Anatomical alterations of leaves of weed plant Galium mollugo L. (Rubiaceae) caused by eriophyoid mite Aculus anthobius (Nal) are described and quantified. Symptoms can be considered as leaf rolling (galls). Anatomical alterations are expressed as destructions of epidermal cells of upper and under surface of leaves and they can be classified as toxemias.U radu su opisane i kvantifikovane promene na listovima korovske vrste Galium mollugo L. (Rubiaceae) prouzrokovane ishranom eriofidne grinje Aculus anthobius (Nal) (Acari:Eriophyoidea). Simptomi koji se manifestuju uvijanjem ivica listova se mogu uvrstiti u promene tipa gala. Na anatomskom nivou promene se manifestuju u vidu destrukcije epidermalnih ćelija lica i naličja lista koje se mogu prema sadašnjoj klasifikaciji (Westphal & Manson,1996) smatrati toksemijama. Ukazano je na potrebu da se opišu i druge slične promene izazvane drugim vrstama eriofida na istoj i /ili srodnim vrstama roda Galium radi jasnog razgraničenja uticaja na biljku domaćina

Petanović, Radmila

Rančić, Dragana

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ANATOMICAL ALTERATIONS OF GALIUM MOLLUGO L.LEAVES CAUSED BY ERIOPHYOID MITEACULUS ANTHOBIUS ( NAL.)D. RANČIĆ AND R. PETANOVIĆFaculty of Agriculture, Belgrade University, Nemanjina 6, SCG-11080 ZemunAnatomical alterations of leaves of weed plant Galium mollugo L. (Rubiaceae) caused byeriophyoid mite Aculus anthobius (Nal.) are described and quantified. Symptoms can be con-sidered as leaf rolling (galls). Anatomical  alterations are expressed as destructions of epider-mal cells of upper and under surface of leaves and they can be classified as toxemias.KEY WORDS: Galium mollugo, Aculus anthobius, anatomical alterations, eriophyoid mites.INTRODUCTIONSpecies of the genus Galium are on the list for biological control, especiallyG. aparine L. that is included in European crop weeds control programs. G.aparine is increasing agricultural problem in western USA (WHITSTON, 1991),while G. spurium has become a major weed of field crops in Alberta and otherprairie provinces of Canada (MALIK & VANDEN BORN,1988). Both of plant speciesas well as G. mollugo are indigenous to Europe, but introduced to North America.According to ROSENTHAL (1996) eriophyoid mites are ideal biological controlagents against plant pests and they have been seriously considered for the biolog-ical control of weeds since the 1970’s.Eleven species of eriophyoids have been recorded from Galium spp. (AMRINE& STASNY, 1994). Five species have been recorded until now in Serbia &Montenegro (Table I).Acta entomologica serbica, 2002, 7 (1/2): 119-128 UDC 595.42 (497.11)Aculus anthobuius (  Nal.) has been reported only from type locality Loraine,France (NALEPA ,1892) and Finland (LINDROTH, 1904). It was described form G.verum (Rubiaceae) causing greening of blossoms. G. sylvaticum, G. uliginosumand G. boreale have been mentioned as alternate hosts (AMRINE & STASNY, 1994).According to FARKAS (1965) A. anthobius is distributed through out the Europe.Besides greening of blossoms symptoms have also been described as bulging ofleaves and flower deformation (DAVIS et al. 1982).Acta ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites120 Eriophyoid species Plant species Relation to the host Reference  Aceria galiobia (Can.) Galium mollugo L  G. verum  L. flower galls JANEŽIĆ,1982 PETANOVIĆ & STANKOVIĆ,1999 BOCZEK & PETANOVIĆ,1996 PETANOVIĆ & STANKOVIĆ, 1999 Aculus anthobius  (Nal.) G. verum L. G. vernum  Scop  G. rubioides  L.  G . mollugo   L.          flower deformation  and leaf rolling PETANOVIĆ & STANKOVIĆ,1999 PETANOVIĆ, 1998 PETANOVIĆ, 1998 PETANOVIĆ, unpublished ( loc. Krnule-Vladimirci,Beograd) Cecidophyes galii  (Karp.) G. mollugo L.  G. aparine L.      G. verum  L.    G. kitabelianum Roem et Schult leaf curling JANEŽIĆ,1977,1982 JANEŽIĆ,1977,1982 BOŽA,1983 PETANOVIĆ & STANKOVIĆ, 1999 BOŽA,1983 JANEŽIĆ,1977,1982 BOŽA,1983 PETANOVIĆ, unpublished loc.:  Mt.Bukulja Epitrimeru umbonis Boczek G. rubioides L. leaf and shoot rust PETANOVIĆ, 1998 Tegoprionus dentatus (Nal.) G. verum  L.          vagrant PETANOVIĆ, 1999  Table I. Eriophyoids registered on Galium spp. in Serbia & Montenegro(PETANOVIĆ & STANKOVIĆ,1999, PETANOVIĆ, unpublished)Recently, (CRAEMER et al.,1999 ) described new species, Cecidophyesrouhollahi Craemer from G. aparine in France. It was possible to keep a colonyof the mite on G. spurium in the greenhouse throughout the year. C. rouhollahi ismorphologically and  biologically close to C. galii. Symptoms, i.e. rolling ofleaves are similar too. A. anthobius superficially causes the same type of alter-ations to the host plant.Morpho-anatomical alterations of weed host plants have been investigated tillnow only on two species, Euphorbia segierana (Neck) (MIHAJLOVIĆ, 1996) andCirsium arvense (L.) Scop. (RANČIĆ, 2003).Bearing in mind that description of morphoanatomical alterations of plants iscrucial for understanding host plant phytophagous agent relationship which isimportant for the potential use in biological weed control, the aim of the study wasto describe and quantify such alterations of G. mollugo leaves induced by Aculusanthobius infestation.MATERIALS AND METHODSAnatomy of leaves was described from permanent microscopic preparations.Slides  were prepared using standard method for light microscopy (JENSEN,1962,BLAŽENČIĆ,1988). Cross sections of plant material (5-7 μm thick) have beenstained afterwards with saphranine and alcian blue. Preparations have beenobserved under LEICA DMLS microscop. Photographs have been taken usingLEICA DC 300 digital camera. In order to define main differences on the anatom-ical level following characters have been measured: thickness of leaf, high of epi-dermal cells of upper surface of leaf, thickness of mesophyll and high of epider-mal cells of undersurface of leaf. Measurements have been taken using softwarepackage IM 1000, comparatively for four zones of each leaf: the leaf base, centralpart close to the main vein and the zone of the main vein. 45 measurements havebeen done on 15 uninfested and 15 infested leaves. Statistical analysis has beendone using programs package SPSS 8.0. For each of mentioned characters mainparameters of descriptive statistics have been calculated: mean, minimum, maxi-mum and standard deviation. Significant differences between infested and unin-fested plants were strengthened carrying out unifactorial analysis of variance(ANOVA).RESULTS AND DISCUSSIONUninfested leaves of G. mollugo are symmetrical dorsoventraly with theprominent main vein on cross sections. (Figs.1 and 2). Parameters of descriptivestatistics of the main investigated characteristics are presented in Table II. Meso-Acta ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites 121phyll is 50-80μm high and clearly differentiated into palisade and spongy tissues.Epidermal layer of upper and under  surface of leaves are  about 15-16μm, and 10-12μm , respectively, except  close to the main vein were epidermal cells are about20μm high.Edges of infested leaves express rolling galls (Figs. 3 and 4). Parameters ofdescriptive statistics for the main characters of infested leaves are presented onTable III. Infested leaves are significantly thinner in comparison with uninfestedexcept in the zone of the main vein.Mesophyll is about  30-60μm high. Epidermallayer of undersurface  on the edges of leaves and in the middle is significantly thin-ner (average high about 6-8μm and the minimum of 2-3μm). Epidermal layer ofthe undersurface of leaves is thinner only on edges . In the zone of the main veinepidermal cells are significantly larger in comparison with uninfested leaves (aver-age high of infested epidermis account to 20μm and of uninfested 16μm). In thezones with destructed epidermal cells (on edges and fragmentarily in the middleof leaf) structure of mesophyll has been disarranged, especially if both epidermallayers are destructed. The mentioned disarrangement express itself in smaller mes-ophyll cells, larger intercellular spaces, loosing differentiation to spongy and pal-isade tissue and in drying of leaves.Acta ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites122 Minimum Maximum Mean Std. Deviation Epidermal layer of upper surface of leaf-leaf base 9.80 23.00 15.45 2.87 Mesophyll-leaf base 33.90 76.50 52.20 10.47 Epidermal layer of under surface of leaf- leaf base 5.30 17.50 10.54 2.67 Epidermal layer of upper surface of leaf-central part 9.90 22.40 16.21 3.59 Mesophyll- central part 42.90 99.50 73.37 11.22 Epidermal layer of under surface of leaf- central part 5.40 18.80 10.94 2.91 Epidermal layer of upper surface of leaf- close to vein 9.60 25.40 16.97 3.47 Mesophyll- close to vein 51.00 108.70 80.73 13.47 Epidermal layer of under surface of leaf- close to vein 5.60 23.80 12.16 4.57 Epidermal layer of upper surface of leaf- main vein 9.00 34.00 16.74 4.96 Mesophyll-main vain 99.90 197.40 152.21 25.64 Epidermal layer of under surface of leaf- main vain 8.60 35.30 19.91 6.60  Table II. Uninfested  Galium molugo leaves-descriptive statisticsStatistically significant differences (p < 0.5) between uninfested and ifested leaves arepresented in last column with mark +; nssd-no statistically significant differences betweenuninfested and infested leavesDifferences between measured values of investigated characters of uninfest-ed and infested leaves of G. mollugo leaves are summarized on Fig. 5.The mite Aculus anthobius is causative agent of leaf rolling of the host plantGalium mollugo. The symptom, can be  superficially considered as leaf gall.Alterations on anatomical level are expressed as destructions of epidermal cells ofupper and under surface of leaf as the consequence of mite feeding. According toclassification of symptoms given by WESTPHAL & MANSON (1996) these symp-toms can be considered as toxemias. Leaf rolling supply refuge for reproductionand feeding of eriophyoids and very often mites establish prominent colonieswithin. Dense population of mites provokes a large number of dead cells. In placeof them thick layer of calose  and lignin substances are accumulated. These symp-toms are also expresed as russetig (ROYALTY & PERRING,1996).In order to separate the  mite impact on the host , description  and quantifi-cation of similar  leaf rollings caused by othes species of eriophyoids  is needed.Acta ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites 123 Minimum Maximum Mean Std. Deviation Stat. Sign.  Diff. Epidermis of upper surface –leaf base 2.30 18.40 8.48 4.70 + Mesophyll- leaf base 12.40 52.70 33.68 11.52 + Epidermis of under surface - leaf base 2.20 12.60 6.48 3.28 + Epidermis of uppersurface-central part 2.30 59.00 16.34 8.34 nssd Mesophyll-centarl part 41.10 89.70 60.66 9.66 + Epidermis undersurface-central part 2.10 24.20 7.98 5.74 + Epidermis of upper surface-close to vein-close to vain 7.50 26.30 15.38 4.34 nssd Mesophyll-close to vain 43.90 98.50 65.49 15.36 + Epidermis of undersurface-close to vain 1.90 28.30 12.03 6.15 nssd Epidermis of upper surface-main vain 10.40 35.40 21.86 5.37 + Mesophyll-main vain 90.50 223.80 148.79 34.73 + Epidermis of under surface- main vain 15.40 51.60 29.37 8.85 +  Table III. Infested Galium molugo leaves- descriptive statisticsActa ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites124Eup Eun St Pt Fig 2. Cross section of uninfested leaf of Galium mollugo(x 200); Eup-upper epidermis;Eun-under epidermis; Pt-palisade tissue; St-spongie tissue; Eup Eun Mes Mv Fig 1. Cross section of uninfested leaf of Galium mollugo(x 50). Eup-upper epidermis;Eun-under epidermis; Mes-mesophyll; Mv-main veinActa ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites 125Eup Eun Mv Ms Fig 3. Cross section of infested leaf of Galium mollugo (x 50); Eup-upper epidermis; Eun-under epidermis; Ms-mesophyll; Mv-main veinMs Eup Eun Vb Fig 4. Cross section of infested leaf of Galium mollugo(x 200); Eup-upper epidermis; Eun-under epidermis; Ms-mesophyll; Vb-vascular bundle.REFERENCESAMRINE, J.W.JR. AND T.A. STASNY. 1994. Catalog of the Eriophyoidea(Acarina:Prostigmata) of the world. Indira Publishing House, West Bloomfield,Michigan,USA, 804 pp.BLAžENČIĆ, J. 1988: A Mannual of Plant Anatomy with Elements of Microscopy. Naučnaknjiga, Beograd. BOCZEK, J., R.PETANOVIĆ.1996. Eriophyid mites as agents for the biological control ofweeds . In: V.C. Moran and J.H. Hoffmann (Eds.). Proceedings of the IX Interna-tional Symposium on Biological Control of Weeds, January 19-26,1996.Stellenbosh,South Africa.127-131. University of Cape Town, Cape Town, South Africa.BOžA, P.1983. A Contribution to the Knowledge of Cecidofauna of herbaceous Plants ofVojvodina. Matica srpska, Zbornik  za prirodne  nauke,65:131-140. CRAEMER ,C. ,R. SOBHIAN, A.S.MC CLAY AND J.W. AMRINE, JR.1999. A New Species ofCecidophyes (Acari:Eriophyoidea) from Gallium aparine (Rubiaceae) with Notes onits Potential as a Biological Control Agent for Gallium spurium. Internat.J. Acarol.25,4: 255-263.Acta ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites126Galium molugo020406080100120140160leaf base centralpartclose toveinmain veinEUPP UNINEUPP IN MESUNINMESINEUND UNINEUND IN Fig 5. Comparative data of quantitative parameters of infested and uninfested  leaves;EUPP UNIN-upper surface epidermis of uninfested leaves; EUPP IN-upper surface epi-dermis of infested leaves; MESUNIN-mosophyll of uninfested leaves; MESIN-mesophyllof infested leaves; EUND UNIN-undersurface epidermis of uninfested leaves; EUND IN-undersurface epidermis of infested leaves.DAVIS, R., C.H.W. FLECHTMANN, J.H. BOCZEK AND E. BARKE.1982. Catalogue of EriophyidMites (Acari:Eriophyoidea).Warsaw Agricultural University Press,. pp. 254.FARKAS, H. 1965.Spinnentiere, Eriophyidae (Gallmilben). Die Tierwelt Mitteleuropas.3:1-155.JANEŽIĆ, F.1977. Some Zoocecidia on Plants of Eastern Part of Yugoslavia. Zbornikbiotehničke fakultete Univerze v Ljubljani. 30:115-130. JANEŽIĆ, F. 1982. Some Zoocecidia on Plants of Serbia. Zbornik Biotehničke fakulteteUniverze v Ljubljani.39:147-171. JENSEN, W. A. 1962: Botanical Histochemistry: Principles and Practice.W. H. Freeman andCo., San Francsco and London, 408pLINDROTH, J.I. 1904. Neueundund selten finnische Eriophyiden. Acta Soc. Fauna FloraFenn.26:118.MALIK, N. AND W.H. VANDEN BORN. 1988. The biology of Canadian weeds.86. Galiumaparine L. and Galium spurium L. Can. J. Plant Sci. 68:481-499.MIHAJLOVIĆ, N. 1996: Morpho-anatomical alterations of plant species Euphorbia seguier-ana spp. seguierana (Neck.) caused by eriophyid mite Vasates euphorbiae Pet.University Diploma Work. Faculty of biology, University of Belgrade pp54. NALEPA, A. 1892. Les acarocecidies de Lorraine ( Suite) Feuille, Ser.3, 22(258) :122,No.55. PETANOVIĆ, R. AND S. STANKOVIĆ. 1999. Catalog of the Eriophyoidea (Acari:Prostigmata)of Serbia and Montenegro. Acta  ent. serb.Special issue. pp.1-143.PETANOVIĆ, R. 1998. New Data to the Knowledge on the Eriophyoid Fauna(Acari:Eriophyoidea) in Yugoslavia. Acta ent. serb.3(1/2):149-157.RANČIĆ, D. 2003. Morpho-anatomical alterations of vegetative and reproductive organs ofplant species Cirsium arvense (L.) Scop. caused by eriophyid mite Aceria antho-coptes (Nal.). M. Sc. thesis. Faculty of biology, University of Belgrade (in serbian).ROSENTHAL, S. S. 1996. Biological Control of Weeds. Aceria, Epitrimerus and AculusSpecies and Biological Control of Weeds. In: Eriophyoid Mites-Their Biology,Natural Enemies and Control  .E.E. Lindquist, M.W. Sabelis and J .Bruin (Eds.)Elsevier Scinece. B.V. pp. 729-739.WESTPHAL, E. , MANSON, D.C. 1996. feeding Effects on Host plants: Gall Formation andOther Distortions. In:Eriophyoid Mites-Their Biology, Natural Enemies and Control.E.E. Lindquist, M.W. Sabelis and J .Bruin (Eds.) Elsevier Scinece. B.V. pp.  231-241.WHITSTON, T.D. 1991. Weeds of the West. Western Society of Weed Science.Laramie,WY.630pp.Acta ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites 127АНАТОМСКЕ ПРОМЕНЕ ЛИСТОВА GALIUM MOLLUGO L.ПРОУЗРОКОВАНЕ ЕРИОФИДОМ ACULUS ANTHOBIUS (NAL.)Д. РАНчИћ И Р. ПЕТАНОВИћИ з в о дУ раду су описане и квантификоване промене на листовима коровскеврсте Galium mollugo L. (Rubiaceae) проузроковане исхраном ериофидне гри-ње Aculus anthobius (Nal.) (Acari:Eriophyoidea). Симптоми који се манифес-тују увијањем ивица листова се могу уврстити у промене типа гала. На ана-томском нивоу промене се манифестују у  виду деструкције епидермалнихћелија лица и наличја листа које се могу према садашњој класификацији(Westphal & Manson,1996) сматрати токсемијама.Указано је на потребу да се опишу и друге сличне промене изазване дру-гим врстама ериофида на истој и /или сродним врстама рода Galium ради јас-ног разграничења утицаја на биљку домаћина.Received June 11, 2004Accepted July 29, 2004Acta ent. serb., 2002, 7 (1/2): 119-128D. RANČIĆ & R. PETANOVIĆ: Galium mollugo and Aculus anthobius eriophyoid mites128

Anatomske promene listova Galium mollugo L. prouzrokovane eriofidom Aculus anthobius (nal.)

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Anatomske promene listova Galium mollugo L. prouzrokovane eriofidom Aculus anthobius (nal.)

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