Proceedings of 6th International Fruit Symposium 6–10 May 2002, Stellenbosch, South pp. 19–22

Development of capitata (Diptera: ) in three apple varieties in the laboratory

Nikos T. Papadopoulos* & Byron I. Katsoyannos Department of Agriculture, Laboratory of Applied Zoology and Parasitology, Aristotle University of Thessaloniki, 540 06 Thessaloniki, Greece

We studied in the laboratory (25 ± 2°C;65 ± 5% R.H.) the development of the Mediterranean fruit fly, (Wiedemann) (Diptera: Tephritidae), in apples of the varieties Golden Delicious, Granny Smith and Red Delicious. The duration of the larval stage was longer and larval mortality higher in Granny Smith and Red Delicious than in Golden Delicious.The pupal development period was similar in the three varieties, but mortality was higher in Granny Smith and Red Delicious than in Golden Delicious. Total immature developmental period (from larval hatch to adult emergence) was approximately 23,35 and 33 days in Golden Delicious,Granny Smith and Red Delicious,respec- tively, and the percentage of newly-hatched larvae that reached adulthood was c. 47, 25 and 23%, respectively. Studies on the biology of adults that developed as immatures in these varieties showed that the variety in which larvae developed did not influence adult longevity. However, fecundity was much higher in females collected from Golden Delicious (c. 385 eggs/female) than in those collected from Granny Smith and Red Delicious (c. 165 eggs/female in both varieties). In all three cases, females laid eggs only on fruits of the same variety in which they had developed as larvae. These results show that Golden Delicious is the most favourable variety both for larval development and adult fecundity. Fruit firmness, which was higher in apples of Granny Smith and Red Delicious compared with those of Golden Delicious,seems to be the most important factor accounting for the differences in development of C. capitata between the three varieties.

INTRODUCTION main crops in northern Greece and is a very impor- The Mediterranean fruit fly (Medfly), Ceratitis tant host for Medfly as it serves as overwintering capitata (Wiedemann), is one of the most serious refuges for the larvae (Papadopoulos et al. 1996; pests worldwide, infesting fruits of more Papadopoulos et al. 1998). Different apple variet- than 300 plant species,including several cultivated ies show important variability in Medfly field species of high commercial value (Liquido et al. infestation, as well as in their suitability for 1991). There is much data on the biology of this the overwintering of this fly in northern Greece fly under constant conditions in the laboratory, (Papadopoulos et al. 1996, 2001). At present, little mostly for laboratory-adapted populations is known about which factors determine the (Shoukry & Hafez 1979; Carey 1984; Vargas et al. suitability of the different varieties for the ovi- 1984; Krainacker et al. 1987, 1989; Vargas et al. position, development and successful over- 1996, 1997). However, only few studies have dealt wintering of C. capitata. Comparative demo- with the biology of wild Mediterranean popula- graphic studies (life and fecundity tables) of the tions (Rivnay 1950; Carey 1984), and only one Medfly on the main apple varieties cultivated study directly examined the populations from the in northern Greece could provide important infor- northern coasts of the Mediterranean basin, such mation for understanding the factors that deter- as northern Greece, which is considered to be mine the variability in infestation and successful within the northern limits of the fly’s distribution overwintering (Papadopoulos et al. 1996, 2001). (Papadopoulos et al. 2002). Life and fecundity tables for C. capitata reared in In northern Greece, C. capitata infests mostly apples in the laboratory have been developed pome and stone fruits as well as fig (Ficus carica L.) recently, but only for the Golden Delicious variety and oriental persimmon (Diospyros kaki, L.). The fly (Papadopoulos et al. 2002). reaches high populations in autumn. Autumn The objectives of this study were: first, to under- populations pose a serious threat for apples stand which chemical and physical characteristics (Malus sylvestris Mill.), which matures at that time determine the suitability of different apple varieties (Papadopoulos et al. 2001). Apple is one of the for the oviposition and development of C.capitata; second,to explain the observed differences in field *To whom correspondence should be addressed. Present infestation between the main apple varieties; and address: Department of Agriculture Crop Production and Rural Environment, University of Thessaly, Fytokou str. N. Ionia 384 46 third, to understand the mechanism(s) of larval Magnisia Greece. E-mail: [email protected] overwintering in this host. 20 Proceedings of the 6th International Fruit Fly Symposium

MATERIALS AND METHODS The experiments were conducted under laboratory conditions at 25 ± 2°C, 65 ± 5% RH.Wild C.capitata adults were reared from field-infested apples. Three apple cultivars were used, Golden Delicious, Granny Smith and Red Delicious, which are the three main varieties cultivated in the area. Apples were collected from an unsprayed orchard from the Thessaloniki area and kept in the refrigerator for about two months. Before use, apples were acclimatized for 24 hours at 25°C. Physical and chemical characteristics measured in these apples included weight, diameter, firm- ness of pulp (mesocarp) (force measurements using a penetrometer), content of solid soluble materials (using a refractrometer), acidity (mg malic acid/ 100 g) and pH. To study the duration of development of imma- ture stages on apples of the three varieties, five newly-emerged larvae from eggs collected from wild in the laboratory, were gently introduced with a fine brush into each of four holes (20 larvae in total per apple) made with an entomological pin on the surface of the fruit. For each apple variety we used 15 apples, resulting in a total of 300 newly-hatched larvae for the whole experiment. Following larval inoculation, each apple was Fig. 1. Distribution patterns of adult emergence of placed into a plastic cup on a layer of dry sand Ceratitis capitata as affected by apple variety in which and covered with muslin. The number of pupae larvae developed. Time ‘0’ on the x-axis is the time obtained from individual apples was recorded at which newly-hatched larvae were inoculated into the host apples. Results based on 15 apples of each daily. Pupae which formed were kept individually variety, each containing 20 hatched larvae. and the duration of their development and sur- vival was determined. differences in fruit size (both diameter and weight), Newly-emerged adults derived from the experi- in the content of solid soluble materials, and in pH ment were immediately transferred to perspex between the three varieties (Tukey’s HSD test, P > cages, with adult food and water, in groups of 10 0.05). Acidity, however, was substantially higher in males and 10 females. Flies in these cages were Granny Smith than in both Golden Delicious and then exposed every day to apples of the same Red Delicious. variety on which they developed, for oviposi- tion. We ran five replicates for each variety. Adult Development and survival of immatures mortality and oviposition patterns were recorded Duration of larval development was shorter and daily. survival was higher in Golden Delicious apples Data were subjected to analysis of variance than in the other two varieties. There were no (ANOVA) and means were separated using Tukey’s differences in the duration of pupal development HSD test (P < 0.05). When only two means were between the three varieties. Survival of both lar- compared, the t-test was used, while percentages vae and pupae was higher in flies obtained from werecomparedwiththechi-squaretest(P<0.05). Golden Delicious apples than in those derived from the other two varieties. Average duration of RESULTS development from larval hatch to adult emer- gence was about 23 days in Golden Delicious and Apple characteristics 35 and 33 days in Granny Smith and Red Delicious, Pulp firmness was significantly higher in Granny respectively (Fig. 1). The percentage of larvae that Smith than in Golden Delicious and Red Delicious reached adulthood was significantly higher apples (Tukey’s HSD test, P < 0.05). There were no (chi-square test,P < 0.05) in Golden Delicious (47%) Papadopoulos & Katsoyannos: Development of Ceratitis capitata in three apple varieties 21

Table 1. Average longevity in the laboratory of adult Medflies reared as larvae on Golden Delicious, Granny Smith and Red Delicious apples. Averages were calculated from five replicates of 10 males and 10 females for each variety.

Apple variety Average longevity (days ± S.E.) Males Females

Golden Delicious 37.5 ± 2.1 a 33.1 ± 5.3 a Granny Smith 33.2 ± 7.4 a 30.6 ± 3.8 a Red Delicious 30.1 ± 3.4 a 29.3 ± 5.0 a

Means in columns followed by the same letter are not significantly different (Tukey’s HSD, P < 0.05). than in Granny Smith and Red Delicious (25 and 23%, respectively) (Fig. 2).

Adult biology Adult longevity was similar in individuals ob- tained from all three varieties (Table 1,Tukey’s HSD test, P > 0.05). Average longevity for both sexes ranged between 29 and 36 days, and there were no differences between male and female longev- ity (t-test, P > 0.05). Age-specific oviposition patterns were similar in the three varieties. However, fecundity was higher in females collected from, and ovipositing in, Fig. 2. Percentage of adults yielded by rearing larvae Golden Delicious than in the other two varieties in Golden Delicious, Granny Smith, and Red Delicious (Tukey’s HSD test, P < 0.05). On average, fecundity apples. Results based on 15 apples of each variety, each containing 20 newly-hatched larvae. Columns was about 385 eggs per female in Golden Delicious with the same letters are not significantly different (P = and only 165 eggs per female in Granny Smith and 0.05). Red Delicious. several population increase parameters were low DISCUSSION and these results agree with our previous findings, In general, there is a high plasticity in biological supporting the suggestion that apples are not a characteristics of Medfly reared in different host favourable host for the development C. capitata. fruit species (Carey 1984; Krainacker et al. 1987). Survival rates of adults were only moderately Our results suggest that even within fruit species, affected by the variety of apples in which they were different fruit varieties may considerably affect reared. However, female fecundity is greatly various aspects of the biology of both immature affected by the variety on which they oviposit,and and adult Medflies. Different apple varieties together with differences in larval development, greatly influenced biological traits such as larval seems to determine the potential for population survival,duration of development,and adult fecun- growth on different apple varieties. dity. High plasticity in Medfly life history traits in Based on this, we suggest that Golden Delicious response to different environments (including host apples contribute more than Granny Smith and species) is an important attribute that explains the Red Delicious to the population growth of Medfly wide geographical distribution of the species and in autumn in northern Greece and other areas the ample range of the hosts that it attacks. in which Medfly infests apples. Since Golden In a recent study, we managed to rear C. capitata Delicious apples were the more favourable of the in Golden Delicious apples in the laboratory and three varieties for the development and survival we concluded that apple is not as favourable a host of immatures and for female oviposition, we for the development of the Mediterranean fruit fly expected that this would be the most susceptible as other hosts such as figs, peaches, bitter oranges of the varieties tested in field infestation tests. (Papadopoulos et al.2002).The results of this study Indeed, Golden Delicious does suffer greater showed that Golden Delicious was the most infestation in the field than Granny Smith and Red favourable of the three varieties tested; however, Delicious (Papadopoulos et al. 2001). However, 22 Proceedings of the 6th International Fruit Fly Symposium other factors such as the temporal pattern of the partment of Agriculture,University of Thessaloniki) ripening period, and the characteristics of the for technical assistance. varieties regarding Medfly host selection (colour, odouretc.)mightalsoaccountforthedifferencesin REFERENCES field infestation between the varieties and for their CAREY, J.R. 1984. Host specific demographic studies of the Mediterranean fruit fly Ceratitis capitata. Ecologi- contribution to C. capitata population growth. cal Entomology 9: 261–270. Pulp (mesocarp) firmness of the apples on which KRAINACKER, D.A., CAREY, J.R. & VARGAS, R.I. 1987. Effect females oviposited seemed to be the main factor of larval host on life history traits of the Mediterra- determining fecundity rates. Females laid 2.3 neanfruitfly,Ceratitiscapitata. 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