ENTOMOLOGIA HELLENICA 15 (2003-2004)

Ecological data of Lepidosaphes gloverii (: ) in Greece

G.J. STATHAS

Technological Educational Institute of Kalamata, School of Agricultural Technology Department of Crop Production, Laboratory of Agricultural Entomology and Zoology 24 W0-ANTIKALAMOS, GREECE, e-mail: [email protected]

ABSTRACT

In June 2001 the scale Lepidosaphes gloverii (Packard) (Hemiptera: Diaspididae) was found on orange trees in Peloponnesus, Gastouni area, (Southwestern Greece). From the day it was first recorded until August 2003 observations on orange trees were held both in field and laboratory, concerning the biology and ecology of this scale. L gloverii infests mainly the upper surface of the leaves and the fruits and less the shoots of the tree. During the period April to August 2002 the scale completed 3 overlapping generations. Female fecundity ranged between 32 and 57 eggs. Chilo- corus bipustulaius (L.) (Coleoptera: Coccinellidae) and Rhyzobius lophanthae Blais- dell (Coleoptera: Coccinellidae) predators were found to feed upon this scale. In July 2002 a mass release of those predators took place on infested orange trees. To assess the action of these predators, observations were conducted in both field (by shaking the branches of the trees and counting the number of the predators) and laboratory (by counting the predated scales found on leaves). The release of predators contrib­ uted to the decrease of infestation density of trees. C. bipustulaius developed signifi­ cantly higher populations than R. lophanthae.

Introduction jority of Mediterranean countries (Hall 1924, Lepiney and Mimeur 1931, Gomez-Menor The most important scales of Diaspididae Ortega 1937, Longo et al. 1995). It is consid­ family (Hemiptera) that infest trees in ered to cause serious damage to citrus and Greece are Aonidiella aurantii (Maskell), ornamental plants (Talhouk 1975, Rosen Aspidiotus nerii Bouché, Chrysomphalus 1990). dictyospermi (Morgan), Lepidosaphes beckii Many species of parasitoids, predators (Newman) and Parlatorio pergandii Corn- and fungi have been reported as natural ene­ stock (Koroneos 1934, Argyriou 1979a, mies of L. gloverii. The hymenopterous para­ 1979b, Argyriou et al. 1981, Katsoyannos sitoids that attack L. gloverii belongs to the 1996). following species: Signiphora fax (Signi- Lepidosaphes gloverii (Packard) (Hemip­ phoridae) (Teran et al. 1985), Adelencyrtus tera: Diaspididae) is recorded in many areas, inglisiae () (Konar 2001), Encar- like Central and Northern America, Asia and sia herndoni () (Viggiani and Europe. It has also been recorded in the ma­ Liotta 1989) and the aphelinids Aphytis ling- 20 ENTOMOLOGIA HELLENICA 15 (2003-2004) nanensis (Woolley et al. 1994), Encarsia the upper leaf surface were recorded and elongata (Benassy and Brun 1989), Aphytis expressed as number of scales/cm". lepidosaphes, Aspidiotiphagus citrinus The monitoring of population dynamics (Bmwer and Schoeman 1990) and Aspidi­ of the predators was performed by shaking otiphagus lounsburyi (Ceballos et al. 1988). branches of trees over a lmxlm cloth, at 12 Its predators are the coccinellids Zagloba randomly collected points in the orchard. The beaumonti, Pentilia discors (Arias-Reveron species, the number and the developmental 1990) and Chilocorus nigrita (Bruwer and stage of the predators falling from the Schoeman 1990). Pathogenic fungi of L. branches on the cloth, were recorded. These gloverii are Podonectria coccicola and Verti- actions were conducted once every 15 days cillium sp. (Gao and Ouyang 1981). from April to September and once a month, The serious infestation of L. gloverii on for the rest of the year. On 22/7/2002, 1.500 citrus observed in Greece, the importance of adults of Chilocorus bipustulaius (L.) and this enemy that causes serious damage in 1.500 adults of Rhyzobius lophanthae Blais- citrus orchards, as well as the lack of infor­ dell were released, coming from mass rearing mation about its ecology in Greece, were the in insectaries, feeding on Aspidiotus nerii motives that lead to the present study. In this Bouché and Chrysomphalus aonidum (L.), study data concerning the phenology, popula­ under controlled conditions (temperature tion dynamics and the action of natural ene­ 25±2 °C, RH 65±2% and photoperiod mies of L, gloverii, are presented. 16h/day). The mean numbers of the predators (C. bipustulaius and R. lophanthae) counted Materials and Methods using the above procedure were compared using Student's t-test (Landi 1977). L. gloverii was found to infest Citrus sinensis During the study, the trees were sprayed var. navelina in Southeastern Greece, (Pelo­ 3 times with mineral oil 1,5%, at the follow­ ponnesus, area of Gastouni). The scale was ing dates: 5/9/2001, 24/5/2002 and identified by the author at the Laboratory of 25/9/2002. No other applications with plant Biological Control of Benaki Phytopa- protection products were applied in the or­ thological Institute and was confirmed by the chard during the study. Researcher Entomologist Dr Ferenc Kozâr For the study of the fecundity of the (Plant Protection Institute, Hungarian Acad­ scale, 50 ovipositing females were examined emy of Sciences). A specimen was sent to in June 2001. These individuals were settled the collection of the Natural History Museum on the upper surface of the leaves. Tempera­ of France (Museum National d' Histoire ture in the field was recorded using a ther­ Naturelle). The study was conducted from mograph. June 2001 to August 2003 in an orange or­ chard of 37 acres. The age of the trees was Results 25 years. The distance between the trees was 6m on the same row and the distance of one The scale mainly settles on the upper sur­ row to another was 7m. face of the leaves, fruits and to a lesser degree To study the phenology of L, gloverii, 20 on the branches. In Fig. 1 is shown the fre­ samples consisted of branches (25cm length) quency of instars of L gloverii on leaves and were randomly selected and transported to the mean maximum and minimum monthly the laboratory into nylon bags. The samples temperatures during the study period. Crawlers were examined under binocular stereoscope had three distinct peaks per year: in June, Au­ and the number and instars of the scales, as gust and October, respectively. The rest of the well as the predated and dead individuals on instars did not appear to have relevant peaks. STATHAS: ECOLOGICAL DATA OF LEPIDOSAPHES GLOVERII IN GREECE 2.1

During the winter period, preovipositing and sults of the present study (3 generations per ovipositing females were more abundant than year), could be attributed to the differences in individuals of the immature instars. Male climatic conditions and host plant, where the nymphs were recorded throughout the year. scale develops. The number of alive, dead and predated indi­ The increase of dead individuals per scale viduals of L gloverii on leaf surface, is shown after the sprayings and after the release of the in Fig. 2A, Alive scales decreased, while pre­ predators, and the increase in the number of dated scales increased. Higher was the increase predators collected could gather to conclude of the number of dead scales. After spraying, an that the release of predators and spraying con­ increase in the number of dead individuals was tribute to the decrease of infestation. observed, whereas after the mass release of the The population of C. bipustulaius was sig­ predators an increase in the number of predated nificantly higher than that of R. lophanthae individuals was recorded. almost throughout the period of the study. This Population dynamics of larvae and adults of is probably related to the inability of R. lophan­ C. bipustulaius and R. lophanthae is shown in thae to develop high populations on every dias- Fig. 2B. Chtlocorus bipustulaius was observed pidid scale. In other studies concerning dias- in higher populations than R. lophanthae pidid predators in Greece it has been reported {t=6.1, P<0.05). that R. lophanthae develops high populations Fertility fluctuated between 32 and 57 with even in winter (Stathas 2000a, 2001a). The an average of 37.7 ± 8.03 (mean ± SD) eggs per development of fi. lopphanthae depends on the female. species of the scale on which it feeds. It has been reported that the development of R. lo­ Discussion phanthae on scales with harder scale cover [like Aonidiella aurantii (Maskell) and Chrysompha- From the continuous presence of all stages of lus aonidum (Linnaeus)] is more difficult than the scale throughout the year, it is gathered that on scales with softer scale cover (like Aspidio- L. gloverii completes overlapping generations tus nerii Bouche) (Stathas 2000b, 2001b, during the year (Fig. 1). The three peaks of Stathas et al. 2002). Honda and Luck (1995) crawlers observed in June, August and October, attribute the incapability of rearing R. lophan- respectively, indicate that the scale must com­ the on diaspidids with hard scale cover to the plete 3 generations per year. The rest instars did morphological characteristics of its moufhparts. not appear to have relevant peaks during the Bruwer and Schoeman (1988) reared L. year as crawlers did. This may be attributed to gloverii in laboratory on several preys and tem­ the higher mortality of the crawlers compared peratures, and found that the mean optimum with the other instars as well as the applications fecundity was 44.2 crawlers/female, in sour of sprays. Smith et al. (1997) report that L. orange trees at 30°C. The difference will ι the gloverii completes 5-6 generations per year in number of 37.7 found in the present study may Queensland and 2-4 generations in New South be attributed to the differences of the develop­ Wales. The difference in the number of genera­ mental conditions and to the host plant. tions appeared in the above study and the re­ 22 ENTOMOLOGIA HELLENICA 15 (2003-2004)

1st instar

100 2nd instar

% 50

0

100 male nymphs

% 50

0

100 pteoviposiling females

% 50

0

100 depositing females

% 50

0

2001 2002 2003

FIG. 1. De\ç!opmental stages (percentage composition) of Lepidosaphes gloverii on citrus and monthly awrage temperatures from June 2001 to August 2003, in southern Greece, STATHAS: ECOLOGICAL DATA OF LEPIDOSAPHES GLOVERII IN GREECE

FIG. 2. (A): Alive, dead and predated individuals of Lepidosaphes gloverii found on orange tree leaves in southern Greece, from June 2001 to August 2003. (B): Number of predators (larvae and adults) recorded by 12 beatings of tree branches on the cloth screen. •a: Spray applications with mineral oil •b: Releasing of Chilocorus bipustulaius and Rhyzobius lophanthae. 24 ENTOMOLOGIA HELLEN1CA 15 (2003-2004)

Acknowledgements (Hymcnoptera: Aphelinidae) a parasitoid of di- aspidid scales on Citrus in Cuba. Revista-de- The author expresses his gratitude to the Re­ Proteccion-Vegetal. 1988, 3: 201-208. searcher Entomologist Dr Ferenc Kozär Gao, R.X. and Z.A. Ouyang, 1981, Preliminary (Plant Protection Institute, Hungarian Acad­ investigation on parasitic fungi on citrus pests. emy of Sciences) for the confirmation of the Weishengwuxue Tongbao, 8: 57-58. species L. gloverii. Gomez-Menor Ortega, J. 1937. Coccidos de Espapa. (In Spanish). Instituto de Investiga- References ciones Agronomicas, Estacion, Madrid. 432 pp. Hall, W.J., 1924. The pests of citrus trees in Argyriou, L.C., 1979a. The present status of inte­ Egypt. Bulletin, Ministry of Agriculture, Egypt, grated control of citrus pests in Greece. Pro­ Technical and Scientific Service 45: 1-29. ceedings of Internationa! Symposium of Honda, J.Y. and R.F. Luck, 1995. Scale morphol­ IOBC/WPRS on integrated control in agricul­ ogy effects on feeding behavior and biological ,h lh ture forestry, Vienna 8 12 , October, 517-520. control potential of Rhyzobius lophanthae (Col­ Argyriou, L.C., 1979b. Zoogeographical consid­ eoptera: Coccinellidae). Ann. Entomol.Soc. eration of scale of citrus in Greece. Am. 88: 441-450. Biologia Gallo Hellenica, 9: 307-313. Katsoyannos, P., 1996. Integrated Insect Pest Argyriou, L.C., P.A. Mourikis and K. Matsumoto, Management for Citrus in Northern Mediterra­ 1981. Current status of citrus pests in Greece. nean Countries. Benaki Phytopathological Insti­ Proceedings of the International Society of Ci- tute, 110pp. triculture, Vol.e 2, 623-627. Konar, Α., 2001. Insect parasitoids of diaspidid Arias-Reveron, J.M., 1990, Notes on natural ene­ , Mytilococcus sp. attacking orange mies attacking Lepidosaphes species (Homop- in Darjeeling district, West Bengal. Journal of tera: Diaspididae) associated with citrus in Interacademicia, 567-70. Costa Rica. Entomophaga, 35: 301-303. Koroneos, J., 1934, Les Coccidae de la Grèce: Benassy, C. and P. Brun, 1989. Encarsia elongata Surtout du pelion (Thessalie). I: Diaspinae. Dozier (Hym.: Aphelinidae) a new entomo- Athènes, 95 pp. phagous species introduced in France among Landi, R., 1977. Lezioni di Metodologia e Tecnica the citrus scale insects. Mededelingen van de Sperimentale. Cedam, Padova, 234pp. Faculteit Landbouwwetenschappen Rijksuni- Lepiney, J. and J,M. Mhneur, 1931. Les coccides versheit Gent., 54: 861-865. du Maroc. (In French). Revue de Pathologie Bruwer, I.J. and A.S. Schoeman, 1988. Mas- Vignale et d'Entomologie Agricole de France sateling van die langmosseldopluis, Insulaspis 18: 243-255. gloverii (Packard) (Hemiptera: Diaspididae). Longo, S., S. Maratta, G. Pellizzari, A. Russo and Journal of the Entomological Society of South­ A. Tranfaglia, 1995. An annotated list of the ern Africa, 51: 165-170. scale insects (Homoptera: Coccoidea) of Italy. Bruwer, I.J. and A.S. Schoeman, 1990. Key factor Israel Journal of Entomology 29: 113-130. analysis of two populations of the long mussel Rosen, D„ 1990. Armored scale insects. Their scale, insulaspis gloverii (Packard) (Hemiptera: biology, natural enemies and control. Elsevier, Diaspididae). Journal of the Entomological Amsterdam, vol. 4B, 688 pp. Society of Southern Africa, 53: 101-105. Smith, D., G.A.C .Beattie and R.H. Broadley, Ceballos, M., M. Henandez, M. Fernandez and E. 1997, In: Citrus Pests and their Natural Ene­ Garcia, 1998. Aspidiotiphagus lounsburyi mies: Integrated Pest Management in Australia. STATHAS : ECOLOGICAL DATA OF LEPIDOSA PH ES GLO VERI! IN GREECE 25

State of Queensland, Dept. of Primary Indus­ Teran, A.L., M.L. Collado de Manes, S. Glenross, tries, and Horticultural Research and Develop­ R. Alvarez and H. Lazaro, 1985. Primary and ment Corp., Brisbane, Australia. 263 pp. secondary parasitoid Hymenoptera of scale in­ Stathas, G.J., 2000a. The effect of temperature on sects, except Aonidiella aurantii (Mask.) (Ho- the development of the predator Rhyzobius lo­ moptera: Coccoidea), in citrus trees of Tu- phanthae and its phenology in Geece. BioCon- cuman (Argentina). Revista de Investigacion trol, 45:439-451. Centro de Investigaciones para la Regulacion Stathas, G J., 2000b. Rhyzobius lophanthae Prey de Poblaciones de Organismos, Nocivos Argen­ consumption and Fecundity. Phytoparasitica, 28 tina, 3: 25-33. (3): 203-211. Viggiani, G. and G. Liotta, 1989. On the intro­ Stathas, G.J., 2001a. Ecological data on predators duction in Italy of Encarsia herndoni (Girault) of Parlatoria per gondii on sour orange trees in (Hym., Aphelinidae), parasitoid of insulaspis southern Greece. Phytoparasitica, 29: 207-214. gloverii (Pack) (Homoptera, Diaspididae): pre­ Stathas, G.J., 2001b. Studies on mor­ liminary notes. Phytophaga Palermo, No. 3: 79- phology and biology of immature stages of the 81. predator Rhyzobius lophanthae Blaisdell (Col­ Wnolley, IB., M. Rose, P.C. Krauter and D. eoptera: Coccinellidae). Anzeiger fUr Schäd­ Rosen 1994. Morphometric comparisons of lingskunde (Journal of Pest Science), 74: 57-59. Aphytis species in the iingnanensis group (Hy­ Stathas. G.J., Eliopoulos P.A., Kontodimas, D.C. menoptera: Aphelinidae). Advances in the and Siamos D. Th, 2002. Adult morphology study of Aphytis (Hymenoptera: Aphelinidae), and life cycle under constant temperatures of 223-244. the predator Rhyzobius lophanthae Blaisdell (Col,, Coccinellidae). Anzeiger für Schädlings­ kunde (Journal of Pest Science), 75: 105-109. KEYWORDS: Chilocorus bipustulaius, Talhouk, A.S., 1975. Citrus pests throughout the fecundity, Greece, Lepidosaphes gloverii, world. In: E, Halliger (Editor), Citrus. CIBA - orange trees, phenology, Rhyzobius GEIGY Agrochemicals Technical Monograpg lophanthae. No 4, 21-23. 26 ENTOMOLOGIA HELLENICA 15 (2003-2004)

Οικολογικές παρατηρήσεις του Lepidosaphes gloverii (Hemitera: Diaspididae) στην Ελλάδα

Γ.Ι. ΣΤΑΘΑΣ

Τεχνολογικό Εκπαιδευτικό Ίδρυμα ΚαίΜμάτας, Σχολή Τεχνολογίας Γεωπονίας Τμήμα Φυτικής Παραγωγής, Εργαστήριο Γεωργικής Εντομολογίας και Ζωολογίας 24 100-ΑΝΤΙΚΑΛΑΜΟΣ, e-mail: [email protected]

ΠΕΡΙΑΗΨΗ

Τον Ιούνιο του έτους 2001 βρέθηκε το κοκκοειδές Lepidosaphes gloverii (Hemiptera: Dias­ pididae) σε πορτοκαλιές στην περιοχή Γαστούνη Ηλείας. Από την ημέρα της καταγραφής του και μέχρι τον Αύγουστο του 2003 έγιναν παρατηρήσεις σε πορτοκαλιές της περιοχής αυτής ανά τακτά χρονικά διαστήματα και παρατηρήσεις στο εργαστήριο, που αφορούσαν στη μελέτη της βιολογίας και οικολογίας του εντόμου. Το κοκκοειδές προσβάλλει κυρίως την άνω επιφά­ νεια των φύλλων, τους καρπούς και λιγότερο τους βλαστούς. Κατά το χρονικό διάστημα Απρι­ λίου - Οκτωβρίου 2002 συμπλήρωσε 3 επικαλυπτόμενες γενεές. Η γονιμότητα των θηλέων κυμάνθηκε μεταξύ 32 και 57 ωών. Εναντίον του κοκκοειδούς βρέθηκαν να δρουν τα αρπακτι­ κά έντομα Chilocorus bipustulaius (L.) και Rhyzobius lophanthae Blaisdell (Coleoptera: Coc­ cinellidae). Τον Ιούλιο του έτους 2002 έγινε σε προσβεβλημένο πορτοκαλεώνα μαζική εξαπό­ λυση των πιο πάνω αρπακτικών ειδών. Για την εκτίμηση της δράσης των αρπακτικών έγιναν παρατηρήσεις στον αγρό (τινάγματα της κόμης των δένδρων και καταμέτρηση των αρπακτι­ κών) και εξετάσεις στο εργαστήριο (καταμέτρηση στα φύλλα των προσβεβλημένων κοκκοει- δών από αρπακτικά). Από τις παρατηρήσεις αυτές φάνηκε αφενός πως τα αρπακτικά που εξα­ πολύθηκαν συνέβαλαν στη μείωση της προσβολής και αφετέρου πως το Ch. bipustulaius ανα­ πτύχθηκε σε σημαντικά υψηλότερους πληθυσμούς από το R. lophanthae.