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Chrysomya albiceps is a facultative predator and cannibal species during the ... the influence of prey size and larval density on cannibalism by third-instar.
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C 2004) Journal of Insect Behavior, Vol. 17, No. 2, March 2004 (°

Cannibalistic Behavior and Functional Response in Chrysomya albiceps (Diptera: Calliphoridae) Lucas Del Bianco Faria,1 Luzia Aparecida Trinca,2 and Wesley Augusto Conde Godoy1,3 Accepted November 19, 2003; revised January 5, 2004

Chrysomya albiceps is a facultative predator and cannibal species during the larval stage. Very little is known about cannibalism and prey size preference, especially in blowflies. The purpose of this investigation was to determine the influence of prey size and larval density on cannibalism by third-instar larvae of C. albiceps under laboratory conditions. Our results indicate that no cannibalism occurs by third-instar larvae on first- and second-instar larvae, but third-instar larvae do eat second-instar larvae. The functional response on second-instar larvae is consistent with Holling type II. The consequences of consuming second-, compared to first- or third-, instar larvae as well as the implications of cannibalism for the population dynamics of C. albiceps are discussed. KEY WORDS: cannibalism; prey development stage; foraging theory; functional response; Chrysomya albiceps; Calliphoridae.

INTRODUCTION Cannibalism has sometimes been regarded as an abnormal behavior, rare and of little evolutionary or ecological interest (Elgar and Crespi, 1992), 1Departamento

de Parasitologia, IB, Universidade Estadual Paulista, Rubiao ˜ Jr., Botucatu 18618-000, SP, Brazil. 2Departamento de Bioestat´ıstica, IB, Universidade Estadual Paulista, Rubiao ˜ Jr., Botucatu 18618-000, SP, Brazil. 3To whom correspondence should be addressed. Fax: +55-14-38153744. e-mail: wgodoy@ ibb.unesp.br. 251 C 2004 Plenum Publishing Corporation 0892-7553/04/0300-0251/0 °

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receiving little attention until recently (Polis, 1981). Many authors have observed and classified some factors influenced by cannibalism (Fox, 1975; Polis, 1981; Elgar and Crepsi, 1992), such as prey vulnerability (Polis, 1981; Elgar and Crespi, 1992), size (O’Brien et al., 1976; Polis, 1981; Folkvord and Hunter, 1986; Bailey and Polis, 1987), developmental stage (Polis, 1981, Hausfater and Hrdy, 1984; Polis, 1984; Elgar and Crespi, 1992), hunger (Fox, 1975; Polis, 1981), density (Fox, 1975; Hunter and Kimbrell, 1980; Polis, 1981; Crowley et al., 1987; Orr et al., 1990), quantity and quality of food (Fox, 1975; Polis, 1981; Giray et al., 2001), and pheromones (Schausberger and Croft, 1999). Cannibalism may also influence the population dynamics (Dong and Polis, 1992) interfering with population stability (Polis, 1981; Hastings and Costantino, 1987; Orr et al., 1990). Cannibalism has been shown to be able to alter the competitive relationship, decreasing the numbers of competitors and increasing the food quantity (Fox, 1975; Johansson, 1992; Fincke, 1994). Cannibalism has also been considered beneficial in terms of nutrients, especially in situations where food sources are scarce (Ho and Dawson, 1966; Fox, 1975; Sonleitner and Guthrie, 1991; Spence and Carcamo, 1991; Agarwala and Dixon, 1992; Tschinkel, 1993). Tribolium species are considered a classic and very important system, which has been useful to understand the biology of cannibalism in insects and its influence on population dynamics (Hastings, 1987; Hastings and Costantino, 1987; Stevens, 1992; Dennis et al., 1995). There is evidence showing a strong association between cannibalism and chaotic cycles in Tribolium populations (Constantino et al., 1995 and 1997). The Old World blowflies of the genus Chrysomya Robineau-Desvoidy have been introduced to the Americas in the mid-1970s (Guimaraes ˜ et al., 1978, 1979; Baumgartner and Greemberg, 1984; Laurence, 1986). These species transmit pathogenic organisms and can cause myiasis on man and other animals, making them important in medical and veterinary entomology (Zumpt, 1965; Guimaraes ˜ et al., 1978; Baumgartner and Greenberg, 1984; Lawson and Gemmell, 1990; Wells, 1991). After introduction, Chrysomya albiceps, Chrysomya rufifacies, Chrysomya megacephala, and Chrysomya putoria quickly became widespread and abundant in North and South America (Guimaraes ˜ et al., 1978 and 1979; Prado and Guimaraes, ˜ 1982; Baumgartner and Greenberg, 1984). The introduction of Chrysomya species has influenced the native fauna, for example, by displacing species as Cochliomyia macellaria (Guimaraes ˜ et al., 1979; Prado and Guimaraes, ˜ 1982; Baumgartner and Greenberg, 1984). Chrysomya and Cochliomyia macellaria are among the main consumers of carrion, a food resource for a wide variety of species (Putman, 1983; Braack, 1986). Carrion is ephemeral and flies that feed upon it rarely complete more than one generation on a single item (Kneidel, 1984a,b; Ives, 1988).

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Chrysomya albiceps and C. rufifacies are facultative predators during the larval stage, causing substantial mortality to third-instar larvae of Cochliomyia macellaria (Wells and Kurahashi, 1997; Faria et al., 1999). Besides being a predator, C. albiceps also acts as a cannibal through the larval stage (Ullyett, 1950). Queiroz et al. (1997) observed that first-instar larvae do not have developed mouthparts to kill prey. In addition, preliminary studies have demonstrated that second-instar larvae do not cannibalize others. These results differ from results obtained in experiments with Chrysomya rufifacies, which exhibit cannibalism by second-instar larvae (Goodbrod and Goff, 1990). Although the extent of cannibalism and predation by C. albiceps at low density is unknown and probably reduced, these interactions are frequent during times of food scarcity (Faria et al., 1999). Probably, predation occurs before cannibalism in C. albiceps, since prey larvae of other species are apparently easier to catch than cospecifics (Faria, 2001). In addition, Hironori and Katsuhiro (1997) observed that prey density is a key factor influencing the balance between predation and cannibalism. Although some information on searching, pursuing, capturing, and eating (Wells and Greenberg, 1992; Wells and Kurahashi, 1997; Faria et al., 1999; Faria and Godoy, 2001) is available for blowflies, very little is known about cannibalism and prey size preference by C. albiceps. The purpose of this investigation was to determine the influence of prey size on cannibalism under laboratory conditions. We studied the cannibalism by third-instar larvae of C. albiceps on first-, second-, and third-instar larvae in no-choice experiments with different combinations in order to compare the vulnerability of different larval instars to cannibalism.

MATERIALS AND METHODS Laboratory populations of C. albiceps were founded from specimens collected on the Campus of Universidade Estadual Paulista, Botucatu, Sao ˜ Paulo, Brazil. Adult flies were maintained at 25 ± 1◦ C in cages (30 × 30 × 30 cm) covered with nylon and fed water and sugar ad libitum. Eggs were obtained by providing females with fresh beef liver. Hatched larvae were reared on an excess of ground beef until the third instar for C. albiceps (predator), and until the first, second, and third instar for C. albiceps (prey), when they were placed on petri dishes (12-mm height × 30-mm diameter) to estimate cannibalism rates in different combinations. Larval instars were determined using accepted morphological characters used to separate the various development stages of blowflies (Smith, 1986; Queiroz et al., 1997).

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Experiment 1 Cannibalism rates were evaluated in three no-choice settings, with the predator larvae always being third instar. First-, second-, and third-instar lavae were the prey confined with third-instar larvae, the predators. The combinations were set up as follows. 1. One first-instar larva (prey) × one third-instar larva (predator) 2. One second-instar larva (prey) × one third-instar larva (predator) 3. One third-instar larva (prey) × one third-instar larva (predator) Forty petri dishes were prepared for each combination and placed on a continuous light laboratory bench at 25 ± 1◦ C and 70% relative humidity. The larvae were observed continuously for 3 h and the instances of cannibalism on first-, second-, and third-instar larvae were recorded every 30 min. Cannibalistic behavior was considered successful when the predator surrounded and mortally pierced its prey, with the pierced larva struggling violently in response. The number of killed and not killed larvae of each instar and setting was analyzed statistically using the two-sided Fisher’s exact test (SAS Institute, 1989). Experiment 2 The cannibalism rate in the presence of different prey densities (functional response) was determined using second-instar larvae as prey and thirdinstar larvae as predators, since in experiment 1 cannibalistic behavior was observed only in this combination. The prey densities used were 2, 6, 10, 12, 14, 16, 18, 20, 22, and 24, with one predator for each density. Twenty petri dishes (12 × 30 mm) were prepared for each density. The assays were done on 2 days, with 10 petri dishes for each combination. The petri dishes were placed on a continuous light laboratory bench at 25 ± 1◦ C and 70% relative humidity. The larvae were observed for 5 h and all cannibalism was recorded. Analysis was performed by fitting the data to a nonlinear regression (least squares and Marquardt method). Statistical analyses were performed using the PROC NLIN-SAS statistical package (SAS Institute, 1989). The Holling disc equation (1959) for type II response was fitted to describe the pattern of the data as a function of increasing densities. The disc equation may be written Nc =

a NT (1 + a NTh )

where Nc is the number of killed prey; N, the number of offered prey; T, the total time available for the predator; a, the attack rate; and Th , the handling

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Table I. Frequency of Killed/Alive Larvae After Being Maintained in a Petri Dish with a Third-Instar Larvae for 180 min (n = 40 for Each Instar)

Killed Alive

1st instar

2nd instar

3rd instar

0 40

5 35

0 40

time. The attack rate (a) and the handling time (Th ) were estimated from the nonlinear regression. RESULTS Experiment 1 Table I shows the cannibalism in the different treatments. No cannibalism occured on first- or third-instar prey during the 180-min assay period. The cannibalism rate on second-instar prey was 12.5%, with attacks only occurring after 150 min. The proportion of killed larvae was significantly different among prey instars (χ 2 log-likelihood = 11.428, d f = 2, P = 0.010). Experiment 2 The functional response obtained from the second-instar larvae may be considered similar to functional response type II (r 2 = 0.45; regression mean square = 3.3341.0552, d f = 2; residual mean square = 3.9237, d f = 198) (Fig. 1). The estimate of attack rate is a = 0.1234 (SE = 0.0168; P < 0.0001).

Fig. 1. Type II functional response of third-instar larvae of C. albiceps on second-instar larvae of C. albiceps. r 2 = 0.45; regression mean square = 3341.0552, d f = 2; residual mean square = 3.9237, d f = 198. Average of 20 replicates for each combination ± SE.

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The handling time was estimated to be Th = 0.3068 (SE = 0.0623; P < 0.0001).

DISCUSSION Chrysomya albiceps displayed low rate of cannibalism (12.5%) compared with predation rates on Chrysomya megacephala (100%) and Cochliomyia macellaria (92.5%) in a similar experiment, focusing on interspecific predation. The first cannibalism act was detected after 150 min, significantly contrasting with the first interspecific predation act of C. megacephala and C. macellaria, which was observed before the first 30 min (Faria, 2001). Goodbrod and Goff (1990) observing the cannibalism of Chrysomya rufifacies recorded similar behavior where prey of first instar was not killed by third-instar larvae; moreover, there was considerable variation in the mortality rates along the several densities, with the highest density showing a bigger larval mortality. We observed in this study that C. albiceps cannibalizes only in the absence of food such as carcasses or other prey species such as C. megacephala, C. macellaria, and C. putoria (Faria et al., 1999; Faria and Godoy, 2001). Hunger, a primary factor inducing cannibalism (Fox, 1975; Polis, 1981), affects behavior and vulnerability or voracity in many ways, thus promoting cannibalism on several time scales. Over a short period of time, food stress generally increases foraging activity and movement (Hassell, 1978; Polis, 1981), increasing the chance of encounter between predator and prey (Sherrat and McDougall, 1995) and of acts of cannibalism. Cannibalism is a major cause of mortality in many species. A dense age class of older conspecifics may eat nearly 100% of the eggs or young produced by the population (Polis, 1981). The elimination of entire cohorts often causes violent fluctuations in recruitment and skewed age and size distributions in insect populations (Polis, 1981; Constantino et al., 1995, 1997; Dennis et al., 1995) and over 100 studies have shown that the rate of cannibalism increases with density (Fox, 1975; Polis, 1981). When prey and predator are easily distinguished, these interactions can be described by the classic predator– prey theory, especially if cannibalism primarily occurs among members of different age classes or cohorts. Thus, mortality may be described in terms of functional response of the predator to the density of conspecific prey (Dong and Polis, 1992). In terms of prey consumption and functional response, the third-instar predators demonstrated the greatest voracity against second-instar larvae. The rates of cannibalism increased as a function of density, although the proportion of prey killed decreased. This decrease is characteristic of the type II

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functional response, where the acceleration is negative during consumption of prey present at increasing densities (Holling, 1959, 1965; Gotelli, 1995; Case, 2000). Hence, prey at lower densities have a greater chance than prey at higher densities to be killed by the larval predator C. albiceps. Until recently, functional response was considered to be invariant for specific predator–prey combinations (Murdoch and Oaten, 1975; Hassell, 1978). However, the shape of the functional response may vary according to environmental conditions (Abrams, 1982), such as habitat heterogeneity (Hildrew and Townsend, 1977; Kaiser, 1983; Lipcius and Hines, 1986) and refuge for preys (Lipcius and Hines, 1986). The distinction between kinds of curve (types I, II, and III [sensu Holling]) may be important to population stability, but in temporary habitats such as carcasses, an equilibrium is never attained. Hence, the number of prey killed may be the most important factor in prey population dynamics rather than the shape of the curve (Blaustein and Dumont, 1990). There are three major factors influencing cannibalism rates. Prey vulnerability (an individual feature), density (a population property), and quantity and quality of food items (environmental conditions) (Elgar and Polis, 1992). Several individual features such as size (O’Brien et al., 1976; Polis, 1981; Folkvord and Hunter, 1986; Bailey and Polis, 1987), developmental stage (Polis, 1981; Hausfater and Hrdy, 1984; Polis, 1984; Elgar and Crespi, 1992), hunger (Fox, 1975; Polis, 1981), and pheromones (Schauberger and Croft, 1999) may determine the frequency and intensity of cannibalism. These factors must be explicit in studies about population consequences of cannibalism, and specifically, foraging theory facilitates this approach (Schoener, 1987) and also provides a particularly appropriate way to analyse cannibalism (Polis, 1981). The foraging biology of individuals directly affects population dynamics because it links characteristics of food resources to survival and reproduction of individuals. Hence, cannibalism can be viewed as a series of foraging decisions by both the predator and the prey (Elgar and Crespi, 1992). According to optimal foraging theory, predators are expected to utilize large prey as an effort to maximize energy return (Schoener, 1969). On the other hand, consuming smaller prey may be an advantage if large prey are costly in terms of injury risks or if prey are capable of later competing for limited food. Hence, even if the costs associated with the utilization of small or large prey are different, they could result in a lower net energy gain than intermediate-sized prey (Roger et al., 2000). In addition, Polis (1981) pointed out that when the predator and prey are of the same size or development stage, the predator may change to prey and the prey to predator. Elner and Hughes (1978), studying predatory crabs attacking shellfish, observed that they prefer to eat intermediate-sized prey, and the same

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behavior was observed by Roger et al. (2000), who showed that predatory coccinellids prefer to attack lepidopterous larvae of intermediate size. These authors graphically expressed this kind of behavior with a convex curve, where the highest peak of predation involves the intermediate size compared to a small or large size, but the shape of the curve varies according to prey or predator species and predator or prey size. In our study, first-instar prey were smaller than the predator and harder to detect. This benefit might be understood as a kind of refuge (Schuman and Sullivan, 2000). On the other hand, third-instar prey were similar in size to the predators, so that attack became a more difficult act. They were the easiest to detect, increasing the chance of an encounter, but probably were also better able to escape from the predator. Thus, prey of intermediate size (second instar) could offer the highest energy gain because they are easier to find than first-instar prey but exhibit a weaker defense response than third-instar larvae. Future studies focusing on larval behavior and energetic gain during interspecific interactions are necessary to evaluate in detail the aspects of foraging theory in blowflies. ACKNOWLEDGMENTS L.D.B.F. was supported by fellowships from Coordena¸cao ˜ de Aperfei¸coamento de Pessoal de Nivel Superior (Programa de Pos-Gradua¸ ´ cao ˜ em Ciencias ˆ Biologicas, ´ AC: Zoologia, Universidade Estadual Paulista, Botucatu, SP). This research was supported by grants from FAPESP (01/11235-1). REFERENCES Abrams, P. (1982). Functional responses of optimal foragers. Am. Nat. 120: 382–390. Agarwala, B. K., and Dixon, A. F. G. (1992). Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol. Entomol. 17: 303–309. Bailey, K. H., and Polis, G. A. (1987). An experimental analysis of optimal and central place foraging by the harvester ant, Pogonomyrmex californicus. Oecologia 72: 440–448. Baumgartner, D. L., and Greenberg, B. (1984). The genus Chrysomya (Diptera: Calliphoridae) in the New World. J. Med. Entomol. 21: 105–113. Blaustein, L., and Dumont, H. J. (1990). Typhloplanid flatworms (Mesostoma and related genera): Mechanisms of predation and evidence that they structure aquatic invertebrate communities. Hydrobiologia 198: 61–77. Braack, L. E. O. (1986). Arthropods associated with carcasses in the northern Kruger National Park. S. Afr. J. Wild. Res. 16: 91–98. Case, T. J. (2000). An Illustraded Guide of Theoretical Ecology. Oxford University Press, New York. Costantino, R. F., Cushing, J. M., Dennis, B., and Desharnais, R. A. (1995). Experimentally induced transitions in the dynamic behaviour of insect populations. Nature 375: 227–230.

P1: JQX Journal of Insect Behavior [joib]

pp1243-joir-487696

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10:24

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Style file version Feb 08, 2000

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Costantino, R. F., Deshamais, R. A., Cushing, J. M., and Dennis, B. (1997). Chaotic dynamics in an insect population. Science 275: 389–391. Crowley, P., Nisbet, R., Gurney, W., and Lawton, J. (1987). Population regulation in animals with complex life histories: Formulation and analysis of a damself model. Adv. Ecol. Res. 17: 1–59. Dennis, B., Desharnais, R. A., Cushing, J. M., and Costantino, R. F. (1995). Nonlinear demographic dynamics: Mathematical models, statistical methods and biological experiments. Ecol. Monog. 65: 261–281. Dong, Q., and Polis, G. A. (1992). The dynamics of cannibalistic populations: A foraging perspective. In Elgar, M. A., and Crespi, B. J. (eds.), Cannibalism, Ecology and Evolution Among Diverse Taxas, Oxford Science, Oxford, pp. 13–38. Elgar, M. A., and Crespi, B. J. (1992). Ecology and evolution of cannibalism. In Elgar, M. A., and Crespi, B. J. (eds.), Cannibalism, Ecology and Evolution Among Diverse Taxas, Oxford Science, Oxford, pp. 1–13. Elner, R. W., and Hughes, R. N. (1978). Energy maximization in the diet of the shore crab, Carcinus maenas. J. Anim. Ecol. 47: 103–116. ˜ experimentais de Faria, L. D. B. (2001). Predac¸a˜ o larval e resposta funcional em populac¸oes Chrysomya albiceps (Diptera: Calliphoridae). Disserta¸cao ˜ de Mestrado, UNESP, Botucatu, SP, Brazil. Faria, L. D. B., and Godoy, W. A. C. (2001). Prey choice by facultative predator larvae of Chrysomya albiceps (Diptera: Calliphoridae). Mem. Inst. Oswaldo Cruz 96: 875–878. Faria, L. D. B., Orsi, L., Trinca, L. A., and Godoy, W. A. C. (1999). Larval predation by Chrysomya albiceps on Cochliomyia macellaria, Chrysomya megacephala and Chrysomya putoria. Entomol. Exp. Appl. 90: 149–155. Fincke, O. M. (1994). Population regulation of a tropical damselfly in the larval stage by food limitation, cannibalism intraguild predation and habitat drying. Oecologia 100: 118–127. Folkvord, A., and Hunter, J. R. (1986). Size-specific vulnerability of northern anchovy, Engraulis mordax, larvae to predation by fishes. Fish. Bull. (U.S.) 84: 859–869. Fox, L. R. (1975). Cannibalism in natural populations. Annu. Rev. Ecol. Syst. 6: 87–106. Giray, T., Luyten, Y., MacPherson, M., and Stevens, L. (2001). Physiological bases of cannibalism and its evolution in the four beetje Tribolium confusum. Evolution 55: 797–806. Goodbrod, J. R., and Goff, M. L. (1990). Effects of larval population density on rates of development and interactions between two species of Chrysomya (Diptera: Calliphoridae) in laboratory culture. J. Med. Entomol. 27(3): 338–343. Gotelli, N. J. (1995). A Primer of Ecology, Sinauer Associates, Sunderland, MA. Guimaraes, ˜ J. H., Prado, A. P., and Linhares, A. X. (1978). Three newly introduced blowfly species in southern Brazil (Diptera: Calliphoridae). Rev. Bras. Entomol. 22: 53–60. Guimaraes, ˜ J. H., Prado, A. P., and Buralli, G. M. (1979). Dispersal and distribution of three e newly introduced species of Chrysomya Robineau-Desvoidy in Brazil (Diptera, Calliphoridae). Rev. Bras. Entomol. 23: 245–255. Hassell, M. P. (1978). The Dynamics of Arthropod Predator-Prey Systems, Princeton University Press, Princeton, NJ. Hastings, A. (1987). Cycles in cannibalistic egg-larval interactions. J. Math. Biol. 24: 651–666. Hastings, A., and Costantino, R. F. (1987). Cannibalistic egg-larva interactions in Tribolium: An explanation for the oscillations in population numbers. Am. Nat. 120: 36–52. Hausfater, G., and Hrdy, S. (1984). Infanticide: Comparative and Evolutionary Perspectives, Aldine, New York. Hildrew, A. G., and Townsend, C. R. (1977). The influence of substrate on the functional response of Plectrocnemia conspersa (Curtis) larvae (Trichoptera: Polycentropodidae). Oecologia 31: 21–26. Hironori, Y., and Katsuhiro, S. (1997). Cannibalism and interspecific predation in two predatory ladybird in relation to prey abundance in the field. Entomophaga 42: 153–163. Ho, F. K., and Dawson, P. S. (1966). Egg canibalism by Tribolium larvae. Ecology 47: 318–322. Holling, C. S. (1959). Some caracteristics of simple types of predation and parasitism. Can. Entomol. 91: 385–398.

P1: JQX Journal of Insect Behavior [joib]

260

pp1243-joir-487696

May 11, 2004

10:24

Style file version Feb 08, 2000

Faria, Trinca, and Godoy

Holling, C. S. (1965). The functional response of predators to prey density and its role in mimicry and population regulation. Mem. Entomol. Soc. Can. 45. Hunter, J. R., and Kimbrell, C. A. (1980). Egg cannibalism in the northern anchovy, Engraulis mordax. Fish. Bull. (U.S.) 78: 811–816. Ives, A. R. (1988). Aggregation and the coexistence of competitors. Ann. Zool. Fenn. 25: 75–88. Johansson, G. (1992). Effects of zooplankton availability and foraging mode on cannibalism in three dragonfly larvae. Oecologia 91: 179–183. Kaiser, H. (1983). Small scale spatial heterogeneity influences predation success in an unexpected way: model experiments on the functional response of predatory mites (Acarina). Oecologia 56: 249–256. Kneidel, K. A. (1984a). Competition and disturbance in communities of carrion breeding diptera. J. Anim. Ecol. 53: 849–865. Kneidel, K. A. (1984b). The influence of carcass taxon and size on species composition of carrion-breeding Diptera. Am. Mid. Nat. 111: 57–63. Laurence, B. R. (1986). Old World blowflies in the New World. Parasitol. Today 2: 77–79. Lawson, J. R., and Gemmell, M. A. (1990). Transmission of taeniid tapeworm eggs via blowflies to intermediate hosts. Parasitology 100: 143–146. Lipcius, R. N., and Hines, A. H. (1986). Variable function responses of a marine predator in dissimilar homogeneous microhabitats. Ecology 67: 1361–1371. Murdoch, W. W., and Oaten, A. (1975). Predation and population stability. Adv. Ecol. Res. 9: 2–131. O’Brien, W., Slade., N., and Vinyard, G. (1976). Apparent size as the determinant of prey selection by bluegill sunfish (Lepomis macrochirus). Ecology 57: 1304–1310. Orr, B. K., Murdoch, W. W., and Bence, J. R. (1990). Population regulation, convergence, and cannibalism in Notonecta (Hemiptera). Ecology 71: 68–82. Polis, G. A. (1981). The evolution of dynamics of intraspecific predation. Annu. Rev. Ecol. Syst. 12: 125–251. Polis, G. A. (1984). Age structure component of niche width and intraspecific resource partitioning by predators: Can age groups function as ecological species? Am. Nat. 123: 541–564. Prado, A. P., and Guimaraes, ˜ J. H. (1982). Estado atual de dispersao ˜ e distribui¸cao ˜ do genero ˆ Chrysomya Robineau-Desvoidy na regiao ˜ Neotropical (Diptera: Calliphoridae). Rev. Bras. Entomol. 26: 225–231. Putman, R. J. (1983). Carrion and Dung: The Decomposition of Animal Wastes. Studies in Biology Series, Vol. 156, Institute of Biology, London. Queiroz, M. M. C., Mello, R. P., and Lima, M. M. (1997). Morphological aspects of the larval instars of Chrysomya albiceps (Diptera, Calliphoridae) reare in the laboratory. Mem. Inst. Oswaldo Cruz 92: 187–196. Roger, C., Coderre, D., and Boivin, G. (2000). Differential prey utilization by generalist predator Coleomegilla maculata lengi according to prey size and species. Entomol. Exp. Appl. 94: 3–13. SAS Institute (1989). SAS/STAT User’s Guide, v. 6, 4th ed., SAS Institute, Cary, NC. Schausberger, P., and Croft, A. (1999). Predation on and discrimination between cornn-and heterospecific eggs among specialist and generalist Phytoseiid mites (acari: Phytoseiidae). Environ. Entomol. 28: 523–528. Schoener, T. W. (1969). Models of optimal size for solitary predators. Am. Nat. 103: 277–313. Schoener, T. W. (1987). A brief history of optimal foraging ecology. In Kamil, A. C., Krebs, J. R., and Pulliam, H. R. (eds.), Foraging Behavior, Plenum, New York, pp. 5–67. Sherratt, T. N., and Macdougall, A. D. (1995). Some population consequences of variation in preference among individual predators. Biol. J. Linn. Soc. 55: 93–107. Smith, K. G. V. (1986). A Manual of Forensic Entomology, University Printing House, Oxford. Sonleitner, F. J., and Guthrie, P. J. (1991). Factors affecting oviposition rate in the flour beetle Tribolium castaneum and the origin of the population regulating mechanism. Res. Pop. Ecol. 33: 1–12. Spence, J. R., and Carcamo, H. A. (1991). Effects of cannibalism and intraguild predation on pondskaters (Gerridae). Oikos 62: 333–341.

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Stevens, L. (1992). Cannibalism in beetles. In Elgar, M. A., and Crespi, B. J. (eds.), Cannibalism, Ecology and Evolution Among Diverse Taxa, Oxford Science, Oxford, pp. 156–175. Suchman, C. L., and Sullivan, B. K. (2000). Effect of prey size on vulnerability of copepods to predation by the scyphomedusae Aurelia aurita and Cyanea sp. J. Plank. Res. 22: 2289–2306. Tschinkel, W. R. (1993). Resource allocation, brood production and cannibalism during colony founding in the fire ant, Solenopsis invicta. Behav. Ecol. Soc. 33: 209–233. Ullyett, G. C. (1950). Competition for food and allied phenomena in sheep-blowfly populations. Phil. Trans. Roy. Soc. Lond. B234: 77–174. Wells, J. D. (1991). Chrysomya megacephala (Diptera: Calliphoridae) has reached the continental United States: Review of its biology, pest status, and spread around the world. J. Med. Entomol. 28: 471–473. Wells, J. D., and Greenberg, B. (1992). Rates of predation by Chrysomya rufifacies (Macquart) on Cochliomyia macellaria (Fabr.) (Diptera: Calliphoridae) in the laboratory: Effect of predator and prey development. Pan-Pac. Entomol. 68: 12–14. Wells, J. D., and Kurahashi, H. (1997). Chrysomya megacephala (Fabr.) is more resistant to attack by Chrysiomya rufifacies (Marcquart) in laboratory arena than is Cochliomyia macellaria (Fabr.) (Diptera: Calliphoridae). Pan-Pac. Entomol. 73: 16–20. Zar, J. H. (1999). Biostatistical Analysis, 4th ed., Prentice Hall, Upper Saddle River, NJ. Zumpt, F. (1965). Myiasis in Man and Animals in the Old World, Butterworths, London.