Entomologia Experimentalis et Applicata 90: 149–155, 1999. 149 © 1999 Kluwer Academic Publishers. Printed in the Netherlands.

Larval predation by albiceps on macellaria, and

Lucas Del Bianco Faria1,Let´ıcia Orsi1, Luzia Aparecida Trinca2 & Wesley Augusto Conde Godoy1,∗ 1Departamento de Parasitologia, IB, Universidade Estadual Paulista, Rubião Junior, 18618-000 Botucatu, São Paulo, ; 2Departamento de Bioestat´ıstica, IB, Universidade Estadual Paulista, Botucatu, São Paulo, Brazil; ∗Author for correspondence

Accepted: December 3, 1998

Key words: , larval predation, blowflies, interspecific interaction, Diptera,

Abstract Chrysomya albiceps, the larvae of which are facultative predators of larvae of other dipteran species, has been introduced to the Americas over recent years along with other Old World species of blowflies, including Chrysomya megacephala, Chrysomya putoria and Chrysomya rufifacies. An apparent correlate of this biological invasion has been a sudden decline in the population numbers of , a native species of the Americas. In this study, we investigated predation rates on third larvae of C. macellaria, C. putoria and C. megacephala by third instar larvae of C. albiceps in no-choice, two-choice and three-choice situations. Most attacks by C. albiceps larvae occurred within the first hour of observation and the highest predation rate occurred on C. macellaria larvae, suggesting that C. albiceps was more dangerous to C. macellaria than to C. megacephala and C. putoria under these experimental conditions. The rates of larvae killed as a result of the predation, as well as its implications to population dynamics of introduced and native species are discussed.

Introduction 1983; Braack, 1986). As a result of the introduc- tion of Chrysomya species to the Americas, the native Biological invasions frequently cause severe changes species, Cochliomyia macellaria, has shown a sudden in the structure of local communities (Hengeveld, decline in population numbers, which may be attribut- 1989; Andow et al., 1993). However, conclusions able to direct and indirect effects of the introduced about the impact of invaders on native species are species (Guimarães et al., 1979; Prado & Guimarães, rarely based on careful investigation (Simberloff, 1982; Greenberg & Szyska, 1984; Wells & Kurahashi, 1991). Holometabolous such as flies, have life 1997). stages that can easily be transported from one place Several factors can contribute to the success or fail- to another, resulting in the frequent invasion and col- ure of species whose development occurs in carrion. onization of new areas (Gagné et al., 1982; Laurence, This substrate is ephemeral and flies that feed upon it 1986). rarely complete more than one generation on a single Within the last two decades, four species of carrion item (Beaver, 1977; Atkinson & Shorrocks, blowflies, Chrysomya albiceps, C. megacephala, 1981, 1984; Kneidel, 1984a, b; Ives, 1988). The size C. putoria and C. rufifacies have been introduced to of the carrion may limit the availability of food and the Americas (Guimarães et al., 1978; Baumgartner in turn influence the life history of the populations & Greenberg, 1984; Laurence, 1986; Wells, 1991). (Denno & Cothran, 1975; Kuusela & Hanski, 1982). These species are among the main consumers of car- The number of or larvae in carrion frequently rion, a substrate used as a food resource by a wide exceeds its carrying capacity (Kneidel, 1984a, b), variety of species (Peschke et al., 1987; Putman, 150 and often leads to competition for food and predation introduction of the genus Chrysomya in the Amer- (Levot et al., 1979; Goodbrod & Goff, 1990). These icas has influenced local community structure. For processes are important in biological invasions be- this, we studied predation by third instar larvae of cause invading species may compete with or prey upon C. albiceps on third instar larvae of C. macellaria, native species and reduce the survival rates of the latter C. putoria,andC. megacephala in no-choice and two- (Hengeveld, 1989; Wells & Greenberg, 1992a–c). and three-choice situations. These results should also Similarities in the ecological niches of the genus indicate whether C. albiceps has a preference for a Chrysomya and C. macellaria, e.g. in the food re- given species during predation behaviour. quirements of their larvae, suggest the occurrence of interspecific interactions (Ullyett, 1950; Guimarães et al., 1979; Ferreira, 1983; Guimarães, 1984; Wells & Materials and methods Greenberg, 1992b). Evidence for such interactions, in- cluding competition, comes from field and laboratory Laboratory populations of C. albiceps, C. putoria, experiments which show the superior competitiveness C. megacephala and C. macellaria were founded from of C. rufifacies, probably as a result of this species’ specimens collected on the Campus of the Universi- facultative predation on C. macellaria larvae (Wells dade Estadual Paulista, Botucatu, São Paulo, Brazil. & Greenberg, 1992b,c, 1994). Like C. rufifacies, Adult flies were maintained at 25  1 ◦C in cages C. albiceps is a facultative predator of other dipteran (30 × 30 × 30 cm) covered with nylon and had access larvae (Fuller, 1934; Coe, 1978; Gagné, 1981; Erz- to water and sugar ad libitum. Eggs were obtained by inçlioglu & Whitcombe, 1983) and this habit most providing females with fresh beef liver. Hatched lar- likely has an important influence on other species, par- vae were reared on an excess of ground beef until the ticularly in communities where there is reduction in third instar in all species, at which point the flies were the population size of native species (Hanski, 1977; placed in empty vials (7 × 6 cm) in different combina- Wells & Greenberg, 1992a–c; Goodbrood & Goff, tions to estimate predation rates. The larval instar was 1990). Wells & Greenberg (1992a–c) reported that determined using morphological characters to separate larval predation by C. rufifacies reduced the num- the various developmental stages of blowflies (Prins, ber of C. macellaria under natural and experimental 1982; Greenberg & Szyska, 1984; Erzinçlioglu, 1987, conditions. 1990; Tantawi & Greenberg, 1993). There has been no systematic study of the inter- Predation rates were evaluated in three settings. actions between the introduced species C. albiceps, In the first setting, single individuals of C. albiceps C. putoria,andC. megacephala, and the native species and C. macellaria, C. albiceps and C. putoria, and C. macellaria. Furthermore, nothing is known of the C. albiceps and C. megacephala larvae were confined dynamics of larval predation by C. albiceps or whether together to determine whether the predation rates dif- larvae of all prey species are equally attacked by this fered among combinations (no-choice). In the second predator. setting, one C. albiceps was confined with ei- Predatory behaviour consists of a sequence of ther one larva each of C. putoria and C. macellaria events starting with encounter, followed by attack and or with one larva each of C. megacephala and C. ma- capture, and ending in prey ingestion (Tikkanen et al., cellaria to observe the behaviour of the predator larva 1997). If there is no choice among different preys, the in each combination (two-choice). In the third setting, predator has only to decide whether or not to attack one C. albiceps larva and one larvae each of, C. ma- (Tikkanen et al., 1997). If there is choice, the predator cellaria, C. putoria and C. megacephala were placed has to distinguish between different types of potential together to compare the predation rates (three-choice). prey and to choose one rather than the other (Jackson Forty vials were prepared for each combination and & Van Olphen, 1991, 1992). This sequence of events were placed on a lighted laboratory bench at 25 ◦C. has been documented for C. rufifacies in a laboratory The larvae were observed continuously for 2 h and experiment (Wells & Greenberg, 1992a). the instances of predation on C. macellaria, C. puto- In this study, we have analysed the effects of in- ria and C. megacephala larvae by C. albiceps were terspecific interactions between introduced species of recorded for every 15 min. Predatory behaviour was the genus Chrysomya and the native C. macellaria on considered successful when C. albiceps surrounded the population size of the latter. Such an investiga- and pierced its prey to death. Pierced larvae generally tion should help to establish the extent to which the struggled violently in response to the attack. 151

The number of live and killed larvae of each sidering only the cases in which there was predation, species in each setting, was analysed using χ2 statis- we observed 87.1% of predation on C. macellaria tics to test for the homogeneity of rate of predation. and 12.9% on C. putoria. Thus, C. albiceps preferred For each setting, the rate of predation on each species C. macellaria (χ2 = 15.61; d.f. = 1; P<0.05). was analysed further by considering only those cases In the three-choice experiments, the highest preda- where there was predation. Finally, the rates of preda- tion rate (80%) was again on C. macellaria compared tion on C. macellaria for the combinations in the three to 5.0% on C. putoria, 7.5% on C. megacephala and settings were compared to determine whether preda- 7.5% with no predation (Table 4). These rates differed tion is more likely in a given setting. The χ2 test was significantly (χ2 = 60.30; d.f. = 3; P<0.05). also used in these last two analyses. The Yates correc- Considering only the cases where there was preda- tion for continuity of the χ2 statistics was applied to tion, 86.5% involved C. macellaria,8.1%involved all comparisons (Zar, 1996). C. megacephala and 5.4% involved C. putoria.Again, the preference of C. albiceps for C. macellaria was ev- ident (χ2 = 43.95; d.f. = 2; P<0.05). There were Results no significant differences among the predation rates on C. macellaria in the four combinations (χ2 = 3.66; Tables 1–4 show the predation rate relative to the to- d.f. = 3; P>0.05), indicating that the predation tal number of vials (%), the cumulative predation rate rate of C. albiceps on C. macellaria was the same in (%), and the predation rate relative to the number of both no-choice and choice situations. vials available (%) for consecutive time intervals, in the various combinations. Most attacks by C. albiceps on C. macellaria, C. megacephala and C. putoria oc- Discussion curred within the first hour of observation with the highest predation rate on C. macellaria larvae. For the The larval predatory behaviour of C. albiceps was no-choice situation the highest predation rate by C. al- similar to that observed in C. rufifacies (Wells & biceps (77.5%), occurred on C. macellaria, compared Greenberg, 1992a; Wells & Kurahashi, 1997), and to 67.5% on C. putoria and 57.5% on C. megacephala. always seemed to occur in the initial moments of However, the predation rates were statistically ho- contact between the predator and prey larvae. Larval mogeneous (χ2 = 2.82; d.f. = 3; P>0.05), predation by C. albiceps has been reported by sev- indicating that predation rates by C. albiceps were eral authors (Coe, 1978; Gagné, 1981; Erzinçlioglu the same for the three species when no-choice was & Whitcombe, 1983). Nevertheless, this is the first allowed (Table 1). study to quantify and compare the predatory behav- In the two-choice experiments where C. albiceps iour of C. albiceps on native and introduced blowfly was confined with C. macellaria and C. megacephala species. In the no-choice situation, there was no signif- or with C. macellaria and C. putoria, the highest pre- icant difference in the number of larvae of each species dation rate again occurred on C. macellaria (Tables 2 killed by C. albiceps, indicating that in the absence and 3). In the first situation 60% of C. macellaria lar- of choice C. albiceps larvae attack any species. On vae were killed compared to 15% of C. megacephala the other hand, a conspicuous preference of C. albi- larvae (Table 2). There was no predation in 25% of ceps larvae for C. macellaria larvae was observed in the vials. These three rates were significantly different the two and three-choice experiments indicating that (χ2 = 11.86; d.f. = 2; P<0.05). Considering C. albiceps was more dangerous to C. macellaria than only the cases in which there was predation, 80% to other species under our experimental conditions. was on C. macellaria and 20% on C. megacephala. Recently, Wells & Kurahashi (1997) described a study The χ2 test indicated that the difference between the in which C. rufifacies larvae were paired individually predation rates of C. albiceps on C. macellaria and with C. macellaria and C. megacephala larvae in the on the other species was significant (χ2 = 9.63; laboratory. Under these circumstances C. macellaria d.f. = 1; P<0.05). In the second situation 67.5% of larvae were killed at a higher rate than C. megacephala C. macellaria larvae were killed compared to 10.0% larvae. of C. putoria larvae and 22.5% in which there was Preferences for prey types have been attributed to no predation (Table 3). These rates were significantly factors such as sex (Selander, 1966), age (Sandlin & different (χ2 = 19.6; d.f. = 2; P<0.05). Con- Willig, 1993), size (Zerba & Collins, 1992), spatial 152

Table 1. Predation rates by Chrysomya albiceps in a no-choice situation

Time interval Cochliomyia macellaria Chrysomya putoria Chrysomya megacephala (min) PR CR PR2 PR CR PR2 PR CR PR2

15 12.5 12.5 12.5 7.5 7.5 7.5 5.0 5.0 5.0 30 12.5 25.0 14.3 15.0 22.5 16.2 10.0 15.0 10.5 45 22.5 47.5 30.0 12.5 35.0 16.1 15.0 30.0 17.6 60 7.5 55.0 14.3 12.5 47.5 19.2 20.0 50.0 28.6 75 5.0 60.0 11.1 0.0 47.5 0.0 2.5 52.5 5.0 90 5.0 65.0 12.5 5.0 52.5 9.5 5.0 57.5 10.5 105 7.5 72.5 21.4 0.0 52.5 0.0 0.0 57.5 0.0 120 5.0 77.5 18.2 15.0 67.5 31.6 0.0 57.5 0.0

Total 77.5 – – 67.5 – – 57.5 - –

PR = Predation rate for n = 40. CR = Cumulative rate. PR2= Predation rate with respect to the number of vials available in the time interval. Table 2. Predation rates by Chrysomya albiceps in a two-choice situation with C. macellaria and C. megacephala as the choices

Time interval Cochliomyia macellaria Chrysomya megacephala (min) PR CR PR2 PR CR PR2

15 27.5 27.5 27.5 15.0 15.0 15.0 30 10.0 37.5 17.4 0.0 15.0 0.0 45 15.0 52.5 31.6 0.0 15.0 0.0 60 0.0 52.5 0.0 0.0 15.0 0.0 75 5.0 57.5 15.4 0.0 15.0 0.0 90 0.0 57.5 0.0 0.0 15.0 0.0 105 2.5 60.0 10.0 0.0 15.0 0.0 120 0.0 60.0 0.0 0.0 15.0 0.0

Total 60.0 – – 15.0 – –

PR = Predation rate for n = 40. CR = Cumulative rate. PR2= Predation rate with respect to the number of vials available in the time interval. Table 3. Predation rates by Chrysomya albiceps in a two-choice situation with C. macellaria and C. putoria as the choices

Time interval Cochliomyia macellaria Chrysomya putoria (min) PR CR PR2 PR CR PR2

15 15.0 15.0 15.0 0.0 0.0 0.0 30 12.5 27.5 14.7 0.0 0.0 0.0 45 10.0 37.5 13.8 0.0 0.0 0.0 60 15.0 52.5 24.0 2.5 2.5 4.0 75 10.0 62.5 21.1 5.0 7.5 11.1 90 2.5 65.0 6.7 0.0 7.5 0.0 105 0.0 65.0 0.0 2.5 10.0 9.0 120 2.5 67.5 7.1 0.0 10.0 0.0 Total 67.5 – – 10.0 – –

PR = Predation rate for to n = 40. CR = Cumulative rate. PR2= Predation rate with respect to the number of vials available in the time interval. 153

Table 4. Predation rates by Chrysomya albiceps in a three-choice situation

Time interval Cochliomyia macellaria Chrysomya putoria Chrysomya megacephala (min) PR CR PR2 PR CR PR2 PR CR PR2

15 40.0 40.0 40.0 2.5 2.5 2.5 5.0 5.0 5.0 30 27.5 67.5 52.4 2.5 5.0 4.8 2.5 7.5 4.8 45 7.5 75.0 37.5 0.0 5.0 0.0 0.0 7.5 0.0 60 0.0 75.0 0.0 0.0 5.0 0.0 0.0 7.5 0.0 75 5.0 80.0 40.0 0.0 5.0 0.0 0.0 7.5 0.0 90 0.0 80.0 0.0 0.0 5.0 0.0 0.0 7.5 0.0 105 0.0 80.0 0.0 0.0 5.0 0.0 0.0 7.5 0.0 120 0.0 80.0 0.0 0.0 5.0 0.0 0.0 7.5 0.0

Total 80.0 – – 5.0 – – 7.5 – –

PR = Predation rate for n = 40. CR = Cumulative rate. PR2= Predation rate with respect to the number of vials available in the time interval. location (Murdoch et al., 1975) and chance encounters Ullyett (1950) studied the predatory behaviour of (Sherratt & Macdougall, 1995). Microhabitat overlap C. albiceps in mixed cultures of Chrysomya albi- between predator and prey may determine encounter ceps, Lucilia sericata and Chrysomya chlorophyga rates in the field, but this may not translate automat- which were used to estimate mortality rates as an out- ically into prey preferences (Tikkanen et al., 1997). come of interspecific competition. Lucilia sericata and Prey with efficient antipredatory behaviour can risk C. chloropyga were eliminated when bred with C. al- encounters with predators, whereas prey with less biceps at densities higher than 2000 and 10 000 larvae efficient escape mechanisms may have to select micro- per 140 g of meat, respectively (Ullyett, 1950). This habitats to avoid the predator (Tikkanen et al., 1997). elimination was clearly not the effect of simple com- We do not know why C. albiceps prefers C. ma- petition for food, since the total population mass at cellaria. However, a casual observation by Wells & any point was not enough to produce this mortality. Kurahashi (1997) suggests that C. megacephala strug- Predation by C. albiceps larvae was the only plausi- gles more vigorously and flees more quickly following ble explanation (Ullyett, 1950). This conclusion was contact with the mouthparts of C. rufifacies. We ob- supported by results obtained with mixed cultures of served similar behaviour in our experiments since L. sericata and C. chloropyga in the absence of C. al- C. megacephala and C. putoria were apparently more biceps, for which the mortality rate of L. sericata was successful in evading predation than C. macellaria lower (Ullyett, 1950). during contact with C. albiceps. Although we do not know the extent of predation The flexibility of C. albiceps in choosing larvae by C. albiceps in a carrion colonised below carry- suggests that the predatory behaviour of this species ing capacity we suspect that predation begins when can change as a function of prey availability. In natural resources become scarce. The degree to which C. ma- settings, the coexistence of different blowfly species cellaria is controlled by C. albiceps will depend, in the same substrate is not uncommon (Kneidel, among other things, upon the relative densities of each 1984a,b; Hanski, 1987; Wells & Greenberg, 1994) species and upon the total initial density of the mixed and such a situation would provide C. albiceps larvae population per unit of consumable food. We believe with a choice of prey. Our results strongly indicate that experiments designated to investigate this ques- that given a choice, C. albiceps will prey preferentially tion must be performed and currently we are pursuing upon C. macellaria larvae. Since in Brazil Chrysomya this line of investigation in laboratory tests, which con- species and C. macellaria coexist in the same carrion sist of an analysis of the effect of larval competition for throughout most of the year (Linhares, 1981; Mendes food on C. albiceps and other introduced and native & Linhares, 1993) the population demise of C. macel- species. laria is attributable, at least in part, to predation by C. albiceps. 154

Acknowledgements Gagné, R. J., R. R. Gerrish & R. D. Richard, 1982. Correspondence. Entomological Society of America Newsletter 5: 9. We thank two anonymous reviewers and Dr. Sergio F. Goodbrod, J. R. & M. L. Goff, 1990. Effects of larval popula- tion density on rates of development and interactions between dos Reis (Department of Parasitology, IB, UNICAMP, two species of Chrysomya (Diptera: Calliphoridae) in laboratory Brazil) for useful comments and suggestions which culture. Journal of Medical Entomology 27: 338–343. improved the clarity and content of the manuscript. Greenberg, B. & M. L. Szyska, 1984. Immature stages and biology of fifteen species of Peruvian Calliphoridae (Diptera). Annals of The authors also thank Dr. Stephen Hyslop (Depart- the Entomological Society of America 77: 488–517. ment of Pharmacology, UNICAMP) for reviewing the Guimarães, J. H., 1984. Considerações gerais sobre moscas do English of the manuscript. L.D.B.F, L. O. and W. A. gênero Chrysomya no Brasil. Agroquímica 24: 8–12. C. G. were supported by fellowships from FAPESP Guimarães, J. H. , A. P. Prado & A. X. Linhares, 1978. Three newly introduced blowfly species in southern Brazil (Diptera: (97/01441-6), PET-CAPES and CNPq respectively. Calliphoridae). Revista Brasileira de Entomologia 22: 53–60. This research was supported by grants from FAPESP Guimarães, J. H., A. P. Prado & G. M. Buralli, 1979. Dispersal (95/9299-9). and distribution of three newly introduced species of Chrysomya Robineau-Desvoidy in Brazil (Diptera, Calliphoridae). Revista Brasileira de Entomologia, 23: 245–255. Hanski, I., 1977. Biogeography and ecology of carrion flies in the References Canary Islands. Annales Entomologici Fennici 43: 101–107. Hanski, I., 1987. Carrion fly community dynamics: patchiness, sea- Andow, D. A., P. M. Kareiva, S. A. Levin & A. Okubo, 1993. sonality and coexistence. Ecological Entomology 12: 257–266. Spread of invading organisms: patterns of spread. In: K. C. Kim Hengeveld, R., 1989. Dynamics of biological invasions. Chapman and B. A. Mcpheron, eds. Evolution of pests. Patterns of and Hall. New York. variation. John Wiley, New York, pp. 219–242. Ives, A. R., 1988. Aggregation and the coexistence of competitors. Atkinson, W. D. & B. Shorrocks, 1981. Competition on a divided Annales Zoologici Fennici 25: 75–88. and ephemeral resource: a simulation model. Journal of Jackson, R. R. & A. Van Olphen, 1991. Prey-capture techniques Ecology 50: 461–471. and prey preferences of Corythalia canosa and Pystira orbicu- Atkinson, W. D. & B. Shorrocks, 1984. Aggregation of larval lata, ant-eating jumping spiders (Araneae, Salticidae). Journal of Diptera over discrete and ephemeral breeding sites: the impli- Zoology 240: 551–562. cations for coexistence. American Naturalist 124: 336–351. Jackson, R. R. & A. Van Olphen, 1992. Prey-capture techniques and Baumgartner, D. L. & B. Greenberg, 1984. The genus Chrysomya prey preferences of Chrysilla, Natta and Siler, ant-eating jump- (Diptera: Calliphoridae) in the New World. Journal of Medical ing spiders (Araneae, Salticidae) from Kenya and Sri Lanka. Entomology 21: 105–113. Journal of Zoology 227: 163–170. Beaver, R. A., 1977. Non-equilibrium ‘island’ communities: Kneidel, K. A., 1984a. Competition and disturbance in communities Diptera breeding in dead snails. Journal of Animal Ecology 46: of carrion breeding diptera. Journal of Animal Ecology 53: 849– 783–798. 865. Braack, L. E. O., 1986. associated with carcasses in the Kneidel, K. A. 1984b. The influence of carcass taxon and size on northern Kruger National Park. South African Journal of Wildlife species composition of carrion-breeding Diptera. The American Research 16: 91–98. Midland Naturalist 111: 57–63. Coe, R. L., 1978. The decomposition of elephant carcasses in the Kuusela, S. & I. Hanski, 1982. The structure of carrion fly com- Tsavo (East) National Park, Kenya. Journal of Arid Environ- munities: the size and the type of carrion. Holarctic Ecology 5: ments 1: 71–86. 337–348. Denno, R. F. & W. R. Cothran, 1975. Niche relationships of a guild Laurence, B. R., 1986. Old World blowflies in the New World. of necrophagous flies. Annals of the Entomological Society of Parasitology Today 2: 77–79. America 68: 741–754. Levot, G. W., K. R. Brown & K. R. Shipp, 1979. Larval growth of Erzinçlioglu, Y. Z., 1987. The larvae of some blowflies of medical some calliphorid and sarcophagid Diptera. Bulletin of Entomo- and veterinary importance. Medical and Veterinary Entomology logical Research 69: 469–475. 1: 121–125. Linhares, A. X. 1981. Synanthropy of Calliphoridae and Sar- Erzinçlioglu, Y. Z., 1990. The larvae of two closely-related blowfly cophagidae (Diptera) in the city of Campinas, São Paulo, Brazil. species of the genus Chrysomya (Diptera, Calliphoridae). Ento- Revista Brasileira de Entomologia 3: 189–215. mologica Fennica 3: 151–153. Mendes, J. & A. X. Linhares, 1993. Atratividade por iscas e estágios Erzinçlioglu, Y. Z. & R. P. Whitcombe, 1983. Chrysomya albiceps de desenvolvimento ovariano em várias espécies sinantrópicas de (Wiedemann) (Dipt., Calliphoridae) in dung and causing Calliphoridae (Diptera). Revista Brasileira de Entomologia 37: in . Entomologist’s Monthly Magazine 119: 51–52. 157–166. Ferreira, M. J. M., 1983. Sinantropia de Calliphoridae (Diptera) em Murdoch, W. W., S. Avery & M. E. B. Smyth, 1975. Switching in Goiânia, Goiás. Revista Brasileira de Biologia 43: 199–210. predatory fish. Ecology 56: 1094–1105. Fuller, M. E., 1934. The insect inhabitants of carrion, a study in ani- Prado, A. P. & J. H. Guimarães, 1982. Estado atual de disper- mal ecology. Bulletin of the Council for Scientific and Industrial são e distribuição do gênero Chrysomya Robineau-Desvoidy na Research, Melbourne 82: 5–62. região Neotropical (Diptera, Calliphoridae). Revista Brasileira Gagné, R. J., 1981. Chrysomya spp., Old World blowflies (Diptera, de Entomologia 26: 225–231. Calliphoridae), recently established in the Americas. Bulletin of Peschke, K., D. Krapf & D. Fuldner, 1987. Ecological separation, the Entomological Society of America 27: 21–22. functional relationships, and limiting resources in a carrion insect 155

community. Zoologische Jahrbacher Abteilung fur Systematik, Wells, J. D., 1991. Chrysomya megacephala (Diptera: Calliphori- Oekologie und Geographie der Tiere 114: 241–265. dae) has reached the continental United States: review of its Prins, A. J. 1982. Morphological and biological notes on six African biology, pest status, and spread around the world. Journal of blow-flies (Diptera, Calliphoridae) and their immature stages. Medical Entomology 28: 471–473. Annals of the South African Museum 90: 201–217. Wells, J. D. & B. Greenberg, 1992a. Rates of predation by Putman, R. J., 1983. Carrion and dung: the decomposition of animal Chrysomya rufifacies (Macquart) on Cochliomyia macellaria wastes. Studies in Biology, Series, Vol. 156, Institute of Biology, (Fabr.) (Diptera: Calliphoridae) in the laboratory: effect of London. predator and prey development. Pan-Pacific Entomologist 68: Sandlin, E. A. & M. R. Willig, 1993. Effects of age, sex, prior ex- 12–14. perience, and intraspecific food variation on diet composition of Wells, J. D. & B. Greenberg, 1992b. Laboratory interaction between a tropical folivore (Phasmatodea, Phasmatidae). Environmental introduced Chrysomya rufifacies and native Cochliomyia macel- Entomology 22: 625–633. laria (Diptera: Calliphoridae). Environmental Entomology 21: Selander, R. K. 1966. Sexual dimorphism and differential niche 640–645. utilization in birds. Condor 68: 113–151. Wells, J. D. & B. Greenberg, 1992c. Interaction between Chrysomya Sherratt, T. N. & A. D. Macdougall, 1995. Some population con- rufifacies and Cochliomyia macellaria (Diptera: Calliphoridae): sequences of variation in preference among individual predators. the possible consequences of an invasion. Bulletin of Entomo- Biological Journal of the Linnean Society 55: 93–107. logical Research 82: 133–137. Simberloff, D. 1991. Keystone species and community effects of Wells, J. D. & B. Greenberg, 1994. Resource use by an introduced biological introductions. In: L. R. Ginzburg (ed.), Assessing and native carrion flies. Oecologia 99: 181–187. the Ecological Risks of Biotechnology. Butterworth-Heinemann, Wells, J. D. & H. Kurahashi, 1997. Chrysomya megacephala (Fabr.) Boston, pp. 1–19. is more resistant to attack by Chrysomya rufifacies (Macquart) in Tantawi, T. I. & B. Greenberg, 1993. Chrysomya albiceps and laboratory arena than is Cochliomyia macellaria (Fabr.) (Diptera: C. rufifacies (Diptera: Calliphoridae): contribution to an on- Calliphoridae). Pan-Pacific Entomologist 73: 16–20. going taxonomic problem. Journal of Medical Entomology 30: Zar, J. H., 1996. Biostatistical Analysis, 3nd Edition. Prentice Hall, 646–648. New Jersey. Tikkanen, P., T. Muotka, A. Huhta & A. Juntenen, 1997. The roles Zerba, K. E. & J. P. Collins, 1992. Spatial heterogeneity and indi- of active predator choice and prey vulnerability in determining vidual variation in the diet of an aquatic top predator. Ecology the diet of predatory stonefly (Plecoptera) nymphs. Journal of 73: 268–279. Animal Ecology 66: 36–48. Ullyett, G. C., 1950. Competition for food and allied phenomena in -blowfly populations. Philosophical Transactions of the Royal Society of London B234: 77–174.