bè fe& f-S -a l'tslj J's | s * * * N N £3 ^ ^ ^^ 3 £$$$% ^<^^lt^ § § Si WageningenAgric. Univ. Papers91-5 (1991) 33 ^in^rnm-Noo^oon't^ (NM-H(NM-iH(Nfrifnm mc^r^r^^HC^-—i N w ri -H «1 w CA CA CA CA CA CA CA CA CA 3 3 3 3 3 3 3 3 3 3 3 3 O O O O O O O O o O O O CA Ui CA u CA Ui Ui u Ui u u ui CA C/3 CA CA CA CA u CA CA Ui CA co 3 cd 3 3 ca 3 3 3 ca 3 ca ca 3 ca 3 3 ca ca ca 3 ca ca o. 3 O. O ft O O O o O O ft O g. a O o. O O a O a Ui o. ft a Ui u u Ui u Ui Ui u Ui •> ca CS ca ca ca '? ca ca '? '? ca '? ca o> ;> o. '> aca ca O. '> '> ca '>o '> o. CA £> '>CA a '>CA o. o. '>CA '>CA '>CA ft '?CA '>CA ft 9* CA '>CA >CA '>CA 3 '> 3 > '? 3 '? '> '> '> 3 '>s- 3 3 •> 3 3 •> '> 3 3 3 '> 3 O O •> O O O O •> O O O O O O Ui Ui u u D Ui CD CJ Ui Ut Cl) Ui CD 0) Cl) u '> '> CL> '> '> '> '> '> 0) '> '> u CU u '> 0) u CD ca CL) O. 5 5 O. ft O, o. CU ft ft 3 •« D. C3 C8 5 ft ca *c3 « 13 "3 ca "ia 'S "3 ca "ca ca ca ca ca "03 "ca ut ca ftca "3 ca Tj-r-r-m^j-Tfcon-i^Tj- o 5 *s s 'lil > •îî -s* .5 -s: e ,^- ^ e*. ^ .§ s 11 I §• SS 5 -Si ft CA .& •S •s-ss-a si i s« ä -S 1 C3 Ci I -S13i 5S 3 Q O uj SP s g. o Sj a S g 3 s s o CJI-Ä ?c c ,5 ° S u 3 £ sa -a •S ° •S -a "Si* •§ '5, S. T3 "tï -3 o -5 .: a a ? -S o ^ -Si •o « B. CJ CJ -£ §•" a î; g 5 Ä S •IS § •a ?• Rectum The rectum is situated in the seventh abdominal segment and passes into the epi dermal invagination (Figure 1). It consists of small columnar cells with elliptic nuclei;th eapica lcel lmembran e isline dwit h anintim a (Figure 2G).Bot h dorsally and laterally the muscular coat of the posterior end of the caecal intestine and that of therectu m isconnecte d to theabdomina l body wallb yviscera lmuscles . The cellular structure of the epidermal invagination is identical to that of the foregut. The invagination opens to the exterior via the anal opening which is situated ventral to the cauda (Figure IIA). The anus is opened by six dorsal muscles. They arise on the dorsal abdominal wall, at thejunctio n of the eighth and ninth tergites, and pass downward to their point of insertion on the middle of the dorsal wall of the epidermal invagination. Two pairs of lateral muscles serve to close the anus. Each pair of muscles originates at the junction of the seventh and eighth sternites just lateral to the gonopore, and are inserted on the dorsolateral and ventrolateral walls of the anus, respectively (Figure 12A and 181). The presence of a cuticular lining facing the luminal surface of the rectal cells includesth erectu mwit hth eforegu t asa nectoderma l part ofth edigestiv e system (Figure 19an d 20).Th e cuticle of the epidermal invagination (Figure 8J ) isiden tical to that of the body wall. The endocuticle has a lamellate structure whereas that of the foregut (Figure 5A) and rectum (Figure 81)i s an amorphous mass. The exocuticle of the last two organs is very thin compared with that of the epidermal invagination (Figure 20L). The exocuticle of the rectum and that of the epidermal invagination is shed at each moult with the rest of the exuviae. In the coccid, Planococcus citri Risso, the luminal surface of the rectal cells is lined onlywit h anepicuticl econsistin g ofthre ewel ldefine d electron dense layers (Foldi, 1973). The excrement of the aphid is passed out here as honeydew. Smith (1937) observed that Hyalopterus pruni first raises the tip of its abdomen and then excretes a liquid drop of honeydew which is thrown with considerable force by the distal part of the tibia of one of both hindlegs. WageningenAgric. Univ.Papers 91-5 (1991) 35 Figure 1 I.A. Median longitudinal section of an apterous oviparous fourth stage larva ofPhylloxera coccinea von Heyden. Note the S-shaped flexure of the epidermal invagination. Anal opening in ventral position. B. Median longitudinal section of an alate oviparous larva of Adelges (Sacchi- phantes) abietis. Anal opening in dorsal position. The anal musculature is given in Figures 14H and 12Brespectively . Forlist of abbreviations seepag e 61. Bar represents 10/jm . 36 WageningenAgric. Univ.Papers 91-5 (1991) Figure 12. Transverse sections of the anal musculature of (A) Smynlhurodes betae (anal opening in ventral position) and (B) Adelges (Cholodkovskya) viridana (anal opening in dorsal position). Note the waxy droplets in the fat cells, haemolymph, and endocuticle. For list of abbreviations seepag e 61. Bar represents 10/an . WageningenAgric. Univ.Papers 91-5 (1991) 37 Figure 13.A . Dorsal view of the digestive system of an apterous viviparous larva of Geoicasetulosa reconstructed from serial transverse sections. 1-2, pro- and metathoracic spiracles; 3-9, abdominal spiracles. Bar represents 30/an . Transverse sections of (B) the foregut and (C) descending intestine of G. setulosa; and (D) the anal musculature of G. utricularia. Note the presence of waxy droplets in the fat cells, haemolymph, and endocuticle. For list of abbreviations see page 61. Bar represents 10/im. 38 WageningenAgric. Univ.Papers 91-5 (1991) Figure 14.A. Dorsal view of the digestive system and topographical position of the oenocytes of an apterous oviparous third stage larva of Phylloxera coccineareconstructe d from serial transverse sections. 1-2, meso- and metathoracic spiracles; 3-7, abdominal spiracles. Note the absence of a mycetome. Bar represents 30 pm. Transverse sections of the oesophageal valve (B), stomach with merocrine gland cells (C), second region of the intestine (D), caecal intestine (E), oenocyte and a basophilic mesodermal cell (F), rectum (G), and anal musculature (H) of a second stage larva of P. coccinea. Anal opening in ventral position (Figure IIA). For list of abbreviations see page 61. Bar represents 10/im . WageningenAgric. Univ.Papers 91-5 (1991) 39 Discussion Morphologically and histologically the digestive system of Hyalopterus pruni is identical to that of H.amygdali. Moreover, there is no difference between the several morphs of Hyalopterus, viz.apterou s and alate viviparous females, apterous oviparous females,an d alatemales .Simila rresult shav ebee n obtained for Aphis (Doralis)frangulae Koc h (= Aphisfrangulae Kaltenbac h complex) (Roberti, 1946), Aphis tripolii Laing, and Aphisfarinosa Gmelin , although in the latter an additional loop waslackin g in eight out of sixteen apterous males (Ponsen, 1990b) . Foregut The digestive system of Geoica setulosa (Table 13) consists only of a foregut which isclose d at itsposterio r end without an oesophageal valve,an d ablindl y endingdescendin gintestin e (Figure 13A).Th estomac h and thefirst an d second region of the intestine iscompletel y lacking. In all other aphids the foregut is a thin tube, but in G.setulosa it is a dilated structure and the squamous cells areline dwit h anintim a (Figure 13B). In general iti sassume d that thefunctio n of theforegu t istransportin g liquid food quickly from the pharynx to the stomach. However, in G. setulosath e ingested water and nutrients must be able to pass through the cuticular lining of the foregut. From this it can be concluded that the luminal surface of the intima of the foregut isno t lined with an epicuticle (Figure 5Aan d 19A),sinc e an epicuticle provides the waterproof layer of the epidermal cuticle (Wiggles- worth, 1990). Tripletcell s In all aphid species investigated the second region of the crenated intestine is characterized byth epresenc eo f6- 8group so fthre econical-shape d cells(triplet ) at irregular intervalsamon gth eintestina lcell s(Figur e 2E, 14D, 17D,an d 18E). However, in Phylloxeracoccinea von Heyden, feeding on Quercus rohur, the firstan d second region of thecrenate d intestine isreduce d to a very short tube which consists of 2-3 intestinal cells and 7-10 triplets (Figure 14). The triplet cells are presumably peptidergic endocrine cells which occur as single cells among themidgu t cellso fa number ofinsect s(Billingsley , 1990).I n G. setulosa the stomach and the first and second region of the crenated intestine are com pletely lacking and so also are the triplet cells (Figure 13). This implies that in aphids thereleas e of the substance from the 'endocrine' triplet cellsi sstrictl y confined toth eintestine . Filtersystem In the genera Cryptomyzus (Aphididae; Table 10)an d Eulachnus (Lachnidae), 40 Wageningen Agric. Univ.Papers 91-5 ( 1991) c _o 00 "3 I o e O o o o o E CU E .^ 00 "3 c o U av o c e f*l 00 > <* c u £ xi o 00 0\ w m o o* O oo .O *3 s«2 Ü fe .0 ."3 • .oo .oç 3 2 ë '5 S S .9 Ü o vi tn J3 — 3 -2 -2 3 £ _ S 3 3 e» 3 <: ^ ^ oc oo « ^. •C .B. a ft; s- s. .O T «) e U c M E UH ^^ .2 JG 2 <2 •5 -J "ï5 O S 8 5 3 •3 :5 E J2 U c * 3 PI c S «N^ c 2 EU S 5 ^j S. 3 o o, C C a ia" "o .2 3 c 8. CeUu .Q 2 -J c -5 c/) soc o ^ 3 | X?2 •a is S o 5 •S s: -S -5 -5 o. on 3 c -C «s < Ci, tO t/j II < .s. | s: S 2 -o 3 ^ o C 11 3 .00 '5 .g S S. S S .00 3 8 a 2 o c 5 2 § 5- "a PÎ ^ "3 .Si g. < -s u* -5 2 -2 -S s Cu e. 1* •2 r4" ,£ ,"^ O O ^ Ci, c < OS 5 < Ü hl kl a, to H Aphid Hostplant Locality Adelges lapponicus Cholodkovsky Piceaabies Weissensee (Austria), 20.VII.198 4 Adelges (Cholodkovsky a) viridana (Cholodkovsky) Larix kaempferi Wageningen, 23.VI.198 4 Adelges (Dreyfusia) nordmannianae (Eckstein) Picea orientalis Wageningen, 15.VII.1982 Adelges (Gilletteella) cooleyi (Gillette) Adelges (Sacchiphanles) abietis (Linnaeus) Piceasitchensis Hardenberg, 23.VIL198 2 Adelges (Sacchiphanles) viridis(Ratzeburg ) Picea abies Wageningen, 3.VII.1982 Adelges (Sacchiphanles) viridis (Ratzeburg) Piceaabies Weissensee (Austria), 20.VII .198 4 Pineus orientalis (Dreyfus) Piceaabies Hastière (Belgium), 25.V1I.1985 Picea orientalis Wageningen, 24.VII.1984 where theentir efiltergut ( = the anterior region of the midgut) isencapsulate d byth eanterio r region of thecaeca l intestine, thewal lo fth e filterchamber adja cent to the stomach isline d with filterchamber cells,wherea s the opposite wall isline d with caecal intestinecell s(Figur e 22).A n identical cellular arrangement occurs in the filterchamber of Longistigma caryae(Harris ) (Lachnidae) where the entire stomach is encapsulated by the anterior region of the 'hindgut' (Knowlton, 1925),an d in thefilterchamber o f Hyalopterusa n Coloradoawher e only the anterior region of the stomach is encapsulated by the anterior region of the caecal intestine (Figure 3A). In the Drepanosiphidae where the entire stomach isencapsulate d by the blindly ending intestine,filterchamber cell s do not occuri nth efilterchamber (Ponsen , 1979).Phloeomyzus passerinii (Signoret ) does not have filterchamber cells in the anterior region of the caecal intestine (Figure4F) ;th eintestina lcell sen dabruptly ,an dth esquamou scell so fth ecaeca l intestine begin. In the superfamily Cicadoidea thefiltersystem comprise s the anterior region of the stomach, around which areloope d the posterior extremity of themidgu t and the anterior portion of the Malpighian tubules each being enveloped by the walls of the stomach between two adjacent folds (Figure 10an d Table 5 in Ponsen, 1979). In this system the anterior region of the stomach is formed on one side by cuboidal cells, whereas the surface in contact with the internal Malpighiantubule san dinterna lmidgu tconsist so fver yflattene d epithelialcell s (Licent, 1912;Marshal l and Cheung, 1974).I n Cicadulasexnotata (= Macros- telessexnotatus (Fallen) )th echaracte r ofth estomac hcell sadjacen t toth e fused midgut changes abruptly after staining with Wright's solution (Dobroscky, 1931).O n the other hand, in Hyalopterus and Coloradoa there isn o difference in structure of thecell sadjacen t to the filterchamber and those on the opposite wallo fth estomac h (Figure2 A) ,a si sals oth ecas ei nspecimen swithou t a filter- system. The several forms of the filtersystem and their cellular arrangement withinth eorde r Hemiptera hasalread y beendiscusse d (Ponsen, 1979). It is interesting that on Phragmites three times more Hyalopterus specimens with afiltersystem occu r than on Prunus (Table 4).Thi s feature indicates that 42 Wageningen Agric. Univ. Papers 91-5 (1991) the filtersystem must have a function. The function of the filtersystem is the removal of the excess of water in the ingested liquid food from the filtergut or stomach via the filterchamber cells to the lumen of the caecal intestine. In aphid specieswithou t afiltersystem (Tabl e 11) theexces swate ri sremove d from theforegu t orstomac h toth ehaemolymp h and from therevi ath e filterchamber cells to the lumen of the caecal intestine (Figure 4). However, aphid specieso f the families Adelgidae, Mindaridae, Thelaxidae, Chaitophoridae, Drepanosi- phidae,Anoeciida e and Greenideidae, and theAphisgroup, wichhav en o filter- chamberscells ,th eexces swate ri sremove dfro m thehaemolymp hvi ath edescen dingintestin e cellst o theexterio r ashoneydew . Inconclusio n the filterchamber cells are probably a remnant of the descending intestine and have the function ofwate r regulation inaphi d specieswit h acaeca lintestine . Rectum Generally in insects the transition from the endodermal midgut to the ectoder malhindgu t isinserte d with Malpighian tubules.I nth esuperfamil y Aphidoidea Malpighian tubulesar eabsen t (Ramdohr, 1811; Morren, 1836;Witlaczil , 1882), aswel la si nal lmorph so fHyalopterus (Figur e 1) and C. tanacetina. In Geoica setulosa, G.utricularia, Smynthurodes betae,an d Tetraneura ulmi (Eriosomatidae;Tabl e 13) thedescendin g intestinepasse sventrall y intoa recta l bladder, a relatively voluminous structure somewhat extended anteriorly (Fig ure 15).Th e rectal bladder consistso f squamous cellsan d their luminal surface is lined with an intima similar to that of the foregut. The bladder is kept in position byviscera lmuscle swhic h areconnecte d to theabdomina l integument. Insideth erecta l bladder isa glandlik eorga n consistingo fabou t 22lon gconica l cells.Th ecytoplasmi c filaments of theconica lcell sar ejoine d to astal k inserted onth etransitio n from thedescendin gintestin et oth erectum .Thi sorga ni sprob ably homologouswit h theorigina l Malpighian tubuleswhic hhav e disappeared duringth eevolutio n ofth e Aphidoidea. A similar glandlike organ is lacking in the remaining species listed in Table 13, and in all other aphid species investigated. However, in Fordaformicaria and F.marginata theposterio r end of thedescendin g intestine, the rectum, and the anterior region of the epidermal invagination are encapsulated by a ring ofpolygona lcell s(Figur e23) .Thes ecell sar eidentica l toth eindividua l basophi licmesoderma l cells,whic h are evenly dispersed among the fat cells(Figur e 23 in Ponsen, 1972). The dorsal region of the rectum of Schoutedenia lutea(va n derGoot )(Famil yGreenideidae )i sbuil tu po fcolumna r'gland 'cell sbu twithou t acuticula r lining(Figur e 15B). Anal opening In the majority of aphid speciesincludin g Hyalopterus and Coloradoa the anal opening issituate d ventral to thecaud a (Figure IIA). In the Adelgidae (Balch, 1952),Geoica setulosa, G. utricularia, and Smynthurodesbetae th eanu si sdorsa l WageningenAgric. Univ. Papers91-5 (1991) 43 Figure 15.Media n longitudinal section of the rectal bladder and rectal gland of Geoica utricularia (A), Smynthurodes betae (C),&nd Tetraneura ulmi(D ) (Table 12).B.Transvers e section of the rectal gland cellso n thetransitio n ofth edescendin g intestine and theepiderma l invagination in Schoutede- nialutea (va n der Goot). For list of abbreviations seepag e 61. Bar represents 10 /an. 44 WageningenAgric. Univ.Papers 91-5 (1991) Aphis-group Aphididae CD CD VJ, U ! U ' \J * \J , U : ! Anoeciidae Phloeomyzus .—~-^ Acaudinum /^#*~"N Hyalopterus —-— Capitophorus "^ Cryptomyzus fie fig-t ¥rVt * (UWi <Û é Drepanosiphidae Subsatlusaphis Paoliella nn nn an M M on fui on Mi 11 fit ,'di Hwtï ii il:.4 1 •••» Adelgidae Thelaxidae Chaitophoridae Greenidea IsraelaphisIsrae CD CD CD CD W«\ Figure 16.Diagram s illustrating theexistin gan d hypothetical (?)form s ofth edigestiv e system within the Aphidoidea. The dashed line represents the descending intestine, and the dotted line the caecal intestine. For list of abbreviations seepag e 61. WageningenAgric. Univ.Papers 91-5 (1991) 45 to the cauda (Figure IIB), and in Fordaformicaria and F. marginata the anus is in a terminal position (Heie, 1980). In the Phylloxeridae an anal opening is lacking since they do not emit honeydew (Dreyfus, 1894;Kunkel , 1966). However, in Phylloxera coccinea the epidermal invagination is a very thin tube showing a S-shaped flexure which terminates at the anal opening ventral to the cauda (Figure 11A) . The anus iscontrolle d by two pairs of lateral muscles (Fig ure 14H),bu t lacks the anal dorsal muscles (Figure 12A).A n identical S-shaped flexure occurs in the common afferent salivary duct of which the opening to the pumpchamber is controlled by one pair of muscles (Figure 5 in Ponsen, 1972). Phylogeny In general the digestive system of aphids consists of a foregut which opens into an oesophageal valve, a tubular or dilated stomach, the first and second region of the crenated intestine, a smooth transparent intestine, a rectum, and an epi dermal invagination terminating at the anal opening (Figure 10). According to Hille Ris Lambers (1964) and Heie (1967) the Adelgidae and Phylloxeridae may be considered as the phylogenetically oldest family of the Aphidoidea. The digestive system of the Adelgidae consists of a short foregut, a tubular stomach situated inth emiddl eo fth eaphid , and adescendin g intestine. The first region of the crenated intestine lies in a direct line with the stomach (Figure 16an d 17). In the Thelaxidae the tubular stomach is situated centrally, close to the dorsum of the aphid, whereas the crenated intestine runs from the stomach directly ventrally and then passes posteriorly to the abdominal loop. The digestive system of the Chaitophoridae is similar to that of the Thelaxidae, however, in the Chaitophoridae there are genera and even individuals of some species that have or lack an additional loop in the second region of the crenated intestine (Ponsen, 1990C) .I n the genera Greenideaan d Israelaphis of the family Greenideidae, the stomach bends ventrally tojoi n the crenated intestine (Figure 16). The most characteristic structure of the Aphis-growp is the transition from the dilated stomach to the crenated intestine, which could have evolved from the type (Figure 16,1 and III) seen in the Thelaxidae and Chaitophoridae, via a weak loop being an intermediate form (II and IV) to the evolutionary final form, marked by a sharp loop (V). This final form of transition (V) in Aphis isrepresentativ e for the Anoeciidae, with or without an additional loop. Within the family Drepanosiphidae there are certainly three, and possibly sixanatomicall y distinct groups ofaphids .I n the first group thetubula r stomach liesventrally , and starts in one of the first five abdominal segments (Figure 16A- B). In Drepanosiphum acerinum and D. aceris the stomach starts in the sixth abdominal segment and iscurve d (Figure 16C).Th e second group (Figure 16E) has two smooth transparent intestines: the descending intestine which is a con tinuation of the ascending intestine, and the caecal intestine which is a blindly endingevaginatio n of the rectum (Figure 10B).Bot h transparent intestines form 46 WageningenAgric. Univ.Papers 91-5 (1991) a filtersystem: a concentric filtersystem in which the stomach is encapsulated byth e caecal intestine (Figure 9B)an d a parallel filtersystem in which the anteri or region of the ascending intestine is fused with the posterior region of the descending intestine (Figure 9C). Paoliella terminaliae (Hall), a representative of the third group, lacks a filtersystem (Figure 16D). The other three groups are hypothetical (Figure 16F-H). They are likely to have either a concentric filtersystem or aparalle l filtersystem, with or without a caecal intestine. The two types of smooth transparent intestines can be histologically distin guished from each other. The caecal intestine has a simple squamous epithelial lining the cells of which have elongated or elliptical nuclei. The cells contain granules and irregular membraneless 'vesicles' (Figure 7G) in which occur waxy droplets. The apical cell membrane presents irregular fingerlike evaginations in which occur small oblong mitochondria. The descending intestine consists of either cuboidal or triangular cellswit h more or less spherical nuclei and cyto plasmic vacuoles. The apical cell membrane presents a labyrinthine system of closely packed irregular invaginations of different dimensions (Figure 6D, 7F and 20).I n dissections both smooth transparent intestinesexhibit s vigorous per istaltic movements generated by circular and longitudinal muscles. The transi tion from the second region of the crenated intestine to the descending intestine is marked by a gradual increase of 2-4 intestinal cells followed by an abrupt change to the typical cellular structure of the descending intestine. Species belonging toth efamilie s Adelgidae (Figure 17),Mindarida e (Figure 18),Thelax - idae, Chaitophoridae, Greenideidae, Drepanosiphidae, Anoeciidae, and the genus Aphis allhav e a descending intestine (Figure 16). During evolution the descending intestine was presumably replaced by the caecal intestine (Figure 10),bu t with the retention of the concentric filtersystem. Species with such a structure occur in the family Lachnidae, and the genera Acaudinum, Capitophorus, and Cryptomyzus (Figure 16) (Ponsen, 1977, 1981). In these species the anterior region of the midgut (= filtergut) is encapsulated by the anterior region of the caecal intestine (Figure 22). A similar structure occurs in Hyalopterus and Coloradoa, where the anterior region of the stomach is encapsulated by the anterior region of the caecal intestine. This concentric filtersystem is very primitive in comparison with that of the above mentioned family and genera. This primitive filtersystem occurs in 20% of the specimens of Hyalopterus on Prunus and 56% of those on Phragmites (Table 4).Th e pres ence of a filtersystem in Coloradoai s26 % (Table 2). In the remaining specimens the stomach isno t encapsulated by thecaeca l intestinewhic h iscompletel y sepa rated from the stomach and forms a more or less spherical structure (Figure 2H, 3 and 4A). The anterior region of the caecal intestine that envelopes the filtergut or the anterior region of the stomach is the filterchamber (Figure 2A). It is lined with both filterchamber and caecal intestine cells, but arranged so that the filter- chamber cells are situated on the side adjacent to the stomach while the squa mous caecal intestine cells are on the opposite wall of the filterchamber. The number of filterchamber celllsgraduall y decreases until the caecal intestine con- WageningenAgric. Univ.Papers 91-5 (1991) 47 Figure 17.A. Dorsal view of the digestive system of an alate oviparous larva of Adelges (Sacchi- phantes) abietis reconstructed from serial transverse sections. 1-2, pro- and metathoracic spiracles; 3-8, abdominal spiracles. Bar represents 30 /un. Transverse sections of the (B) oesophageal valve and (C) stomach of Adelges (Dreyfusia) nordmannianae; (D) second region of the intestineo f Pineus orienlalis; (E) the beginning and (F) halfway the descending intestine of Adelges (Sacchiphantes) viridis; and (G) the rectum of Adelges (Gillelteellaj cooleyi (Table 14). For list of abbreviations seepag e 61. Bar represents 10 urn. 48 Wageningen Agric. Univ. Papers 91-5 (1991) Figure 18.A. Dorsal view of the digestive system and topographical position of the oenocytes of an apterous oviparous larva of Mindarus abietimis Koch reconstructed from serial transverse sec tions. The siphuncular pores (CO) are situated on the sixth abdominal tergite. Bar represents 30 //m. Transverse sections of the oesophageal valve (B), stomach (C), first (D) and second region of the intestine (E), descending intestine (F), rectum (G), epidermal invagination (H), and anal musculature (I) of M. abietinus. Anal opening in ventral position. Note the waxy droplets (W) in the fat cells, haemolymph, and endocuticle. For list of abbreviations see page 61. Bar represents 10pm. Wageningen Agric. Univ. Papers 91-5 (1991) 49 Figure 19. Schematic representation of the apical cell membrane of the foregut (A, second stage), outer layero fth eoesophagea l valve (B,first stage) ,stomac h (merocrinesecretion ; C,Myzus persicae; D, Subsaltusaphis ornata), and triplet cell (E) (Table 12). For list of abbreviations seepag e 61.Ba r represents 0.5 /an. 50 WageningenAgric. Univ.Papers 91-5 (1991) Figure20 .Schemati crepresentatio n ofth eapica lcel lmembran e ofth ecrenate d intestine (F),descen ding intestine (G, Subsaltusaphis ornata;H , Aphisfabae), caecal intestine (I), rectum (J, Drepanosi- phum platanoidis; K, Subsaltusaphis ornatä), and epidermal invagination (L) (Table 12). For list of abbreviations seepag e 61. Bar represents 0.5 /im. WageningenAgric. Univ.Papers 91-5 (1991) 51 Figure 21. Transverse sections of the most contracted (A) to the most dilated position of the caecal intestine forming a more or less spherical shape (B) to the most bizarre shapes (C-G). For list of abbreviations seepag e 61. Bar represents 10/mi . 52 WageningenAgric. Univ.Papers 91-5 (1991) Figure 22. Transverse section of the filtersystem of Eulachnus brevipilosus Borner (A) and that of Cryptomyzus ribisLinnaeu s (B,modifie d after Ponsen, 1977)showin gencapsulatio n ofth e filtergut by the anterior region of the caecal intestine. Bar represents 10 jjm. C. The basic principle of the filtersystem. For list of abbreviations seepag e 61. WageningenAgric. Univ.Papers 91-5 (1991) 53 Figure 23. Transverse sections of the middle region (A) and the posterior end of the descending intestine (B), rectum (C), and epidermal invagination (D) of Forda marginala showing position of the 'basophilic mesodermalcells' . Bar represents 10/im . For list of abbreviations seepag e 61. 54 WageningenAgric. Univ.Papers 91-5 (1991) Figure 24. Topographical position of oenocytes (A) and mycetome (B) of an apterous viviparous larva of Hyalopterus, reconstructed from serial sections. 1-2, meso - and metathoracic spiracles; 3-9, abdominal spiracles. Bar represents 30/mi . Amycetocyte , oenocyte, and a basophilic mesoder mal cell of an alate male of Hyalopterus (C),an d those of an apterous oviparous larva of Coloradoa tanacetina (D).Ba r represents 10/mi . For list of abbreviations seepag e 61. WageningenAgric. Univ.Papers 91-5 (1991) 55 sists of only squamous cells (Figure IB and 3A). This cellular arrangement also occurs in the filterchamber of aphid species belonging to the family Lachnidae (including Eulachnus, Figure 22A), and the genera Acaudinum, Capitophorus, Cryptomyzus (Figure 22B), Hyalopterus(Figare 2A), and Coloradoa. An identi cal cellular arrangement is present in the anterior region of the caecal intestine ofthos e specimens ofHyalopterus and Coloradoatha t lacka filtersystem (Figure 2H and 3B). It appears that all aphid genera with a filtersystem have a caecal intestine. Onth eothe r hand, therear egenera ,liste di nTabl e 11,tha t havea caeca l intestine but lack a filtersystem. In these genera the cellular arrangement in the anterior region of the caecal intestine is identical to that in specimens of Hyalopterus and Coloradoa with and without a filtersystem (Figure 3 and 4A-E). Probably allth especie si nTabl e 11 that havea caeca lintestin ema y haveha d a filtersystem, which has beenlos t duringevolution . Allgener a inTabl e 11 belong to the family Aphididae, excluding the genera Anuraphis, Aphis, Brachycaudus, Plocamaphis, and Pterocomma, which have adescendin g intestine. During evolution thecaeca l intestine hasincrease d inlengt h with an exponen tial increase in the number ofcells . In the species of the family Drepanosiphidae with a filtersystem the total number of cells of the caecal intestine varies from 13 to 19, in Phylloxera coccinea from 14 to 16, in Phloeomyzus passerinii from 52 to 54, and in the family Aphididae from 40 in Idiopterus nephrolepidis to 322i n Macrosiphum albifrons (Table 11). It is interesting that within the family Aphididae (Table 11) the majority of the genera have had a filtersystem, whereas inthre e genera all specimens possess a filtersystem (Acaudinum, Capitophorus, and Cryptomyzus), and in two genera specimens occur with or without a filtersystem (Hyalopterus and Coloradoa). Probably there occur among the not yet investigated genera within the family Aphididae, other genera of theAcaudinum (Figure 22)a s Hyalopterus-type (Fig ure 3). Mycetome and oenocytes In both alate and apterous viviparous females, oviparous females and males of Hyalopterus and C. tanacetina the mycetome consists of two longitudinal masses ofmycetocyte swhic hru n from themetathora x to the seventh abdominal segment; in the fourth abdominal segment theyjoi n together to separate subse quently in the sixth abdominal segment (Figure 24B). The total number ofmycetocyte s in Hyalopterus isabou t 52an d that in Color adoa about 34. The scanty cytoplasm of the mycetocytes is completely filled with globular cell organelles. These organelles multiply by binary fission and have a diameter of 2.7 p.m.Eac h mycetocyte has an irregularly-shaped nucleus due to the pressure ofth emultiplyin g globular organelles (Figure 24C-D). The mycetome is surrounded by a nucleated sheath. During larval life the mycetome disintegrates into clusters ofmycetocyte s orindividua l ones.Th e nuc- 56 WageningenAgric. Univ.Papers 91-5 (1991) leated sheath breaks open and a part of it remains connected with the separated mycetocytes. The degeneration process of the mycetocytes by which the globules areliberate d into thehaemolymph , has already beendescribe d (Ponsen, 1972). Against the lateral mycetome the oenocytes are situated. During larval life the oenocytes partly become separated from the mycetome. They are situated in the body cavity between the mesodermal tissue and the internal organs of the thorax and the first seven abdominal segments (Figure 24A).Th e majority of them occur as single cells, but sometimes in groups of 2-3 cells in intimate contact with each other. The oenocytes contain many vacuoles and granules; their development dur ingembryoni c and larvallif eha salread ybee ndescribe d (Ponsen, 1972).I n Hyalop- terusther ear e about 40oenocyte san d in Coloradoaabou t 20. In all aphid species investigated there occur in the body cavity oenocytes and amycetome .Th etota lnumbe ro foenocyte svarie sfro m4 fo r Phloeomyzuspasserinii to5 6fo r Macrosiphumalbifrons. However,bot hPhylloxera coccinea an dCerataphis palmaelac ka mycetom e(Profft , 1937;Büchner , 1958),bu tth eoenocyte sar epresen t (Figure 14). On the other hand, in Geoicautricularia ther e occurs a mycetome, but no oenocytes. In another species of this genus, Geoicasetulosa, both themyce tome and themycetocyte s arelacking ,bu t theviviparou s embryosi nvariou s stages of development growing parthenogenetically in their mother's ovarioles, all have a mycetome. The mycetocytes are completely filled with globular cell organelles, identicalt othos eo fGeoica utricularia, Hyalopterus, an d Coloradoa(Figur e24C-D) . Themycetocyte si nSubsaltusophis ornata ar ecompletel yfille dwit h irregular-shaped organelleswhic hmultiply bya buddin gprocess . The oenocytes are situated in the body cavity and the basophilic mesodermal cellsar eeve ndisperse dindividuall yamon gth efa tcell s(Figur e 12B,14 ,an d24C-D) . Summary Thedigestiv esyste mo fHyalopterus and Coloradoaconsist so fa foregut , oesopha geal valve, a dilated stomach, a crenated intestine, caecal intestine, rectum, and an epidermal invagination, which terminates at the anal opening. The anterior region of the stomach of Hyalopterus consists of apocrine cells and the posterior region of merocrine cells. In Coloradoath e stomach isline d with merocrine cells. The transition from the stomach to the crenated intestine is marked by a sharp loop. The second region of the crenated intestine contains one or two additional loops and is characterized by the presence of 6-8 groups of three cells (triplets) at irregular intervals among the intestinal cells. The caecal intestine is a smooth transparent structure made up of squamous cells with elliptic nuclei. In about 20% of the specimens of Hyalopterus on Prunus and in about 56% of those on Phragmites the anterior region of the stomach is encapsulated by the anterior region of the caecal intestine, forming a concentric filter-system. In Coloradoa about 26% of the specimens have a filtersystem. In the remaining specimens of both genera the stomach isno t encapsulated byth ecaeca lintestine .Thi s phenom enon isdescribe d in detail and isdiscusse d in thecontex t of the family Aphididae. WageningenAgric. Univ.Papers 91-5 (1991) 57 Acknowledgements I am most grateful to the late Dr. D.Hill e Ris Lambers,t o Ing.A . van Harten (Praia, Cabo Verde), and to Miss J.D. Prinsen (Institute for Plant Protection, Wageningen)fo rcollectin gan didentifyin g ofth eaphids . I wish to express my thanks to Dr. S. Barbagallo (Instituto di Entomologia Agraria, Universita Catania, Sicilia, Italy), to Dr. Ch. Brough (University of East Anglia, Norwich, England), to Professor Dr. P.H. Hewitt (University of Orange Free State, Bloemfontein, South Africa), to Dr. J. Holman (Institute ofEntomology , CeskéBudejovice , Czechoslovakia), toDr . F.A .Ilharc o (Esta- cao Agronomica Nacional, Oeiras, Portugal), to Dr. H. Loxdale (Rothamsted Experimental Station, Harpenden, England), to Dr. M. Miyazaki (National Institute of Agro-Environmental Sciences, Ibaraki, Japan), to Dr. T.K. Singh (Life SciencesDepartment , Manipur University, Conchipur, India),an d to Dr. M.B. Stoetzel (Systematic Entomology Laboratory, Beltsville, Maryland, U.S.A.)fo r collectingan dsendin go fth eaphids . Thanks are also due to Ing. P.W.T. Huisman (Department of Entomology, Agricultural University, Wageningen) and to Mr. P.G.M. Piron (Institute for Plant Protection, Wageningen) for collecting of the aphids in Hungary, to Dr. L.Turkenstee n (Institute for Plant Protection, Wageningen) in Central Africa, and to Professor Dr. A.F.G. Dixon (University of East Anglia, Norwich, Eng land)an dt oDr .P .Welling si nAustralia . Iexpres sm ythank s toIr . F.L.Dielema n (Department ofEntomology ,Agri cultural University, Wageningen),t o Ir.P .va n Dijk (Institute for Plant Protec tion, Wageningen), to Dr. C.C. Payne (Glasshouse Crops Research Institute, Littlehampton, England), and to Dr. M.G. Solomon (East Mailing Research Station, Maidstone,England )fo r theaphid sreare di nthei r Insectarium. I am indebted to Professor Dr. A.F.G. Dixon (University of East Anglia, Norwich,England )fo r valuablesuggestion san dfo r correctingth eEnglis h text. I am also very grateful to Professor Dr. J.C. van Lenteren for his approval toprepar ethi sinvestigation si nth eDepartmen t ofEntomology . References Balch, R.E., 1952. Studies of Adelges piceae (Ratz.) (Homoptera: Phylloxeridae) and its effects on Abies bahamea (L.) Mill.Canadia n Department ofAgriculture , Publication, 867: 1-76 . Basky, Z., 1974. Data on the biology of Hyalopterus pruni (Geoffr.). Plant Protection 10(2) : 71-73 (in Hungarian). Basky, Z., 1978. The morphology and the hostplant changing ability of Hyalopterus pruni species complex. Dissertation, Kecskemet, 129pp . (in Hungarian). Basky, Z. and Szalay-Marszó, L., 1987. Study of isolation mechanisms in the Hyalopterus pruni and Hyalopterus amygdali complex. Proceedings of International Symposia, Smolenice, Czechos lovakia, 9-14, 1985. Billingsley, P.F., 1990. The midgut ultrastructure of hematophagous Billingsley, P.F., 1990. The midgut ultrastructure of hematophagous insects.Annua l Review of Entomology 35:219-248 . 58 WageningenAgric. Univ.Papers 91-5 (1991) Bodenheimer, F.S. and Swirski, E., 1957. The Aphidoidea of the Middle East. The Weizmann SciencePres s of Israel,Jerusalem , 378pp . Borner,C , 1938.Neue r Beitrag zur Systematik und Stammesgeschichte der Blattläuse. Abhandlun gen des Naturwissenschaftlichen Vereins Bremen 30: 167-179. Borner,C , 1952.Europa e centralis Aphides (DieBlattläus e Mitteleuropas). Mitteilungen des Thür inger Botanischen Gesellschaft, Beiheft 3:1-484. Börner, C. and Heinze, K., 1957. Aphidina-Aphidoidea, Blattläuse, plantlice (aphids), pucerons (aphides).In :P .Sorauer , Handbuch der Pflanzenkrankheiten, 5:1-402.Pau l PareyVerlag , Berlin, Hamburg. Buchner, P., 1958. Eine neue Form der Endosymbiose bei Aphiden. Zoologischer Anzeiger 160: 222-230. Dobroscky, I.D., 1931.Morphologica l and cytological studies on thesalivar y glands and alimentary tract of Cicadulasexnotata (Fallen), thecarrie r of aster yellows virus. Contributions of the Boyce Thomson Institute 3:39-58 . Dreyfus, L., 1894. In J. Krassilstschik's Mitteilungen über 'die vergleichende Anatomie und Syste matik der Phytophthires' mit besonderer Bezugnahme auf die Phylloxeriden. Zoologischer Anzeiger 17:237-243. El-Kady, E.A., Hassan, M.S. and Attia, A.A., 1970. Studies on the life-cycle of Hyalopteruspruni (Geoffroy), in Egypt (Hemiptera-Homoptera: Aphididae). Bulletin Société entomologique d'Egypte 54:579-582 . Foldi, I., 1973. Etude de la chambre filtrante de Planococcus citri (Insecta, Homoptera). Cell and Tissue Research 143: 549-568. Forbes, A.R., 1964. The morphology, histology, and fine structure of the gut of the green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae). Memoirs of the Entomological Society of Canada 36:1-74. Gildow, F.E., 1985. Transcellular transport of barley yellow dwarf virus into the hemocoel of the aphid vector, Rhopalosiphumpadi. Phytopathology 75:292-297. Heie, O.E., 1967. Studies on fossil aphids (Homoptera: Aphidoidea), especially in the Copenhagen collection of fossils in Balticamber . Spolia Zoologica Musei Hauniensis Copenhagen 26:1-274. Heie, O.E., 1980.Th e Aphidoidea (Hemiptera) of Fennoscandia and Denmark.I.Th e families Min- daridae, Hormaphididae, Thelaxidae, Anoeciidae, and Pemphigidae. Fauna Entomologica Scan- dinavica9:1-236. Hille Ris Lambers, D., 1944. Weitere Aphiden von Borkum (Hemiptera-Homoptera: Aphididae). Arbeiten über physiologische und angewandte Entomologie aus Berlin-Dahlem 11:152-156. Hille Ris Lambers, D., 1964.Highe r categories of the Aphididae. In: Heie,O.E. , 1967. Ilharco, F.A., 1966.Afideo s das fruteiras dePortuga l continental. Agronomia Lusitana 27: 1-86. Janiszewska, J., 1932.Untersuchunge n über die Hymenoptera Aphidius sp., Parasiten der Blattlaus Hyalopterus pruni Fabr. Bulletin International de l'Académie polonaise des sciences et des lettres 7BII : 277-293. Knowlton, G.F., 1925.Th e digestive tract ofLongistigma caryae (Harris). OhioJourna l of Science 25:244-252. Kunkel, H., 1966. Ernährungsphysiologische Beziehungen der Stenorrhynchen zur Wirtspflanze unter besondere Berücksichtigung der Coccina und Aphidina. Dissertation, University of Bonn, 172 pp. Kunkel, H. and Kloft, W., 1977.Fortschritt e auf dem Gebiet der Honigtau-Forschung. Apidologie 8:369-391. Leonard, M.D., 1968.Californi a aphids in the Cornell University Collection (Homoptera: Aphidi dae). Cornell University Agricultural Experiment Station Memoir 407: 3-31. Licent, E., 1912.Recherche s d'anatomie etd ephysiologi ecomparée s sur letub edigesti f des Homop- tères supérieurs. La Cellule 28:1-161. Marshall, A.T. and Cheung, W.W.K., 1974. Studies on water and ion transport in homopteran insects: ultrastructure and cytochemistry of the cicadoid and cercopoid Malpighian tubules and filter chamber. Tissue &Cel l6 : 153-171. Morren, M.Ch., 1836. Mémoire sur l'émigration du puceron du pêcher (Aphis persicae), et sur lescaractère s etl'anatomi e decett e espèce.Annale s des Sciences Naturelles, Zoologie 6:65-93 . WageningenAgric. Univ.Papers 91-5 (1991) 59 O'Loughlin, G.T. and Chambers,T.C. , 1972.Extracellula r microtubules in theaphi d gut. The Jour nal ofCel lBiolog y 53: 575-578. Ponsen, M.B., 1969. Theeffec t ofpotat o leafroll viruso n thebiolog y ofMyzuspersicae. Wageningen Agricultural University papers 75; 360-368. Ponsen, M.B., 1972. The site of potato leafroll virus multiplication in its vector, Myzus persicae. An anatomical study.Wageninge n Agricultural University papers 72-16: 1-147. Ponsen,M.B. , 1977.Th egu t ofth ere dcurran t blister aphid, Cryptomyzus ribis(Homoptera : Aphidi- dae). Wageningen Agricultural University papers 77-11:1-11. Ponsen,M.B. , 1979.Th edigestiv esyste mo fSubsaltusaphis ornata(Homoptera : Aphididae). Wagen ingen Agricultural University papers 79-17: 1-30. Ponsen, M.B., 1981.Th edigestiv e systemoîEulachnus brevipilosusBorne r(Homoptera : Aphididae). Wageningen Agricultural University papers 81-3:1-14. Ponsen, M.B., 1990 a. The phylogenetic implications of the structure of the alimentary tract of theAphidoidea.I . Greenidea,Israelaphis, and Neophyllaphis. Wageningen Agricultural University papers 90-4:3-19 . Ponsen, M.B., 1990 b. The phylogenetic implications of the structure of the alimentary tract of theAphidoidea.il . The Aphis-group- Wageningen Agricultural University papers 90-4:23-52 . Ponsen, M.B., 1990 c. The digestive system of Hyalopterus and its bearing on the evolution of the structure ofth edigestiv esyste mi nth eAphidoidea . Acta Phytopathologica etEntomologic a Hun- garica 25(1-4) :261-272 . Profft, J., 1937. Beiträge zur Symbiose der Apiden und Psylliden. Zeitschrift für Morphologie und Ökologie der Tiere 32:289-326 . Ramdohr, K.A., 1811.Abhandlun g über dieVerdauungswerkzeug e der Insecten. Halle, 221 pp. Roberti, D., 1946.Monografi a dell Aphis (Dorsalis) frangulae Koch.I. Morfologia, anatomia, isto- logia. Bolletino della Regia Laboratoria Entomologia Agraria di Portici 6: 127-312. Robinson, A.G., 1972. Annotated list of aphids (Homoptera: Aphididae) collected in Thailand, with description of a new genusan d species.Canadia n Entomologist 104:603-608. Robinson,A.G . and Bradley,G.A. , 1968.A revise d listo faphid s ofManitoba . Manitoba Entomolo gist 2:60-65. Schouteden, H., 1903. Les Aphidocécidies Paléarctiques. Annales de la Société entomologique de Belgique 47: 167-195. Shen Tseng and Chia-chu Tao, 1936. A list of the Aphididae of China with descriptions of four new species.Entomolog y &Phytopatholog y 4: 120-176. Smith, L.M., 1936. Biology of the mealy plum aphid, Hyalopterus pruni (Geoffroy). Hilgardia 10: 167-211. Smith, L.M., 1937.Growth , reproduction, feeding, and wing development of themeal y plum aphid in relation to climatic factors. Journal of Agricultural Research 54:345-364 . Spampinato, R., Arduino, P., Barbagallo, S., and Bullini, L., 1988.Analis i genetica di Hyalopterus pruni eH. amygdali edimostrazion e dell' esistenza di una nuova specie(Homoptera , Aphidoidea). Atti XV Congresso nazionale italiana Entomologia, L'Aquila:261-265 . Stroyan, H.L.G., 1984. Aphids - Pterocommatinae and Aphidinae (Aphidini). Handbooks for the Identification of British Insects 2(6) :1-232 . Taylor, C.E. and Gair, R., 1954. A preliminary annotated list of aphids of certain East Midland Counties. The North Western Naturalist 29:512-525 . Theobald, F.V., 1927.Th e plant liceo r Aphididae of Great Britain. Volume II,41 1pp . Wigglesworth, V.B., 1990.Th e distribution, function and nature of 'cuticulin' in the insect cuticle. Journal of Insect Physiology 36: 307-313. Willcocks, F.C., 1916. Some notes on the mealy plum aphid Hyalopterus pruni, Fabricius. Bulletin dela Société Entomologique d'Egypte 4:33-37 . Witlaczil, E., 1882. Zur Anatomie der Aphiden. Arbeiten aus den Zoologischen Instituten der Universität Wien 4: 397-441. 60 Wageningen Agric. Univ.Papers 91-5 (1991) Abbreviations usedi n figures adm anal dorsal muscles hg hindgut ai ascending intestine il first region of intestine al abdominal loop i2 second region of intestine ali additional loop of intestine in intima alm anal lateral muscles is intravalvular space ao anal opening 1 lumen bl basal lamina Is labyrinthine system bmc basophilic mesodermal cell m mitochondrion ce compound eye mbv membraneless vesicle ci caecal intestine mvs microvillar system cic caecal intestine cell M2 circular muscle fibres CO siphunculus (cornicle) Mil longitudinal muscle fibres etc connective tissuecel l n nucleus di descending intestine oen oenocyte ecm ecdysial membrane ov oesophageal valve ecu embryonic cuticle Pi plaques ei epidermal invagination r rectum em extracellular microtubules reb rectal bladder encu endocuticle rg rectal gland epcu epicuticle rgc rectal gland cell excu exocuticle sj septatejunctio n f foregut st stomach fac fat cell to triommatidion fe fingerlike evaginations tpc triplet cells fh flabellate hair vm visceral muscles fie filterchamber w waxy droplet ficc filterchamber cell wc wax cell fig filtergut wp wax plate with pores fm fibrous mass wr wax reservoir go gonopore za zonula adherens WageningenAgric. Univ.Papers 91-5 (1991) 61