Host utilization by the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae)
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1 Proceedings of 6th International Fruit Fly Symposium 6 10 May 2002, Stellenbosch, South Africa pp Host utilization by the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae) D.F. Segura*, M.T. Vera & J.L. Cladera IGEAF, INTA Castelar (CC25), Los Reseros y Las Cabañas, Castelar (1712), Buenos Aires, Argentina Host utilization by fruit flies has traditionally been studied using data on infestation levels found in different hosts. This analysis does not allow any comparison among hosts, because the variables are affected by the carrying capacity (i.e. maximum number of pupae/kg of fruit) of each host. Also, the data from different hosts species cannot be pooled to obtain a global measure of the degree of exploitation of available resources. In this study, host utilization by the Mediterranean fruit fly, Ceratitis capitata (Wied.), was determined by defining a new variable, percentage of exploited resource (PER), which relates the extracted pupae in a host with the maximum quantity of pupae extractable in the same host, in order to: 1) compare host utilization with host availability (globally and for each host species); 2) compare host utilization among fruit species; and 3) analyse the effect of environmental variables on the capacity of the C. capitata population to exploit this resource during the reproductive season. The results showed that PER values reached by any host species were never higher than 60%, and that the maximum PER value obtained by pooling all species together in a given sample was below 35%, suggesting that host availability is not a limiting resource in this system. However, PER was not constant over time, probably indicating periods in which competition becomes more intense. These fluctuations were associated with biotic and abiotic factors, which in turn determine the fluctuations in the activity and abundance of adults. No association was found between global PER and global availability of hosts, probably due to the lack of synchrony between C. capitata population levels and host availability. For each species, PER usually showed a gradual growth that ended sharply when the host disappeared,while the host availability grew, reached a maximum and then dropped gradually. Apparently, during this gradual reduction in host availability, fruit fly infestations are confined to the few available fruits of the same species, instead of using other host species with higher abundance. Significant differences were found comparing PER among hosts species. In most cases, the host species with a high PER were those with a high carrying capacity, indicating that C. capitata was preferentially exploiting the hosts with better yield. This behaviour probably tends to improve the fitness of the females. INTRODUCTION The nature of the relationship between fruit flies and their host plants (and the effect of the environment on this relationship) is of fundamental importance for an understanding of strategies for acquiring food, water, oviposition sites and shelter (Prokopy 1982). This is also fundamental in any economically important species for designing effective management tactics. The Mediterranean fruit fly, Ceratitis capitata (Wiedemann), is one of the most important pests in the world due to its destructive capacity. This is partly due to the diversity of fruit species that this insect can use as hosts; more than 350 species from 65 taxonomic families have been listed as hosts for C. capitata (Liquido et al. 1991). Many studies have analysed the relationship between the availability of the different fruit species (hosts for C. capitata) and the population fluctuations of this pest (Vargas et al. 1983; Harris & Lee 1986; Harris & Lee 1987; Harris et al. 1993; *To whom correspondence should be addressed. dsegura@cnia.inta.gov.ar Mazih & Debouzie 1996; Katsoyannos et al. 1998; Debouzie & Mazih 1999; Mavrikakis et al. 2000; Papadopoulos et al. 2001). In general these studies show that the population dynamics of C.capitata is intimately associated with a few hosts species (key hosts). To significantly affect the population fluctuation, a host should present a high abundance and a high carrying capacity (sensu Lack 1954), that is, the capacity to support high infestation levels (Vargas et al. 1983). Another important conclusion of these studies is that the presence of a key host is decisive for determining the population levels reached by the pest, but the presence of a staggered fruiting sequence of diverse fruit species (that includes non-key hosts) also plays an important role (Puzzy & Orlando 1965; Malavasi & Morgante 1981). In spite of efforts to study the interaction between C. capitata and its hosts, there are currently no studies that compare the availability of different hosts with the way in which C. capitata exploits them. Previous studies presented some analyses based on a survey of the abundance of several host
2 84 Proceedings of the 6th International Fruit Fly Symposium species and the infestation levels reached by the fruit fly populations (Malavasi & Morgante 1980; Vargas et al. 1983; Nishida et al. 1985; Jirón & Hedström 1988). Nevertheless, the methodology and analysis used in these studies does not allow an analysis of exploitation of the hosts species by C. capitata, because the differences in carrying capacity among hosts is not considered. A standard measure of exploitation of each host species, considering the differences in quality among them, would be preferable and will allow classifying the different fruit species on a common scale. This would allow comparison of the exploitation of host plants on a global scale. A detailed analysis of the utilization by fruit flies of host plants can produce important information that may allow a better understanding of this complex interaction. An analysis of the effect of the environment on this interaction should also be included in the study. In the present study, the objectives were: 1) to compare host utilization with host availability (globally and for each host species); 2) to compare host utilization among fruit species; and 3) to analyse the effect of environmental variables on the capacity of the C.capitata population to exploit this resource during the reproductive season. Host utilization or exploitation by C. capitata was quantified by dividing the number of pupae extracted from a host fruit by the highest number of pupae obtained from a fruit of the same host species.this new variable measures the proportion of the hosts that is being used by the population and allows the calculation of a global measure of exploitation of this resource regardless of the fruit species involved. It will also allow a comparison of the way in which C.capitata uses each host species. MATERIALS AND METHODS Study area The study area was the Agricultural Experimental Station of the National Institute of Agriculture (INTA) in San Pedro, Argentina (33 41 S, W). This area covers 115 ha and has experimental plantations of orange, two varieties of mandarin (early ripening and late ripening), peach and plum. Other fruit species cultivated on a smaller scale are fig, persimmon, kiwi, feijoa, apple, Asian pear and nectarine. Two species of fruit flies have been reported in this area, C. capitata and Anastrepha fraterculus (Wied.) (Segade & Polack 1999). However, at present A. fraterculus is not detected by the trapping system in use in the area (G. Segade, pers. comm.). Sampling Twelve fortnightly samples were taken between November 1999 and May 2000, and two individual samples were taken in January and February 2001 (samples A and B respectively). Fortnightly samples. The sampling was stratified. Twenty sample units (SUs, trees with ripening fruits) were taken. Each fruit species was a stratum. The number of SUs sampled for each fruit species was assigned proportionally to the number of SUs for that species relative to the total number of SUs. On each sampling date, the whole study area was inspected and the phenological stage of each host species was noted. Only those host species bearing mature fruits (susceptible to fruit fly infestation) were sampled. The SUs in each stratum were selected randomly. In each selected SU, fruits on the ground were counted and then removed. Ten fruits of those that remained on the tree were sampled in each SU. The fruits were transported to the National Centre of Agriculture Investigations of the INTA in Castelar (170 km from the study area), where they were weighed and placed in individual plastic flasks containing sand as pupation substrate. Flasks were examined weekly and the number of pupae obtained was recorded. Pupae were placed in individual containers and maintained at room temperature until adult emergence for identification. Individual sampling (A and B). These samples were carried out on dates on which the highest diversity of fruit species was present (i.e. number of host species). On each sampling date, a total of 50 SUs were sampled. The number of SUs assigned to each fruit species was as homogeneous as possible. For each host species the SUs were selected randomly. Then, the same procedure as for the fortnightly samplings was used. Adult population level of C. capitata Simultaneous to the fortnightly samples, the Plant Health Laboratory of INTA San Pedro monitored the adult C.capitata population density using traps. Two types of traps were used, Jackson traps, baited with trimedlure, and McPhail traps, baited with food attractant (G. Segade, pers. comm.). The data were plotted on a graph. The population level of C.capitata adults on a particular date of fruit sampling was estimated as the area below the curve of the number of flies per trap per day between that date and the previous date of fruit sampling. A separate estimation was made for each trap type.
3 Segura et al.: Host utilization by the Mediterranean fruit fly 85 Data analysis Host utilization. To study how flies used the resource, a new variable, percentage of exploited resource (PER), was developed. This variable was calculated as the ratio (in per cent) between the number of pupae per kg yielded by a fruit in a sampling, and the maximum number of pupae per kg which could be yielded by a fruit of the same species. The maximum number of pupae per kg was defined as the 90 percentile of the distribution of pupae per kg values, for each species and for each sampling date. Fruits that did not yield any pupae were not considered part of the distribution. The ratio between real pupae per kg and the maximum possible pupae per kilogram for each fruit was then calculated. These values were averaged to calculate the PER for each SU. The PER values of all the SUs of the same host species on each sampling date were then averaged to obtain a species PER value (s-per). All the SUs on each sampling date, regardless of the host species, were averaged to obtain a global PER (g-per). Description of host availability. For each sampling date the total availability of the resource was estimated as the sum of the availability recorded for each host species. To estimate the availability of each host species, its abundance was multiplied by its quality as host. Abundance for each host species was obtained by multiplying the estimated weight of ripening fruits per tree by the number of trees in the study area. Host quality was determined from the ratio between the carrying capacity of a species and the maximum carrying capacity recorded among all the species. Thus, host quality does not have any units,and ranges between 1 (the quality of the best host, in terms of pupae/kg yielded) and 0. Correlation between PER and other variables. A correlation analysis between the global PER and several biotic and abiotic variables was performed. The abiotic variables used were daily maximum, mean and minimum temperature (Tmax, Tmean and Tmin, respectively); ground temperature at 5, 10 and 20 cm of depth (Tground 5, Tground 10 and Tground 20, respectively); relative humidity (RH) and precipitation (Pp). For all the variables except Pp, the average of the values of the previous 14 days (the period between two consecutive samplings) was considered as a representative value for the sampling date. For Pp, the sum of the daily values for the same period of time was considered instead of the average. A correlation analysis was also performed between PER and the values of the abiotic variables recorded on the previous sampling date (designated as t 1). The biotic variables used were the C. capitata population levels estimated from McPhail and Jackson traps, and total availability of hosts (Tav). PER variations among host species. Differences in host utilization among fruit species were analysed from data of individual samplings A and B by means of a non-parametric one-way analysis of variance (Kruskal-Wallis) for the PER. In all the analyses the fruit species was considered as the treatment. A separate analysis for each sample (A and B) was performed. Each tree was considered a replicate. When this analysis showed significant differences among species, non-parametric pairwise comparisons were carried out, using the Dunn s test (Hollander & Wolfe, 1976). RESULTS Host utilization Global percentage of exploited resource (g-per) (Fig. 1a) was low (less than 5%) during November and December. It reached values of more than 10% only after January. It then increased to its maximum in the first sampling date of March (32.7%). The g-per then decreased gradually, and a small increase occurred in the last sampling date (May 3). The maximum values of PER reached by each host species varied substantially (Table 1). High values (>40%) were recorded for plum, feijoa, peach, orange and persimmon. Asian pear, fig, nectarine and late mandarin were grouped in a second category (20% < PER < 40%). Other hosts had lower maximum values, near or less than 10%. Host availability The global availability of hosts (Fig. 1b) increased gradually from the first sampling date of December and reached a maximum in January. It then decreased until February, after which it increased again but did not attain very high levels. After the first sampling date in March, the global availability decreased, and no further increase was recorded. Population fluctuations of C. capitata Adults were first detected in traps in December (Fig. 1c).After the first sampling date in January,the number of adults increased rapidly, reaching a maximum in February, after which the population decreased. Towards the end of the sampling period, a small increase was recorded.
4 86 Proceedings of the 6th International Fruit Fly Symposium Fig. 1. a, Global percentage of exploited resource by Ceratitis capitata (average PER from all host species [g-per] and S.E. for each sampling date); b, total host availability; c, population levels of adult C. capitata in McPhail and Jackson traps on each sampling date. Correlation between PER and other variables There was an association (P <0.05) between g-per and the following variables: Tmin t 1 (r = 0.60), Tground t 1 at the three depths (r = 0.63, r = 0.65 and r = 0.68 for 5 cm, 10 cm and 20 cm, respectively), McPhail (r = 0.63) and Jackson (r = 0.62) catches. It is important to emphasize the lack of association between the g-per and Tav (r = 0.07, P > 0.05). The graphs of s-per and host availability (Fig. 2) shows that in most cases (peach, early and late mandarin, plum, feijoa, orange and kiwi) the PER gradually increased. This increase only stopped when the host was no longer available. Host availability increased initially,reached its maximum and then decreased gradually. In some host species (nectarine and apple) both variables increased simultaneously, but in others (persimmon, Asian
5 Segura et al.: Host utilization by the Mediterranean fruit fly 87 Table 1. Maximum percentage of exploited resource by Ceratitis capitata for each host species (s-per), and the sampling date in which these maximum levels occurred. Host species Maximum Sampling s-per (SE) date Plum (11.88) 8 Mar Feijoa (13.11) 3 May Peach (6.77) 9 Feb Orange (11.74) 23 Feb Persimmon (4.94) 8 Mar Asian pear (7.96) 26 Jan Fig (2.62) 8 Mar Nectarine (12.52) 12 Jan Late mandarin (4.07) 9 Feb Early mandarin (3.50) 3 May Apple (10.03) 26 Jan Kiwi 6.54 (5.02) 19 Apr pear and fig) the decrease in host availability was accompanied by a decrease in the PER. PER variations among host species For both samples A and B there were significant differences (P = and P = 0.004, respectively) in the PER among host species (Table 2). For sample A, there were differences between peach and the rest of the species. Peach had the highest value of exploitation. In sample B, there were significant differences in four cases, namely Asian pear and fig, Asian pear and plum, Asian pear and late mandarin, and orange and plum. Asian pear and orange were the hosts with the highest PER values, with peach having an intermediate value. Late mandarin, fig and plum were the hosts with the lowest PER values (Table 2). DISCUSSION The highest PER values for any host species was never more than 60%, and the highest value obtained on a given sampling date (g-per) was less than 35%, indicating that fruit flies did not exploit all the available resource of any host plant. Environmental constraints imposed on this Medfly population, and the existence of other limiting resources or other biotic factors, might prevent the C.capitata population from exploiting the resource to a greater extent. The g-per was not constant over time. There was a fluctuation in the capacity of the population of C. capitata to exploit the resource, which could be explained by fluctuations in the activity or abundance of C. capitata adults during the season. The correlation analysis revealed an association between g-per and temperature (Tmin and Tground), and between g-per and the level of C. capitata adults. The effect of temperature on PER was probably indirect and could be explained by the effect of temperature on the activity and survival of the flies, since a positive correlation has been found between the population levels of adults and temperature (Segura 2001). The fluctuations in the population levels of C. capitata adults would be also responsible for the lack of association between the g-per and the host availability. From November to January the adult population was low and host availability was very high, so a small proportion of the resource was exploited. At the same time that the adult population reached its maximum (in February), the host Table 2. Percentage of exploited resource (PER) by Ceratitis capitata, carrying capacity (maximum number of pupae/kg extracted from a host species) and relative abundance (kg of a individual fruit species/total kg of fruit of all species 100) of each host species in samples A and B. Sample A Sample B PER 1 (S.E.) Carrying Relative PER 1 (S.E.) Carrying Relative capacity abundance capacity abundance Peach 4.51 (1.47) a (4.85) abc Orange 0.00 b (6.70) ab Asian pear 0.00 b (4.02) a Apple 0.00 b Plum 0.92 (0.68) b (2.50) c Fig (2.32) bc Late mandarin (2.69) bc Values followed by the same letter do not differ significantly (P > 0.05). 2 Host species absent in this sample.
6 88 Proceedings of the 6th International Fruit Fly Symposium Fig. 2. Percentage of exploited resource (PER) by Ceratitis capitata and availability (kg) of each host species for each sampling date.
7 Segura et al.: Host utilization by the Mediterranean fruit fly 89 availability dropped. The joint effect of higher numbers of adults and fewer available hosts resulted in higher levels of host utilization (in the last sampling date of February and the first sampling date on March). The level of C. capitata population could thus explain the lack of synchrony between host availability and percentage of exploited resource. The utilization by C. capitata of each host usually increases steadily until the host is no longer available, while host availability initially increases, reaches a maximum and then gradually decreases. Fruit fly infestation seems to be confined to the few fruit available on an individual host species, in spite of the presence of other host species. There are at least three possible explanations for this phenomenon. First, the relative cost to the insect of moving to new hosts is higher than the cost imposed by an increase in larval competition. Severin & Hartung (1912), and Steiner (cited as unpublished data in Christenson & Foote 1959) pointed out that movements of individuals within orchards and between orchards and the surrounds are very common, and they suggested that flies move toward host trees for oviposition and probably to mate, and then return to non-host trees, seeking shelter or food.therefore, it seems unlikely that the cost of moving among plants is high. The second possibility is the Hopkin s Host Selection Principle (Prokopy 1982), which suggests that females have a higher tendency to lay eggs in host species in which they fed as larvae. Nevertheless, Prokopy et al. (1982) working with fruit flies of the genus Rhagoletis (Tephritidae) found no influence of larval experience on adult host selection behaviour. Thirdly, there is evidence, at least for Rhagoletis pomonella, that previous experiences of oviposition in a particular host species can decrease the propensity to search for and accept fruit of another species (Prokopy 1982). In our study, this could explain why females continued using certain species in spite of the presence of other hosts, even though their availability diminished. Females have the capacity to modify their search pattern if the species in which they specialize disappears (Prokopy 1982). Therefore, females will keep searching for the same species even though their abundance diminished. They would switch to another host species only when the preferred host becomes very difficult to find. In other hosts analysed in our study (persimmon, Asian pear and fig), host utilization decreased simultaneously with host availability. In those hosts, it appeared that the adults responded more rapidly to the changes in host availability. Nevertheless, it was impossible to determine whether or not this behaviour was due to the availability of the particular host species or the adult population level, or the combined effect of these two factors. Significant differences were observed in the levels of PER found in each host species. This indicates that some hosts are exploited to a greater extent than others. In most cases, the fruit species that were exploited more intensively were those showing the highest carrying capacity, suggesting that females were taking advantage of hosts species with higher yields. Probably this behaviour tends to increase their reproductive success. The present study put a new perspective on the way in which C. capitata exploits different hosts. The new variable (percentage of exploited resource, PER) enables us to analyse the way in which C. capitata uses each host species, and to compare all hosts species independently of their carrying capacity. Also, PER permits an analysis of the factors (biotic and abiotic) that affect the capacity of this pest to exploit the resource, giving deeper insight into the biology and ecology of this pest. ACKNOWLEDGEMENTS We thank Gonzalo Segade and Andrés Polack at INTA San Pedro for their support and valuable contribution to this study. Also, we would like to thank María Busch for her collaboration in the experimental design and Nancy Kahn for statistical advice. We also thank an anonymous reviewer of a previous version of this manuscript. This study was financed with founding from the Project Foncyt PID 615 to J.L.C. REFERENCES CHRISTENSON, L.D. & FOOTE, R.H Biology of fruit flies. Annual Review of Entomology 5: DEBOUZIE, D. & MAZIH, A Argan (Sapotaceae) trees as reservoirs for Mediterranean fruit fly (Diptera: Tephritidae) in Morocco. 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8 90 Proceedings of the 6th International Fruit Fly Symposium fruit fly (Diptera: Tephritidae) in upland and lowland areas on Kauai, Hawaii. Environmental Entomology, 22: HOLLANDER, M. & WOLFE, D.A Nonparametric Statistical Methods. John Wiley, New York. JIRÓN, L.F. & HEDSTRÖM, I Occurrence of fruit flies of the genera Anastrepha and Ceratitis (Diptera: Tephritidae), and their host plant availability in Costa Rica. The Florida Entomologist 71: KATSOYANNOS, B.I., KOULOUSSIS, N.A. & CAREY, J.R Seasonal and annual occurrence of Mediterranean fruit flies (Diptera: Tephritidae) on Chios Island, Greece: differences between two neighboring citrus orchards. Annals of the Entomological Society of America 91(1): LACK, D The Natural Regulation of Animal Numbers. Clarenden, Oxford. LIQUIDO, N.J., SHINODA, L.A. & CUNNINGHAM, R.T Host plants of the Mediterranean fruit fly (Diptera: Tephritidae): an annotated world review. Miscellaneous Publications of the Entomological Society of America 77: MALAVASI, A. & MORGANTE, J.S Biologia de Moscas-das-frutas (Diptera, Tephritidae). II: Indices de infestação em diferentes hospedeiros e localidades. Revista Brasileira de Biologia 40: MALAVASI, A. & MORGANTE, J.S Adult and larval population fluctuation of Anastrepha fraterculus and its relationship to host availability. Environmental Entomology 10: MAVRIKAKIS, P.G., ECONOMOPOULOS, A.P. & CAREY, J.R Continuous winter reproduction and growth of the Mediterranean fruit fly (Diptera: Tephritidae) in Heraklion, Crete, southern Greece. Environmental Entomology 29: MAZIH, A. & DEBOUZIE, D Infestation rate of argan fruit (Argania spinosa) by the Mediterranean fruit fly (Ceratitis capitata) in relation to phenology and maturation of the fruit. Entomologia Experimentalis et Applicata 81: NISHIDA, T., HARRIS, E.J., VARGAS, R.I. & WONG, T.T.Y Distributional loci and host fruit utilization patterns of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae), in Hawaii. Environmental Entomology 14: PAPADOPOULOS, N.T., KATSOYANNOS, B.I., CAREY, J.R. & KOULOUSSIS, N.A Seasonal and annual occurrence of the Mediterranean fruit fly (Diptera: Tephritidae) in Northern Greece. Annals of the Entomological Society of America 94: PROKOPY, R.J Tephritid relationships with plants. In: Proceedings of the CEC/IOBC International Symposium November 1982, Athens, Greece. PROKOPY, R.J., AVERILL, A.L., COOLEY, S.S., ROITBERG, C.A. & KALLET, Y.C Variation in host acceptance pattern in apple maggot flies. In: Visser, J.H. & Minks, A.K. (Eds) Insect Plant Relationships. Springer Verlag, New York. PUZZY, D. & ORLANDO, A Estudios sobre a ecologia das moscas-das-frutas (Trypetidae) no Estado de São Paulo, visando o controle racional da praga. Arquivos do Instituto Biológico, São Paulo 32: SEGADE, G. & POLACK, L.A Monitoreo de Moscas de la fruta (Diptera: Tephritidae) en montes de duraznero y de cítricos en el Partido de San Pedro, Pcia. de Buenos Aires. In: Book of abstracts of the Primer Taller Internacional sobre Programas de Control y Erradicación de Moscas de los Frutos. SENASA. September Buenos Aires, Argentina. SEGURA, D.F Dinámica del uso del recurso nutricio por estadios inmaduros de Ceratitis capitata (Diptera: Tephritidae). Tesis de Licenciatura, Universidad de Buenos Aires, Argentina. SEVERIN, H.H.P. & HARTUNG, W.J The flight of two thousand marked male Mediterranean fruit flies (Ceratitis capitata Wied.). Annals of the Entomological Society of America 5: VARGAS, R.I., HARRIS, E.J. & NISHIDA, T Distribution and seasonal occurrence of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) on the island of Kauai in the Hawaii Island. Environmental Entomology 12:
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