Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 96(6): 875-878, August 2001 875 Prey Choice by Facultative Predator Larvae of albiceps (Diptera: ) Lucas Del Bianco Faria, Wesley Augusto Conde Godoy+

Departamento de Parasitologia, IB, Universidade Estadual Paulista, Rubião Junior, 18618-000 Botucatu, SP, Brasil In this study we investigated predation rates on third larvae of and C. megacephala by third instar larvae of C. albiceps in a two-choice situation. The highest predation rate occurred on C. putoria larvae and this result is compared to previous experiments, in which C. macellaria larvae were present. Our results suggest that, when C. macellaria is absent C. albiceps larvae attack more C. putoria than C. megacephala larvae. Prey choice decisions and its implications for introduced and native blowflies are discussed.

Key words: - prey choice - larval predation - interspecific interaction - Diptera - Calliphoridae

Understanding the patterns and ways in which fore rarely completing more than one generation utilize food resources is fundamental to inside them (Putman 1977, Hanski 1987). the study of any population and commu- The blowfly community is a very complex sys- nity (Gotelli 1995). Foraging efficiency may dif- tem, including probably many simultaneous pro- fer considerably between classes of animals within cesses such as intra and interspecific competition, the population and between individuals within a facultative larval predation and cannibalism class (Brewer 1994). Class differences may be re- (Ullyett 1950, Gagné 1981, Erzinçlioglu & lated to size or age (Marchetti & Price 1989, Whitcombe 1983, Wells & Greenberg 1992a,b,c). Hirvonen & Ranta 1996), but even among indi- All these interactions have a strong impact on the viduals within a class there may be significant dif- diptera community, mainly when severe competi- ferences in rates of energy intake (Ranta & tion takes place (Ullyett 1950, Hanski 1977, Nuutinen 1985, Ehlinger 1989). This might be due Goodbrood & Goff 1990, Wells & Greenberg to individual abilities in utilizing available prey, 1992a,c). but also because individuals utilize different prey Interspecific interactions in blowfly system species or sizes of those available (Holbrook & have been investigated in experiments in which Schmitt 1992). population dynamics and competitive ability of the The most important period of life for some in- invading species C. rufiffacies and C. albiceps, and sects, such as blowflies, is the larval stage because of the native species C. macellaria were analyzed in this phase they acquire food and minimum (Wells & Greenberg 1992a,b,c, 1994, Wells & weight necessary to become pupae and subse- Kurahashi 1997, Faria et al. 1999, Reis et al. 1999, quently adults (Levot et al. 1979). Blowflies feed Von Zuben et al. 2000). These investigations were usually on carcasses and the amount of food avail- attempts to gain a deeper understanding of recent able may influence the population dynamics of blowfly biological invasion in Americas and its many species (Godoy et al. 1993). Carcasses are implications on population dynamics. ephemeral substracts in which many individuals There is some evidence in the Americas that and species are generally present, consuming all the native species C. macellaria has been displaced food resources in a short period of time and there- by Chrysomya species (Guimarães et al. 1978, 1979, Prado & Guimarães 1982). A gradual de- cline of C. macellaria has been observed probably as a consequence of the introduction of Chrysomya species in the New World (Guimarães et al. 1978, 1979, Prado & Guimarães 1982, Baumgartner & Research supported by grants 97-01441-6, from Fapesp. Greenberg 1984). Additionally, we have strong +Corresponding author. Fax: +55-14-821.3744. E-mail: evidences to believe that the principal prey of C. [email protected] albiceps and C. rufifacies during larval stage is C. Received 14 November 2000 macellaria (Wells & Greenberg 1992a, Wells & Accepted 5 April 2001 Kurahashi 1997, Faria et al. 1999). 876 Prey Choice by C. albiceps • LDB Faria, WAC Godoy

In this sense, it would be interesting to investi- for 2 h and instances of predation on C. putoria gate if there are other blowfly species that C. and C. megacephala, were recorded every 15 min. albiceps can attack when C. macellaria is not Predatory behavior was considered successful present. The existence and abundance of alterna- when C. albiceps surrounded and mortally pierced tive prey can be important factors to C. albiceps its prey with the pierced larvae struggling violently population dynamics, mainly in situations where in response. the natural food source is scarce (Ullyett 1950, Polis The number of killed and surviving larvae of 1981, Faria et al. 1999). In this study we extended each species was statistically analyzed using χ2 test choice experiments from Faria et al. (1999) to in- for homogeneity of rates. Then, the rates of preda- vestigate if C. albiceps attacks C. putoria and C. tion on each species were analyzed further by con- megacephala at the same rate when C. macellaria sidering only the predation cases. In all compari- is not present. sons the Yates correction for continuity of the χ2 MATERIALS AND METHODS statistics was used (Zar 1996). Laboratory populations of C. albiceps, C. RESULTS AND DISCUSSION putoria and C. megacephala were taken from speci- The highest predation rate by C. albiceps lar- mens collected from the Campus of the vae (72.5%) occurred on C. putoria, compared to Universidade Estadual Paulista, Botucatu, São 15% on C. megacephala (Table). There was no Paulo, Brazil. Adult were maintained at 25 ± predation in 12.5% of the vials. These three rates 1oC in cages (30 X 30 X 30 cm) covered with ny- were significantly different (χ2 = 25.36; d. f. = 2; lon and were fed water and sugar ad libitum. Adult P < 0.05). Considering only the predation cases, females were fed fresh beef liver to permit the com- 82.9% was on C. putoria and 17.1% on C. plete development of the gonotrophic cycle. megacephala. The χ2 test indicated that there was Hatched larvae were reared on an excess of ground significant difference between these predation rates beef until the third instar in all species studied, (χ2 = 13.83; d. f. = 1; P < 0.05). when they were taken and introduced in empty vials Our results suggest that, when C. macellaria is (7 cm height x 6 cm diameter) to estimate preda- absent C. albiceps larvae attack more C. putoria tion rates in different combinations. Larval instar than C. megacephala larvae. In a recent paper, Faria was determined by using accepted morphological et al. (1999) investigated larval predation by C. characters used to separate the various develop- albiceps on C. macellaria, C. megacephala and C. ment stages of blowflies (Prins 1982, Greenberg putoria. In choice experiments, where all species & Szyska 1984, Erzinçlioglu 1987, 1990,Tantawi were confined together, C. albiceps killed C. & Greenberg 1993, Queiroz et al. 1997). macellaria at a larger rate than C. megacephala Predation rates were evaluated in a two-choice and C. putoria. When species were confined in experiment, confining one C. albiceps with pairs, no choice experiment, C. albiceps predated two larvae, one of C. putoria and one of C. all species practically at the same rate, indicating megacephala. Forty vials were prepared for each there is no preference for a specific prey if the combination, and placed on a lighted laboratory predator larvae has no choice of species (Faria et bench at 25oC. The larvae were continually scanned al. 1999).

TABLE Predation rates by Chrysomya albiceps in a two-choice situation with C. megacephala and C. putoria as the choices Time interval Chrysomya putoria (min) Predation Cumulative Predation Cumulative 15 10 10 32.5 32.5 30 0 10 5 37.5 45 2.5 12.5 10 47.5 60 2.5 15 17.5 65 75 0 15 2.5 67.5 90 0 15 5 72.5 105 0 15 0 72.5 120 0 15 0 72.5 Total 15 15 72.5 72.5 Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 96(6), August 2001 877

The flexibility of C. albiceps in relation to somya species and C. macellaria occurs (Reis et choice of larvae observed both by Faria et al. (1999) al. 1999). These results have brought important and and in this study, suggests that its predatory be- interesting questions and answers, which have havior can be changed as a function of prey avail- motivated new studies. Biological invasions like ability. In natural settings the coexistence of dif- this are very complex phenomena and demand ferent species of blowflies in the same substrate is careful examination of all aspects involved. The not uncommon (Kneidel 1984a,b, Hanski 1987, results obtained up to now have helped us to un- Wells & Greenberg 1994) therefore, larvae of C. derstand part of the mechanism involved in the albiceps probably have a choice of prey. invasion and colonization processes, but more stud- Diet preference has been investigated in Co- ies focussing larval behavior, interspecific inter- leoptera from an evolutionary perspective, since actions, and frequency distribution of species are coccinellids exhibit considerable diversity in habi- necessary to evaluate in detail the current situation tat, dietary preference, and specificity (Sloggett & of Brazilian necrophilic fauna structure. Majerus 2000). Feeding in atypical habitats, on ACKNOWLEDGEMENT alternative food, when optimal prey is scarce, is likely to be a factor of major importance in evolu- To the anonymous reviewer for useful comments tionary shifts towards novel diets and habitats and suggestions which improved the clarity and content (Sloggett & Majerus 2000). The incorporation of of the manuscript. a new kind of prey may occur frequently, as a func- REFERENCES tion of main prey scarcity (Hodek 1996). Baumgartner DL, Greenberg B 1984. The genus Chry- Different predators may adopt different strate- somya (Diptera: Calliphoridae) in the New World. J gies to utilize food resources. Optimal foraging Med Ent 21: 105-113. theory explains how foragers, maximizing their net Brewer R 1994. The Science of Ecology, 2nd ed., energy intake, can do this in different types of prey Saunders College Publishing, Ft. Worth, 773 pp. environment (Stephens & Krebs 1986). How indi- Calow P 1994. 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