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Revista Brasileira de Entomologia

On-line version ISSN 1806-9665

Rev. Bras. entomol. vol.55 no.3 São Paulo July./Sept. 2011  Epub Oct 07, 2011

http://dx.doi.org/10.1590/S0085-56262011005000039 

Influence of different tropical fruits on biological and behavioral aspects of the Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera, Tephritidae)

 

 

Anne M. CostaI; Francismare de O. AmorimI; Cyntia S. Anjos-DuarteI; Iara S. Joachim-BravoI,II

IDepartamento de Biologia Geral, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão do Geremoabo s/n, Campus Universitário de Ondina, 40170-290 Salvador-BA, Brasil
IIAuthor for correspondence: ibravo@ufba.br

 

 


ABSTRACT

Influence of different tropical fruits on biological and behavioral aspects of the Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera, Tephritidae). Studies on Ceratitis capitata, a world fruit pest, can aid the implementation of control programs by determining the plants with higher vulnerability to attacks and plants able to sustain their population in areas of fly distribution. The objective of the present study was to evaluate the influence of eight tropical fruits on the following biological and behavioral parameters of C. capitata: emergence percentage, life cycle duration, adult size, egg production, longevity, fecundity, egg viability, and oviposition acceptance. The fruits tested were: acerola (Malpighia glabra L.), cashew (Anacardium occidentale L.), star fruit (Averrhoa carambola L.), guava (Psidium guajava L.), soursop (Annona muricata L.), yellow mombin (Spondias mombin L.), Malay apple (Syzygium malaccense L.), and umbu (Spondias tuberosa L.). The biological parameters were obtained by rearing the recently hatched larvae on each of the fruit kinds. Acceptance of fruits for oviposition experiment was assessed using no-choice tests, as couples were exposed to two pieces of the same fruit. The best performances were obtained with guava, soursop, and star fruit. Larvae reared on cashew and acerola fruits had regular performances. No adults emerged from yellow mombin, Malay apple, or umbu. Fruit species did not affect adult longevity, female fecundity, or egg viability. Guava, soursop, and acerola were preferred for oviposition, followed by star fruit, Malay apple, cashew, and yellow mombin. Oviposition did not occur on umbu. In general, fruits with better larval development were also more accepted for oviposition.

Keywords: Demography; insects; medfly; nutritional ecology; oviposition.


RESUMO

Influência de diferentes frutos tropicais em aspectos biológicos e comportamentais da mosca-das-frutas Ceratitis capitata (Wiedemann) (Diptera, Tephritidae). Estudos em Ceratitis capitata, uma praga agrícola, pode auxiliar na implementação do programa de controle determinando as plantas com maior vulnerabilidade de serem atacadas e plantas capazes de sustentar sua população em áreas de distribuição da mosca. O objetivo deste trabalho foi avaliar a influência de oito frutos tropicais em alguns parâmetros biológicos e comportamentais de C. capitata: porcentagem de emergência, duração do ciclo de vida, tamanho do adulto, produção de óvulos, longevidade, fecundidade, viabilidade dos ovos e aceitação de frutos para oviposição. Os frutos testados foram: acerola (Malpighia glabra L.), caju (Anacardium occidentale L.), carambola (Averrhoa carambola L.), goiaba (Psidium guajava L.), graviola (Annona muricata L.), cajá (Spondias mombin L.), jambo (Syzygium malaccense L.), and umbu (Spondias tuberosa L.). Os parâmetros biológicos foram obtidos colocando larvas recém eclodidas em cada fruto testado. Nos experimentos de aceitação para a oviposição, as moscas foram expostas a dois pedaços das mesmas frutas. A melhor performance foi obtida com goiaba, graviola e carambola. Larvas criadas no caju e na acerola tiveram performance regular. Nenhum adulto emergiu do cajá, jambo ou umbu. As frutas não influenciaram a longevidade dos adultos, fecundidade das fêmeas, ou viabilidade. Goiaba, graviola e acerola foram preferidos para oviposição, seguidos por carambola, jambo, caju e cajá. Oviposição não ocorreu em umbu. Em geral, frutos nos quais houve um melhor desenvolvimento larval, também foram mais aceitos para oviposição.

Palavras-chave: Demografia; ecologia nutricional; insetos; mosca do Mediterrâneo; oviposição.


 

Studies on the biology and behavior of economically important species such as Ceratitis capitata (Wiedemann) (Diptera, Tephritidae) - a major pest of fruit trees worldwide (Christenson & Foote 1960; Bateman 1972; Zucchi 2001) - have contributed for the management and control of agricultural pests. The studies have provided insight for the theoretical approaches to the life history and dynamic distribution of species in different host plants, in addition to baseline information on emergence percentage and mortality for the development of prediction models of population growth and control (Carey 1993).

Several factors can affect the biological and demographic parameters of populations, such as: mass-rearing, body size, adult feeding, and larvae host (Carey 1989). Studies on larvae hosts have shown the influence of several host plants on the demographic parameters of C. capitata larvae (Carey 1984; Krainacker et al. 1987; Zucoloto 1993).

In addition to species biology and demography, oviposition behavior has an important role in the distribution of insect populations among host plants, especially among the holometabolous phytophagous species (Thompson & Pellmyr 1991), where survival of immature flies depends on the nutritional resources selected by adult females (Renwick 1989). Several studies show the controversial and numerous factors influencing oviposition behavior in insects (Jaenike 1990; Barron 2001; Leather 2002; Scheirs 2002), but the main hypothesis for behavior evolution is that females choose hosts that are able to maximize offspring survival and development, in a positive correlation between oviposition preference and larvae performance (Thompson 1988; Thompson & Pellmyr 1991). In this context, a host plant must be able to allow the specimen to complete its normal development in nature (Hanson 1983). A plant becomes a host when two factors occur: the selection by the females at the moment of oviposition and the offspring survival. Oviposition behavior and offspring performance are apparently controlled by different gene sets and therefore, the relationship between preference and performance does not always occur (Futuyma & Peterson 1985; Jaenike 1990). Thus, the introduction of a new host plant in the "menu" of an insect is determined both by female oviposition behavior and immature survival and development (Barron 2001).

Literature data show that although females of holometabolous insects can oviposit in several different hosts, they present a hierarchical behavior by choosing some hosts more often than others (Thompson 1988). In the absence of a favorite host, females can oviposit in less preferred hosts (Wiklund 1981) and a polyphagous species such as C. capitata can also oviposit in usually no-host plants (Aluja & Mangan 2008). The choice of a potential host is determined also by the presence of competitors or natural enemies and by female physiology (Thompson 1988; Jaenike 1990), among other factors. Host plant condition has been recognized as a key factor in controlling agricultural pests. However, assessing such a condition is not a simple task (Aluja & Mangan 2008).

From an evolutionary point of view, the range magnitude of insect hosts has both increased and decreased (Bernays 1998). Aluja & Mangan (2008) reviewed the literature on the issue and suggest that most species of Tephritidae as the most phytophagous insects tend to specialization. They also report that the host status of highly polyphagous species such as the fruit flies must be analyzed at three levels: species, population, and individual levels due to the high variability in patterns of host plant use.

In Brazil, the species C. capitata was introduced in the early 20th century. According to the data compiled by Zucchi (2001), the fly is currently widespread in 16 states and attacks 58 host species, 20 of which are native species. In the Brazilian Northeast, specifically at the San Francisco Valley (Juazeiro, BA - Petrolina, PE) - the greatest fruit tree export region in the country, C. capitata appears as one of the most destructive pests, receiving high levels of investments for technical control, including the SIT (Sterile Insect Technique) (Enkerlin 2005).

Data on the biology and the oviposition behavior of this species can help identify its preferred hosts, those hosts able to support the fly population, and other potential hosts. According to Aluja & Mangan (2008), potential hosts are those not yet infested in the field, but already infested in controlled conditions and considered able to sustain the larval cycle due to the high adaptability of flies.

The aim of the present work was to evaluate the influence of eight traditionally grown and sold tropical fruits in the Northeast of Brazil, on the biological parameters and oviposition behavior of the fruit fly C. capitata. The different fruits were compared only by the nutritional point of view, i.e. chemical and physical aspects of the interior of the fruit that affect the development and survival of offspring. Other variables that can also affect oviposition behavior, such as fruit color, shape, and density, in addition to presence of competitors or natural enemies were not studied.

 

MATERIAL AND METHODS

The C. capitata strain used in this research has been kept at the Laboratory of Insect Nutritional Ecology (IBio/UFBA) for approximately 12 years; occasionally, wild flies have been introduced. Maintenance of the strain follows the methodology described by Zucoloto (1987).

The fruits tested were: acerola (Malpighia glabra L.), yellow mombin (Spondias mombin L.), cashew (Anacardium occidentalis L.), star fruit (Averrhoa carambola L.), guava (Psidium guajava L.), soursop (Annona muricata L.), Malay apple (Syzygium malaccensis L.), and umbu (Spondias tuberosa L.). These fruits have considerable socioeconomic importance, especially in the Northeast of Brazil, and all of them have had records of infestation by C. capitata (Zucchi 2001; Araujo et al. 2005). The fruits were purchased in supermarkets to reduce the possibility of obtaining infested fruits. Before use, the fruits were washed to remove agricultural residues and then stored in refrigerator or freezer to maintain their qualities.

To evaluate the development and immature survival, twenty-five newly hatched larvae of C. capitata were placed on small pieces (±5.0 g) of fruit, on Petri dish lined with filter paper. New pieces of fruit were added daily, until the end of larval development. Six replicates of each fruit were tested, and the following parameters were analyzed: emergence percentage, life cycle duration (hatching to emergence), egg production during the first five days of female life, before the oviposition period (pre-oviposition period), and adult size (estimated by measuring a wing vein, R4+5 to cu-m). Fifteen females in each fruit had their wings measured and the eggs counted.

Acceptance of fruits for oviposition (oviposition preference) was assessed using no-choice tests. Five couples of newly emerged flies were placed in plastic cages (9.0 x 7.5 cm) containing water and a yeast-based diet. At the oviposition peak (approximately 15 days after emergence), the tested fruits were offered for female oviposition in two small pieces (5.0g) placed at equidistant locations. Twenty-four hours later the old pieces were replaced by fresh ones, and the test was concluded 48 hours later. All fruit pieces were identified and frozen for later counting of the eggs. Ten replicates were performed for each fruit. The cages had fluorescent lamps (12 hours of light) to stimulate oviposition. Results of these tests were compared with immature performance tests for each fruit.

Adult longevity and fecundity, and egg viability (F2) were used to evaluate fruit influence on adult performance. The tests were performed only with cashew, guava, soursop, and star fruit, the only fruits with sufficient numbers of emerged adults.

Adult longevity was measured in 50 couples in each fruit. The specimens were separated by sex, placed individually in transparent cages (9.0 x 7.5 cm), and fed with saturated sugar solution and water ad libitum. The adults were observed daily, until death.

Female fecundity was assessed by placing five sexually mature couples in a transparent cage (15 x 13 cm) and feeding them with sucrose solution, water, and a yeast based diet to increase egg production. Adult protein intake increases egg production (Cangussu & Zucoloto 1997). Eggs were counted daily until the female death. Ten replicates were conducted for each fruit.

Egg viability was studied in 100 eggs of flies reared in each fruit. The eggs were collected, transferred to a Petri dish (50 x 10 mm) containing moistened filter paper, and observed every 12 hours for larvae eclosion. All experiments were conducted at 25ºC and 75% relative humidity, in the dark (larvae experiments), or 12 hours of light per day (adult experiments).

The biological parameters and oviposition preferences were compared using one-way ANOVA and the Tukey-Kramer's test for multiple comparisons. The Kruskal-Wallis test (with Dunn's test for multiple comparisons) was used to analyze the longevity data. All tests were performed using GraphPad Instat Software (1997 version, San Diego), at a critical value for an error probability of 5%.

 

RESULTS

The best performances of the biological parameters (Table I) occurred in guava, soursop, and star fruit, with emergence averages equal or above 60%, life-cycle 14-18 days and 12-21 eggs/female. Larvae reared on cashew and acerola fruits had regular performances: 30-45% emergence, 19-20 days of life-cycle, and 06-11 eggs/female during the pre-oviposition period. No adults emerged from larvae reared on yellow mombin, Malay apple, or umbu. Adults reared on the different fruits had similar sizes at emergence (p > 0.05).

 

 

Oviposition preference was ranked from higher to lower: guava, soursop, and acerola were first, followed by star fruit, Malay apple, cashew, and yellow mombin (Fig. 1). Flies did not oviposit on umbu. In general, fruits providing better larvae development were also well accepted for oviposition.

 

 

Fecundity, adult longevity, and egg viability were not statistically different among flies fed on cashew, star fruit, soursop or guava during the immature stage (p > 0,05) (Table II).

 

 

DISCUSSION

Food consumption highly determines the growth, development, and reproduction of species. Therefore, the quantity and quality of food consumed by immature insects determine their early development and adult lives, and affect the demographic parameters of populations (Slansky & Scriber 1985).

In holometabolous phytophagous insects, adult females face the challenge of finding appropriate food for the immature insects, during oviposition (Via 1986; Thompson 1988). In general, the female behavior can be shaped by processes of natural selection related to two events: i. the phytochemical coevolution between plants and phytophagous insects, and ii. the selective pressure of natural enemies (Aluja & Mangan 2008). The former has led to the discussion about the discrimination degree among generalist (polyphagous) and specialist (olygophagous and monophagous) host insects (Wilklund 1981).

According to Bernays (2001), polyphagous insects have less ability than monophagous insects in perceiving and discriminating among large quantities of volatile substances (neural limitation hypothesis). Other authors argue that polyphagous insects choose their hosts primarily by the nutritional value of plants, and specialists by secondary substances (Edwards & Wratten 1980).

In our study, although a polyphagous species, C. capitata showed discrimination capability and hierarchy in oviposition preference for several fruits tested. This suggests a preference association with the nutritional value of the fruit to feed the larvae; in general, fruits with the largest numbers of eggs were also the best in providing insect development at the immature stage. This can be an advantage in the evolutionary trait because females preferred appropriate resources for their offspring, according to the preference-performance theory. This event may also be related to the hypothesis of evolution of the oviposition behavior, which states females will choose plant species that maximize larvae survival and development (Thompson & Pellmyr 1991; Janz 2002). Studies on this subject are still controversial. According to Joachim-Bravo & Zucoloto (1997), there was no correlation between oviposition preference and larval performance in C. capitata if deemed the nutritional value of the artificial diet. Furthermore, Fernandes-da-Silva & Zucoloto (1993) did not observe any oviposition preference of C. capitata for the most nutritional fruit parts. However, it is possible to infer that females of C. capitata in nature can recognize the most suitable hosts and lay more or less eggs accordingly, with consequences for the relevance of particular plants to sustain the species population.

According to Malavasi & Morgante (1980), host origin is one of the determinants of fruit infestation levels in Brazil, with native fruits being more infested by Anastrepha (native of the Americas) and exotic fruits by C. capitata (native of the Mediterranean).

In the Anacardiaceae family, especially in genus Spondias, several fruit species are hosts of Tephritidae, mainly Anastrepha spp. (Malavasi et al. 1980; Zucchi 2000). In our study, C. capitata larvae did not perform well on umbu (S. tuberosa) or yellow mombin (S. mombin), resulting in absence of emergence and suggesting that these fruits cannot sustain C. capitata populations from a nutritional standpoint. These fruits were rarely accepted for oviposition, indicating the possible occurrence of an association between preference and performance among these flies. Recent field data showed that umbu infestation by C. capitata was recorded for the first time in 1999-2000 in Rio Grande do Norte state (Brazil), at a low rate (0.04 pupae/Kg of fruit) (Araujo et al. 2005). Yellow mombin was reported as host for C. capitata by Malavasi et al. (1980), according Zucchi (2001). Recent infestation studies, however, have reported yellow mombin as a host only for Anastrepha (Carvalho et al. 2004; Souza et al. 2007; Leal et al. 2009).

No adult emergence was observed in Malay apple. According to Zucchi (2001), only Costa Lima (1926) reported Malay apple as a host for C. capitata in Brazil. Our results for oviposition preference showed its unattractiveness to females, indicating a potential inadequacy of Malay apple as host for C. capitata.

Of all the fruits belonging to the Anacardiaceae family as tested in our study, cashew was the only one to provide a reasonable development of immature individuals. Cashew was not preferred by females for oviposition, supporting the few infestation records obtained in field. Only Canal D. (1997), in the north of Minas Gerais state (Brazil), recorded cashew as C. capitata host. The correlation of results obtained here and the infestation data collected in the field suggest that the low infestation by C. capitata was probably caused by the inadequate nutrition provided by cashew.

We also found a clear preference-performance relationship in guava and soursop, two native fruits. Compared with other fruits, they received more eggs and provided better immature performance. Although often known as a primary host plant of genus Anastrepha (Araujo et al. 2005), guava is also reported as C. capitata host in Brazil (Zucchi 2001) and in other regions of the world (Woods et al. 2005). In Brazil, different studies show that guava infestation by C. capitata is lower than by Anastrepha (Malavasi et al. 1980; Uchoa-Fernandes et al. 2002; Araujo & Zucchi 2003; Corsato 2004). However, guava can adequately host and sustain populations of C. capitata in terms of nutrition and attractiveness for oviposition. A possible competition with Anastrepha might explain the lower rate of C. capitata on guava. Studies show the occurrence of interspecific interactions between polyphagous species of Tephritidae introduced in areas already occupied by other polyphagous species of Tephritidae, resulting in niche changes and a decrease in number of individuals belonging to the pre-established species (Duyck et al. 2004). In this case, we can expect that C. capitata changes or displaces niches of Anastrepha. Other studies suggest that Anastrepha species compete with C. capitata for oviposition on the same fruits. Castilho (1987) noted that adults of Anastrepha striata Schiner attack adults of C. capitata, and remove them from the guava fruit. In laboratory experiments with mango, Camargo et al. (1996) observed that Anastrepha obliqua Macquart removed C. capitata of fruits in 60.4% of the encounters, indicating that A. obliqua is probably a better competitor because it is bigger.

Soursop has been reported as C. capitata host in Brazil by Canal D. (1997) and as occasional host in other regions (Thomas et al. 2008). Woods et al. (2005) refer to soursops as non-primary hosts but report that 103 individuals of C. capitata emerged from a single fruit. This soursop infestation index per Kg of fruit (296 individuals/Kg of fruit) was greater than the mango infestation index (228 individuals/Kg of fruit) obtained in the same study. These data support our results related to soursop nutritional quality for the development of immature C. capitata.

The results we obtained with acerola and star fruit were not compatible with the preference-performance relationship. Acerola is well-accepted for oviposition, as reported in studies showing its high infestation by C. capitata (Albuquerque et al. 2002; Araujo et al. 2005; Souza et al. 2008). However, unexpectedly, acerola emergence percentage was lower than in other fruits preferred for oviposition. It could be happen because, in laboratory, acerola had faster maturity than star fruit.

Star fruit has been registered as host of C. capitata (Zucchi 2001; Feitosa et al. 2007), with high levels of infestation (Araújo et al. 2005). In our study, although the fruit nutritional value was appropriate for immature individuals, it was not well accepted for oviposition when compared with other fruits. However, it is interesting to note that the rates of infestation by C. capitata do not always coincide with female oviposition preferences. Kolbe & Eskafi (1989), who studied the infestation pattern by C. capitata on different hosts in a region in Guatemala, found that some fruits with moderate infestation were preferred for oviposition. In contrast, other fruits with high numbers of pupae per kilogram were less preferred for oviposition. Further studies should be conducted on the factors leading to such results.

Unlike the development of immature individuals, adult parameters (adult longevity, fecundity, and egg viability in F2 generation) apparently were not affected by larvae rearing on different fruits. Studies have shown that higher protein ingestion during the immature phase improve adult performance, such as higher fecundity rates (Ferro & Zucoloto 1990; Cangussu & Zucoloto 1997).

When explaining the data obtained in the present study, we must consider that a selection among the immature individuals might have occurred during the larval stage and, consequently, those who reached adulthood emerged with minimum necessary nutritional reserves even when on poor hosts. This hypothesis can be supported by the different emergence percentage results obtained among all the fruits tested. Therefore, we can argue that the fruit nutritional traits are more important for individuals at immature development stages than for the adult biological parameters. These are rather primarily determined by adults´ diet.

 

ACKNOWLEDGMENTS

We thank FAPESB (Fundação de Amparo à Pesquisa do Estado da Bahia) for the Scientific Initiation scholarship granted to the first author.

 

REFERENCES

Albuquerque, F. A.; F. C. Pattaro; L. M. Borges; R. S. Lima & A. V. Zabini. 2002. Insetos associados à cultura da aceroleira (Malpighia glabra L.) na região de Maringá, Estado do Paraná. Acta Scientiarum 24: 1245-1249.         [ Links ]

Aluja, M & R. L. Mangan. 2008. Fruit fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annual Review of Entomology 53: 473-502.         [ Links ]

Araujo, E. L. & R. A. Zucchi. 2003. Moscas-das-frutas (Diptera: Tephritidae) em goiaba (Psidium guajava L.), em Mossoró, RN. Arquivos do Instituto Biológico 70: 73-77.         [ Links ]

Araujo, E. L.; M. K. Medeiros; V. E. Silva & R. A. Zucchi. 2005. Moscas-das-Frutas (Diptera: Tephritidae) no Semi-Árido do Rio Grande do Norte: Plantas Hospedeiras e Índices de Infestação. Neotropical Entomology 34: 889-894.         [ Links ]

Barron, A. B. 2001. The Life and Death of Hopkins' Host-Selection Principle. Journal of Insect Behavior 14: 725-737.         [ Links ]

Bateman, M. A. 1972. The ecology of fruit flies. Annual Review of Entomology 17: 493-518.         [ Links ]

Bernays, E. A. 1998. Evolution of feeding behavior in insect herbivores. BioScience 48: 35-44.         [ Links ]

Bernays, E. A. 2001. Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annual Review of Entomology 46: 703-27.         [ Links ]

Camargo, C. A.; E. Odell & L. F. Jirón. 1996. Interspecific interactions and host preference of Anastrepha obliqua and Ceratitis capitata (Diptera: Tephritidae), two pests of mango in Central America. Florida Entomologist 79: 266-268.         [ Links ]

Canal, N. A. 1997. Levantamento, flutuação populacional e análise faunística das espécies de moscas-das-frutas (Dip., Tephritidae) em quatro municípios do Norte de Minas Gerais. PhD Thesis, Piracicaba, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 113 p.         [ Links ]

Cangussu, J. A. & F. S. Zucoloto. 1997. Effect of protein sources on fecundity, food acceptance and sexual choice by Ceratitis capitata (Diptera, Tephritidae). Revista Brasileira de Biologia 5: 611-618.         [ Links ]

Carey, J. R. 1984. Host-specific demographic studies of the Mediterranean fruit fly Ceratitis capitata. Ecological Entomology 9: 261-270.         [ Links ]

Carey, J. R. 1989. Demographic analysis of the fruit flies, p. 253-265. In: A. S. Robinson & G. Hooper (eds.). Fruit flies, their biology, natural enemies and control, Vol. 3B. Elsevier Science Publishers B.V, xv + 447 p.         [ Links ]

Carey, J. R. 1993. Applied demography for biologists with special emphasis on insects. New York, Oxford University Press, 206 p.         [ Links ]

Carvalho, C. A. L.; W. S. Santos; A. C. V. L. Dantas; O. M. Marques & W. S. Pinto. 2004. Moscas-das-frutas e parasitóides associados a frutos de cajazeiras em Presidente Tancredo Neves-Bahia. Magistra 16: 85-90.         [ Links ]

Castillo, E. 1987. Combate químico de Anastrepha striata (Diptera: Tephritidae) en cinco variedades de Psidium guajava L., en Turrialba, Costa Rica. Tesis Ing. Agr., San José, Universidad de Costa Rica, Facultad de Agronomía. 61 p.         [ Links ]

Christenson, L. D. & R. H. Foote. 1960. Biology of fruit flies. Annual Review of Entomology 5: 171-192.         [ Links ]

Corsato, C. D. A. 2004. Moscas-das-frutas (Diptera: Tephritidae) em pomares de goiaba no norte de Minas Gerais: biodiversidade, parasitóides e controle biológico. PhD Thesis, Piracicaba, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 95 p.         [ Links ]

Costa Lima, A. 1926. Sobre as moscas-das-frutas que vivem no Brasil. Chácaras e Quintais 34: 21-234.         [ Links ]

Duyck, P. F.; P. David & S. Quilici. 2004. A review of relationships between interspecific competition and invasions in fruit flies (Diptera: Tephritidae). Ecological Entomology 29: 511-520.         [ Links ]

Edwards, P. J. & S. D. Wratten. 1980. Ecology of Insect-Plant Interactions. London, Edward Arnold Publishers, iv + 60 p.         [ Links ]

Enkerlin, W. R. 2005. Impact of fruit fly control programmes using the sterile insect technique, p. 651-76. In: Dyck, V. A.; J. Hendrichs & A. S Robinson (eds.). Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, Springer, 787 p.         [ Links ]

Feitosa, S. S.; P. R. R. Silva; L. E. M. Pádua; M. P. S. Sousa; E. P. Passos & A. A. R. A. Soares. 2007. Primeiro registro de moscas-das-frutas (Diptera: Tephritidae) em carambola nos municípios de Teresina, Altos e Parnaíba no estado do Piauí. Semina, Ciências Agrárias 28: 629-634.         [ Links ]

Fernandes-da-Silva, P. G. & F. S. Zucoloto. 1993. The influence of host nutritive value on the performance and food selection in Ceratitis capitata (Diptera, Tephritidae). Journal of Insect Physiology 39: 883-887.         [ Links ]

Ferro, M. I. T. & F. S. Zucoloto. 1990. Influence of amino acid deletion on egg production and egg laying by Ceratitis capitata. Revista Brasileira de Biologia 51: 407-412.         [ Links ]

Futuyma, D. J. & S. C. Peterson. 1985. Genetic variation in the use of resources by insects. Annual Review of Entomology 30: 217-238.         [ Links ]

Hanson, F. E. 1983. The behavioral and neurophysical basis of food-plant selection by lepidopterous larvae, p. 3-23. In: S. Amahd (ed.). Herbivorous Insects: Host Seeking Behavior and Mechanisms. New York, Academic Press, xvi + 257 p.         [ Links ]

Jaenike, J. 1990. Host specialization in phytophagous insects. Annual Review of Ecology and Systematics 21: 243-273.         [ Links ]

Janz, N. 2002. Evolutionary ecology of oviposition strategies, p. 349-376. In: M. Hilker & T. Meiners. Chemoecology of Insect Eggs and Egg Deposition. Berlin, Blackwell, p.         [ Links ]

Joachim-Bravo, I. S. & F. S. Zucoloto. 1997. Oviposition preference in Ceratitis capitata (Diptera, Tephritidae): influence of rearing diet. Iheringia, Série Zoologia 82: 133-140.         [ Links ]

Krainacker, D. A.; J. R. Carey & R. I. Vargas. 1987. Effect of larval host on life history traits on the Mediterranean fruit fly, Ceratitis capitata. Oecologia 73: 583-590.         [ Links ]

Kolbe, M. E. & F. M. Eskafi. 1989. Method to rank host plants infested with Mediterranean fruit fly, Ceratitis capitata in multiple host situation in Guatemala. Florida Entomologist 72: 708-711.         [ Links ]

Leal, M. R.; S. A. S. Souza; E. L. Aguiar-Menezes; M. Lima-Folho & E. B. Menezes. 2009. Diversidade de moscas-das-frutas, suas plantas hospedeiras e seus parasitóides nas regiões Norte e Noroeste do Estado do Rio de Janeiro, Ciência Rural 39: 627-634.         [ Links ]

Leather, S. R. 2002. Does variation in offspring size reflect strength of preference performance index in herbivorous insects? Oikos 96: 192-195.         [ Links ]

Malavasi, A. & A. J. Morgante. 1980. Biologia de "moscas-das-frutas" (Diptera, Tephritidae). I. Índices de infestação em diferentes hospedeiros e localidades. Revista Brasileira de Biologia 40: 17-24.         [ Links ]

Malavasi, A.; J. S. Morgante & R. A. Zucchi. 1980. Biologia de "moscas-das-frutas". I. Lista de hospedeiros e ocorrência. Revista Brasileira de Biologia 40: 9-16.         [ Links ]

Renwick, J. A. A. 1989. Chemical ecology of oviposition in phytophagous insects. Experientia 45: 223-228.         [ Links ]

Scheirs, j. 2002. Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos 96: 187-191.         [ Links ]

Slansky, F. J. R. & M. R. Scriber. 1985. Food consumption and utilization, p. 88-151. In: S. A. Kerkut & J. F. Gilbert (eds.). Comprehensive Insects Physiology. Biochemistry and Pharmacology. vol. 8, Oxford, Perganom Press, 595 p.         [ Links ]

Souza, S. A. S.; C. M. A. Santos; A. L. S. Resende; E. B. Menezes & E. L. Aguiar-Menezes. 2007. Índices de infestação de Spondias uútea L. por moscas-das-frutas (Diptera: Tephritidae) e seus parasitóides no município de Seropédica, RJ. Magistra 19: 25-30.         [ Links ]

Souza, A. J. B.; M. G. A. Lima; J. A. Guimarães & A. E. Q. Figueiredo. 2008. Moscas-das-frutas (Diptera: Tephritidae) associadas às plantas hospedeiras do pomar do Campus do PICI da Universidade Federal do Ceará. Arquivos do Instituto Biológico 75: 21-27.         [ Links ]

Thomas, M. C.; J. B. Heppner; R. E. Woodruff; H. V. Weems; G. J. Steck & T. R. Fasulo. 2008. Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Insecta: Diptera: Tephritidae). EENY-214 (IN371). Available from http://creatures.ifas.ufl.edu. (accessed 15 December 2010).         [ Links ]

Thompson, J. N. 1988. Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomologia Experimentalis et Applicata 47: 3-14.         [ Links ]

Thompson, J. N. & O. Pelmyr. 1991. Evolution of oviposition behavior and host preference in Lepidoptera. Annual Review of Entomology 36: 65-89.         [ Links ]

Uchôa-Fernades, M. A.; I. Oliveira; R. M. S. Molina & R. A. Zucchi. 2002. Species diversity of frugivorous flies (Diptera: Tephritoidea) from hosts in the Cerrado of the state of Mato Grosso do Sul, Brazil. Neotropical Entomology 31: 515-524.         [ Links ]

Via, S. 1986. Genetic covariance between oviposition preference and larval performance in an insect herbivore. Evolution 40: 778-785.         [ Links ]

Wilklund, C. 1981. Generalist vs. specialist oviposition behaviour in Papilio machaon (Lepidoptera) and functional aspects on the hierarchy of oviposition preference. Oikos 36: 163-170.         [ Links ]

Woods, B.; I. B. Lacey; C. A. Brockway & C. P. Johnstone. 2005. Hosts of Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera:Tephritidae) from Broome and the Broome Peninsula, Western Australia. Australian Journal of Entomology 44: 437-441.         [ Links ]

Zucchi, R. A. 2000. Espécies de Anastrepha, sinonímias, plantas hospedeiras e parasitóides, p. 41-48. In: A. Malavasi & R. A. Zucchi (eds.). Moscas-das-frutas de importância econômica no Brasil. Conhecimento básico e aplicado. Ribeirão Preto, Holos Editora, 327 p.         [ Links ]

Zucchi, R. 2001. Mosca-do-mediterrâneo, Ceratitis capitata (Diptera: Tephritidae), p. 15-22. In: E. F. Vilela, R. A. Zucchi & F. Cantor (eds.). Histórico impacto das pragas introduzidas no Brasil. Holos Editora, Ribeirão Preto, Brasil.         [ Links ]

Zucoloto, F. S. 1987. Feeding habits of Ceratitis capitata: Can larvae recognize a nutritional effective diet? Journal of Insect Physiology 33: 349-353.         [ Links ]

Zucoloto, F. S. 1993. Acceptability of different Brazilian fruits to Ceratitis capitata (Diptera: Tephritidae) and fly performance o each species. Brazilian Journal of Medical and Biological Research 26: 291-298.         [ Links ]

 

 

Received 21/1/2010; accepted 5/8/2011
Editor: Mauricio Osvaldo Moura

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