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University of Thessaloniki, Faculty of Agriculture, Laboratory of Applied Zoology and Parasitology, Thessaloniki, Greece Field observations on the biology and behavior of the black fig fly Silba adipata McAlpine (Diptera, Lonchaeidae), and trapping experiments By B. I. KATSOYANNOS Abstract Large populations of the black fig fly, Silba adipata McAl ine, previously misidentified as Lonchaea (Carpolonchaea) aristella Becker, were observed on [g trees in Chios, Greece. O n fig trees flies fed mostly during the morning and late afternoon hours, predominantly on sweet exudates from ripe figs and on fresh or dry milky fig-tree sap exuded from injuried plant parts. The odor of this sap attracted the flies. Oviposition always took place in the eye of unripe figs, mostly during the afternoon hours until dark. As many as 63 S. udiputu pupae were obtained from a single unripe fig. A parasite, Pachycwpoidegs vindemmiue Rondani (Hym., Pteromalidae), emerged from S. adipata pupae. McPhail traps baited with 2 % ammonium sulfate or 0.5 to 1 ml fresh fig- tree sap were attractive for the flies. Sticky, yellow traps were not effective. 1 Introduction According to earlier workers, the black fig fly, Silba adipata McAlpine (often misidentified as Lonchaea [Carpolonchaea, Silba] aristella Becker), (Dipt., Lonchaeidae), is a serious pest of figs in the Mediterranean basin and Middle East countries as far as Iraq (SILVESTRI 1917; ANAGNOSTOPOULOS 1939; TALHOUK 1969). It is a multivoltine (4-6 generations per year), apparently monophagous species; the female oviposit exclusively in cultivated and wild figs which serve as the larval food. In September 1981, I detected large populations of lonchaeid flies resting, feeding or ovipositing on figs, in the island of Chios, Greece. Samples of these flies, captured in traps or bred from infested figs, were identified by Dr. J. E. MCALPINE, Biosystematics Research Institute, Ottawa, Canada, as Silba adipata McAlpine. Flies of the same species were also obtained from pupae originating from infested wild figs collected in October 1981 in Thessaloniki (Northern Greece). According to McAlpine, S. adipata is the same species as Lonchaea (Car- polonchaea, Silba) aristella, studied by SILVESTRI (1917), i.e. SILVESTRI mis- identified his specimens. Silba aristella is a junior synonym of s. virescens Maquart which has been reared on several occasions from shoots, stalks and ears of corn, the sole known host (MCALPINE, pers. commun.). Thus, previous reports (CZERNY 1934; SCHEWKET 1934; %GUY 1934; ANAGNOSTOPOULOS 1939; TALHOUK 1969), based on SILVESTRI’S study and referring to the black US. Copyright Clearance Center Code Statement: 0044-2240/83/9505-0471 $ 02.50/0 Z. ang. Ent. 95 (1983), 471-476 0 1983 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-2240 / Intercode: ZANEAE

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  • University of Thessaloniki, Faculty of Agriculture, Laboratory of Applied Zoology and Parasitology, Thessaloniki, Greece

    Field observations on the biology and behavior of the black fig fly Silba adipata McAlpine (Diptera, Lonchaeidae),

    and trapping experiments

    By B. I. KATSOYANNOS

    Abstract Large populations of the black fig fly, Silba adipata McAl ine, previously misidentified as Lonchaea (Carpolonchaea) aristella Becker, were observed on [g trees in Chios, Greece. O n fig trees flies fed mostly during the morning and late afternoon hours, predominantly on sweet exudates from ripe figs and on fresh or dry milky fig-tree sap exuded from injuried plant parts. The odor of this sap attracted the flies. Oviposition always took place in the eye of unripe figs, mostly during the afternoon hours until dark. As many as 63 S. udiputu pupae were obtained from a single unripe fig. A parasite, Pachycwpoidegs vindemmiue Rondani (Hym., Pteromalidae), emerged from S. adipata pupae. McPhail traps baited with 2 % ammonium sulfate or 0.5 to 1 ml fresh fig- tree sap were attractive for the flies. Sticky, yellow traps were not effective.

    1 Introduction

    According to earlier workers, the black fig fly, Silba adipata McAlpine (often misidentified as Lonchaea [Carpolonchaea, Silba] aristella Becker), (Dipt., Lonchaeidae), is a serious pest of figs in the Mediterranean basin and Middle East countries as far as Iraq (SILVESTRI 1917; ANAGNOSTOPOULOS 1939; TALHOUK 1969). It is a multivoltine (4-6 generations per year), apparently monophagous species; the female oviposit exclusively in cultivated and wild figs which serve as the larval food.

    In September 1981, I detected large populations of lonchaeid flies resting, feeding or ovipositing on figs, in the island of Chios, Greece. Samples of these flies, captured in traps or bred from infested figs, were identified by Dr. J. E. MCALPINE, Biosystematics Research Institute, Ottawa, Canada, as Silba adipata McAlpine. Flies of the same species were also obtained from pupae originating from infested wild figs collected in October 1981 in Thessaloniki (Northern Greece).

    According to McAlpine, S. adipata is the same species as Lonchaea (Car- polonchaea, Silba) aristella, studied by SILVESTRI (1917), i.e. SILVESTRI mis- identified his specimens. Silba aristella is a junior synonym of s. virescens Maquart which has been reared on several occasions from shoots, stalks and ears of corn, the sole known host (MCALPINE, pers. commun.). Thus, previous reports (CZERNY 1934; SCHEWKET 1934; %GUY 1934; ANAGNOSTOPOULOS 1939; TALHOUK 1969), based on SILVESTRIS study and referring to the black

    US. Copyright Clearance Center Code Statement: 0044-2240/83/9505-0471 $ 02.50/0 Z. ang. Ent. 95 (1983), 471-476 0 1983 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-2240 / Intercode: ZANEAE

  • 472 B. I . Katsoyannos

    fig fly as Lonchaea or Carpolonchaea aristella, were in fact dealing with S. adipata.

    Here, I report observations concerning the biology and behavior of this fly and its responses to some odor and color traps.

    2 Materials and methods

    The observations were made during September 1981 and also in August and September 1982, in Chios, Greece, on a farm producing mainly citrus fruits and vegetables. In and around the cultivated area and in the proximity of the farm-buildings, there were also other species of trees including several fig trees.

    Direct observations on the behavior of S. adimta were made on 3 large fig trees of different local varieties. The trees were ca. 10 m high and '10-15 m in canopy diamgter,\ith branches and foliage extending to the ground. They bore fruits in all stages of maturity, most being immature. The observations were made at intervals from early morning until dark. They consisted of watching flies located on various plant parts for as long as remained in view, from some seconds to 30 minutes and recording their location and activities. The presence of the observer, as long as he remained at a distance of half a meter or more from the flies, apparently did not influence their normal behavior.

    Figs in various stages of maturity were picked on several occasions and taken to the laboratory to determine the degree of infestation. Flies that emerged from field-collected pupae were kept in groups of ca. 20-50 individuals of both sexes in 30 x 30 x 30 cm cages under 25 "C and 60-70 '70 RH, with daylight entering from the room windows, and were provided with water, fdod (yeast hydrolysate, water and sugar in proportion 1 :4 :5) and unripe figs for oviposition.

    Tra ping experiments were conducted on 6 fig trees variously spaced from 10 to 200 m, using

    sulfate or a small quantity, (10 drops or 0.5 to 1 ml), of fresh milky fig-tree sap dissolved in water or poured over a piece of cotton suspended into the trap containing water. Tree sap is easily collected by cutting leaves or unripe figs and letting the few drops formed at each cut fall into a bottle or directly into the trap. McPhail traps containing only water served as a check. Usually 4-8 traps, 1-2 of each treatment, were suspended per tree for 2-5 days. The position of the traps was daily rotated.

    Rebell cit yellow sticky traps and McPhail traps baited with 2 % aqueous solution of ammonium

    3 Results and discussion 3.1 Feeding behavior

    Observations on more than 200 flies revealed that S. adipata adults fed predominantly during the early morning, as soon as the temperature increased above 18 "C and also from late afternoon until dark. In most cases, the flies fed on sweet fig juice exuding from overripe figs which remained hanging on the trees. Although two or more flies were frequently observed feeding at the same point, one almost touching the other, there was no indication of aggressive behavior between those flies. Flies were also frequently observed feeding on drops of fresh or dry milky fig-tree sap exuded when unripe fruits or leaves were removed from the tree or where unripe figs or leaves had been injured by insects, friction or other causes. Fresh milky fig-tree sap was strongly attractive to the flies. On one occasion, I observed an aggregation of 7 flies feeding upon a drop coming from a fresh scar of a leaf I had removed a few minutes earlier. After this accidental observation, I repeated the process several times by removing leaves or unripe figs. Almost always, within a few minutes, several flies approached by a zig-zag flight pattern, landed near the wound from which sap was being exuded and began to feed on it. That this attraction is due to a humidity gradient from the fresh sap rather than to fig-tree sap odor is unlikely because many water sources were available in the vicinity. Further- more, flies were frequently observed feeding on wounds made the previous

  • Field observations on biology and behavior of S. adipata 473

    day, where the sap had already dried up. It is noteworthy that the response of the flies to the fig-tree sap was so marked and frequent that causing sap to exude, could be a useful and rapid method for detecting S. udiputu flies on fig trees.

    Exudates from ripe figs are probably the main adult food when ripe figs are available. However, before fig maturity, other food sources including milky fig-tree sap serve as food for the flies. Before mature figs were available in the area, in August 1982 I often observed flies feeding upon or inside the flowers of an ornamental creeping plant, the trumpet-creeper, Cumpsis (Tecornu) rudicuns Juss (Bingoniacae), located ca. 50 m away from the fig trees. During the same period S. udiputu flies were also observed on citrus and olive trees of the area. These observations indicate that S. udiputu flies exhibit foraging behavior.

    TALHOUK (1969), referring to previous literature concerning L. uristellu which he believed was the black fig fly, reported that the adults feed on exudates of the fig wax scale, Ceroplustes rusci L., and other insects, as well as on juice from ripe figs later in the season.

    3.2 Mating behavior

    No mating activity by S. udiputu was observed in the field or in the laboratory where flies from field-collected pupae were kept in cages. More than 2000 eggs deposited by females of these flies in unripe figs offered to them as oviposition sites failed to hatch; this suggests that these females were unmated. The presence of unripe figs, shoots or fig leaves placed in the cages holding the flies failed to elicit mating behavior.

    Information concerning the mating behavior of lonchaeids is not available in the literature, except for a few cases of pairs observed in copulation. The well-documented swarming behavior exhibited by many lonchaeid species (MCALPINE and MUNROE 1968) including S. udiputa (KATSOYANNOS, unpubl.), may be of some importance for the mating of this species.

    3.3 Oviposition behavior and fruit infestation

    Although females were observed ovipositing throughout the day except early morning, oviposition most occurred during the afternoon and until dark. In all cases observed, the eggs were laid in the eye of unripe figs, preferably those in shade at the time.

    Following a zig-zag flight, each female landed upon the fig and in a short time, in most cases within some seconds, it located the fig eye and began to insert its ovipositor between the scales surrounding the eye. After some ovipositor-pushing movements presumably followed by oviposition, the female changed position by walking over the eye and took up new position for further egg laying in the same fruit. The direction of the new position was usually at an angle between 90 to 180" in relation to the previous one. This behavior of changing position followed by further egg laying in the same fruit was repeated by each female several times; the maximum counted was 16 times. Examination of figs after oviposition revealed that the eggs were deposited next to one another beneath the eye-scales, in small groups. More than 50 eggs per fig were counted, including hatched ones, although not necessarily all by S. adiputa, in view of the fact that in the eye of some still

  • 474 B. I . Katsoyannos

    Table 1, Numbers of Silba adzpara, and Cevutitis cupituta pupae obtained from figs of different maturity

    Date of Number Degree of maturity Number of pupae obtained collection of fruits Srlba adzpara Ceratirrr caprtara

    10. 9. 81 7 15. 9. 81 10 ripe 18. 9. 81 1 swollen2 9 2

    unripe 63 0 0 > 100

    19. 9. 81 1 25. 9. 81 30 ripe

    29. 8. 82 15 ripe, fallen 0 62

    5 unripe and 2 swollen 146 19 0 148

    29. 8. 82 20 ripe, fallen 0 > 100 29. 8. 82 1 begin ripening 24 0 30. 8. 82 18 ripe, fallen 1 > 100

    9. 9. 82 50 ripe, fallen 0 > 100 30. 9. 82 30 unripe > 50 0

    4. 9. 82 15 ripe, fallen 0 > 50

    Except for the 3 cases of individual1 kept figs, all other fruits were randomly taken without previous checking for infestation. - Fig already semidecayed, with exit holes. - Fig with many eggs visible in the eye.

    immature swollen figs females of the Mediterranean fruit fly Cerutitis cupitutu (Wiedemann), were also observed ovipositing. Thus, the eggs found could have been from more than one S. udiputu female, and, in figs beginning to mature (swollen), from either S. udiputu and C. cupitutu.

    Only S. udiputu pupae were obtained from unripe figs incubated in the laboratory and in the most cases only C. cupitutu from ripe figs (table 1). As many as 63 S. udiputu pupae were obtained from a single unripe fig. In one case, 70 pupae collected in Chios on 27. IX. 1981 yielded 45 S. udiputu flies and 8 individuals of a parasite, identified as Puchycsepoideus vindemmiue Rondani (Hym., Pteromalidae). SILVESTRI (1917) has also obtained specimens of this parasite from black fig fly pupae. He also reported that during the spring generation of the black fig fly, 1 4 eggs per fig was usual but in autumn as many as 50-100 eggs per fig were recorded. He concluded that the later eggs probably originated from different females and explained the differences in numbers to be the result of differences in fecundity between the flies of the spring and autumn generations.

    Whether S. udiputu females can distinguish and select uninfested rather than infested fruits for oviposition as do many tephritid flies PROKOPY 1972a, KATSOYANNOS 1975, PROKOPY et al. 1978 and others), which belong to the same superfamily of Tephritoidea, is unknown. During this study no behavior was observed indicating fruit exploration before the initiation of oviposition, or fruit marking after egg laying.

    3.4 Attraction to odor and color traps

    The results of the trapping experiments conducted during 1981 and 1982 are given in table 2. In addition to S. adiputu numerous other insects, mostly Diptera including C. cupitutu, were captured by the ammonium sulfate baited McPhail traps while those baited with fig-tree sap captured almost exclusively S . udiputu flies.

  • Field observations on biology and behavior of S. adipata 475

    Table 2. Attraction of Silba udipata flies to Rebell yellow sticky traps and McPhail traps baited with 2 % ammonium sulfate (= as.), fresh milky fig-tree sap in water, or poured in a piece of cotton suspended into the trap, or water (check). Traps comparatively suspended on fig trees. By

    expts No. 2, 4, and 5 only McPhail traps were used

    Expt. Treatments Expt. duration No. of Number of flies captured I No. (days) replicates Males Females Total 1981

    1 McPhail (a.s.) 5 18 151 662 813

    Rebell 9 - - 38 2 1 ml sap in water 3 4 29 99 128

    McPhail (water) 9 1 2 3

    Water (check) 4 0 0 0

    3 McPhail (as.) Rebell

    4 13 180 386 563 - - 20 13

    4 10 drops sap in water 2 4 25 32 57 Water (check) 4 0 0 0

    5 0.5 ml sap in water 2 6 20 82 1 02

    Water (check) 6 0 0 0 0.5 ml sap on cotton 6 7 51 58

    The results show that S. adipata flies were strongly attracted by McPhail traps baited with ammonium sulfate. Such baited traps could be effectively used for S. adipata monitoring and possible control. The results also confirm the attraction of S. adipata to the odor of fresh fig-tree sap, reported above. This finding merits further evaluation with a view to improving trap efficiency and selectivity. Sticky, yellow traps, which have proven to be attractive to many tephritid flies (PROKOPY 1972b; PROKOPY and BOLLER 1971; GIROLAMI and CAVALLORO 1973; PROKOPY and ECONOMOPOULOS 1976), seem to have little or no attractiveness.

    Acknowledgements Many thanks are due to: Dr. J. F. MCALPINE, Biosystematics Research Institute, Ottawa Canada for identifying the black fig flies, reviewing an earlier draft of the manuscript and providing useful information and literature, Dr. C . M. YOSHIMOTO of the same institute for identifying the parasites, Prof. M. E. TZANAKAKIS for reviewing the manuscript and for his suggestions, Dr. P. GUERIN for comments and Drs. P. FIMIANI and P. MOURIKIS for providing useful literature.

    Zusammenfassung Feldbeobachtungen dber Biologie und Verhalten der Scbwarzen Feigenfliege, Silba adipata

    McAlpine (Dipt., Loncbaeidae), und Anlockungsversuche mit Fallen Grol3e Populationen der Schwarzen Feigenfliege, Silba adipata McAlpine, vorher irrtiimlich als Lonchaeu (Carpolonchaea) aristellu Becker beschrieben, wurden auf Feigenbaumen in Chios, Griechenland, beobachtet. 5. adipata-Fliegen in Feigenbaumen nahmen ihre Nahrung morgens und in den spaten Nachmittagsstunden auf, vorwiegend d e n Saft aus reifen Feigen und frischen oder getrockneten milchigen Feigenbaumsaft, der aus Verletzungen der Pflanzen austrat. Der Geruch dieses Saftes zog die Fliegen an. Eier wurden immer in das Auge der unreifen Feigen abgelegt, meistens wihrend des Nachmittags bis zur Dunkelheit. Aus einer einzigen unreifen Feige wurden 63 5. adipata-Puppen erhalten. Parasiten der Art Pacbymepoideus vindemmiae Rondani

  • 4 76 B. I . Katsoyannos

    (Hym., Pteromalidae), schliipften aus S. adipata-Puppen. McPhail-Fallen, gekodert mit 2 % Ammoniumsulfat oder 0,5-1 ml frischem Feigenbaumsaft, lockten diz Fliegen an, gelbe Leimfallen dagegen waren nicht attraktiv.

    References

    ANAGNOSTOPOULOS, P., 1939: The Enemies of Fruit Trees. Athens (in Greek). CZERNY, L., 1934: Lonchaeidae. In: Linder, E., Die Fliegen der Palaearktischen Region. 5,1,-40. GIROLAMI, V.; CAVALLORO, R., 1973: Methodi cromotropici per indagini di popolazione degli

    adulti di Dacus oleae Gmelin. Note App. Sper. Entomol. Agr. 14, 13-29. KATSOYANNOS, B. I., 1975: Oviposition-deterring, male-arresting, fruit-marking pheromone in

    Rhagoletis cerasi. Environ. Entomol. 4, 801-807. MCALPINE, J. F.; MUNROE D. D., 1968: Swarming on lonchaeid flies and other insects, with

    descriptions of four new species of Lonchaeidae (Diptera). Can. Entomol. 100, 1154-1 178. PROKOPY, R. J., 1972a: Evidence for a marking pheromone deterring repeated oviposition in apple

    maggot flies. Environ. Entomol. 1, 326-332. - 1972b: Response of apple maggot flies to rectangles of different colors and shades. Environ.

    Entomol. 1, 721-726. PROKOPY, R. J.; BOLLER, E. F., 1971: Response of European cherry fruit flies to colored

    rectangles. J. Econ. Entomol. 64, 1444-1447. PROKOPY, R. J.; ECONOMOPOULOS, A. P., 1976: Color responses of Ceratitis capitata flies. 2. ang.

    Ent. SO, 434-437. PROKOPY, R. J.; ZIEGLER, J. R.; WONG, T. T. Y., 1978: Deterrence of repeated oviposition by

    fruit-marking pheromone in Ceratitis capitata (Diptera: Tephritidae). J. Chem. Ecol. 4,55-63. SCHEWKET, N., 1934: Die Feigeninsekten und die wesentlichen Ursachen der Feigenfruchtfaule.

    Anz. Schadlingskunde 10, 118-119. SBCUY, E., 1934: Diptcres (BrachycPres). Faune de France, Vol. 28, Paris. SILVESTRI, F., 191 7: Sulla Lonchaea aristelIa Beck. (Diptera: Lonchaeidae) dannosa alle infiores-

    TALHOUK, A. M., 1969: Insects and Mites Injurious to Crops in Middle Eastern Countries. cenze e fruttescenze del caprifico e del fico. Boll. Lab. 2001. Agr. Ponici 12, 123-146.

    Hamburg und Berlin: Paul Parey.

    Authors address: Dr. B. KATSOYANNOS, University of Thessaloniki, Faculty of Agriculture, Laboratory of Applied Zoology and Parasitology, Thessaloniki, Greece