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Priority Effects on the Life-History Traits of Two Carrion Blow fly (Diptera, Calliphoridae) Species

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Priority Effects on the Life-History Traits of Two Carrion Blow fly (Diptera, Calliphoridae) Species Ecological Entomology (2014), DOI: 10.1111/een.12128 Priority effects on the life-history traits of two carrion blow fly (Diptera, Calliphoridae) species ADRIENNE BRUNDAGE,1 MARK ERIC BENBOW 2 andJEFFERY K. TOMBERLIN1 1Department of Entomology, Texas A&M University, College Station, Texas, U.S.A. and 2Department of Entomology and Department of Osteopathic Medicine, Michigan State University, East Lansing, Michigan, U.S.A. Abstract. 1. Third instars of the invasive blow fly Chrysomya rufifacies are facultative predators on larvae of the native blow fly Cochliomyia macellaria. 2. The effects of priority arrival time on the survivorship and fitness of C. rufifacies and C. macellaria were investigated in laboratory experiments. 3. Cochliomyia macellaria colonising a resource within 1–2 days after C. rufifacies resulted in a 20–70% reduction in survivorship, pupal weight and fecundity compared with those colonising a resource more than 2 days before or after C. rufifacies.Inversely, C. rufifacies exhibited a 50% increase in survivorship and fecundity when closely (∼2 days) associated temporally on the resource with C. macellaria and was negatively affected by disparate arrival. 4. These results demonstrate that arrival sequence significantly affects the fitness of both C. rufifacies and C. macellaria. Early colonisation may allow C. macellaria to persist in a community, while there are fitness benefits for C. rufifacies colonising after C. macellaria. 5. The 60% reduction in C. macellaria survivorship when in close temporal association with C. rufifacies may act as an agent of selection for C. macellaria to colonise a resource early and develop quickly to avoid predation on resources colonised by C. rufifacies. 6. Selection for such traits may explain how C. macellaria is able to persist despite intraguild predation by this invasive species. In contrast, the 50% increase in survivorship and fecundity exhibited by C. rufifacies when arriving after C. macellaria may select for C. rufifacies to delay colonisation. Key words. Chrysomya rufifacies, Cochliomyia macellaria, forensic entomology, interspecific competition, intraguild predation. Introduction 1971; Beaver, 1984; Shorrocks & Bingley, 1994; Hodge, 1996). Competitively inferior species exploiting resources before Patchy distribution of exploitable resources is widespread patch invasion by more competitively dominant species may throughout nature, and interspecific competition for such survive and consequently persist in an environment (Schoener, patches is often intense. Species’ colonisation patterns have 1974; Hodge, 1996). For example, offspring of Drosophila been considered random or governed by individual physiology sp. (Diptera, Drosophilidae) arriving to Instant Drosophila (Hodge, 1996). A temporal disparity between ecologically Medium (IDM) was significantly earlier than ecologically similar species may confer a competitive advantage to primary similar species, had a 35% increase in survivorship, a 22% colonisers under exploitative competition circumstances. An decrease in developmental time, and a 17% increase in adult early coloniser is relatively unaffected by the presence of size when compared with those resulting from adults arriving later species, but resource depletion may be a detriment to later (Hodge, 1996). This ‘priority effect’ (Alford & Wilbur, later-arriving conspecific or interspecific individuals (Bryant, 1985) has been documented in other systems, such as fish (Geange & Stier, 2009), crustaceans (Irving et al., 2007) and Correspondence: Jeffery K. Tomberlin, Department of Entomology, amphibians (Eitam et al., 2005). In each case, early-arriving Texas A&M University, 2475 TAMU, College Station, TX 77845-2475, species gained a fitness advantage by exploiting a patch before U.S.A. E-mail: [email protected] a competitor arrived. However, priority effects have not been © 2014 The Royal Entomological Society 1 2 Adrienne Brundage, Mark Eric Benbow and Jeffery K. Tomberlin examined in detail for blow flies (Diptera, Calliphoridae) that As C. macellaria and C. rufifacies larvae exploit carrion as often colonise discrete resource patches – carrion. their primary resource, they are considered direct competitors Priority effect may be responsible for the coexistence of (Kneidel, 1984a; Baumgartner, 1993; De Jong, 1997). Studies competing Calliphoridae on a carrion resource (Denno, 1975; documented competition among carrion flies in the field (Denno, O’Flynn, 1983; Schoenly, 1992). Primary colonisers of car- 1975; Denno et al., 1995; Archer & Elgar, 2003), and in rion tend to exhibit efficient detection, location and colonisa- experimental caged populations illustrated that some species tion (Tomberlin et al., 2011a,b), along with rapid feeding and regularly outcompete others to the point of extinction (Hanski growth while on the resource (Beaver, 1984). These traits lead & Kuusela, 1977). However, these results do not completely to carrion colonisers arriving at a patch early in the decomposi- apply to C. macellaria and C. rufifacies, as both species tion process and consuming the maximum amount of resource continue to persist in the southern U.S.A. The objective of before competitors arrive (Schoenly, 1992). Secondary colonis- this study was to determine the priority effects between C. ers must contend with reduced nutrient value and high com- macellaria and C. rufifacies larvae on liver. These effects petitor diversity (Beaver, 1984). Natural selection would seem- on each species were determined by measuring the impact ingly therefore favour the earliest and most efficient colonis- of temporal variation in colonisation on the fitness-related ers of a carcass (Kneidel, 1984a,b). Secondary colonisers of life-history traits of survivorship, pupal weight, adult longevity carrion require an advantage over those already in residence and egg production of resulting adults. (Lane, 1975). Two common hypotheses about such an advan- tage are that: (i) the species must be an inferior competitor when in direct competition with other species on a resource Materials and methods (Atkinson & Shorrocks, 1981); or (ii) the species requires the resource to be modified by early colonisers in a way that Laboratory colonies of C. rufifacies and C. macellaria larvae enhances the fitness of the secondary colonising species (Lang used in this study were initiated from flies collected in Bra- zos County, Texas, U.S.A., during spring and summer of 2009 et al., 2006). and 2010. Larvae were reared on fresh bovine liver provided Central Texas has 10 commonly occurring species of Cal- ad libitum in 3-litre plastic containers (Sterilite Corporation, liphoridae that naturally colonise and feed on decomposing Townsend, Massachusetts) housed in a walk-in growth chamber animal tissue of carrion (Tenorio et al., 2003) and are consid- at 27.0 ± 1.0 ∘C, 60.0% RH, and with a LD 12:12 h photoperiod. ered a major part of the necrobiome (Benbow et al., 2013). Dispersing third-instar larvae were transferred to 3-litre contain- Of these, Cochliomyia macellaria (Fabricius) and Chrysomya ers with autoclaved sand (Town & Country Landscape Supply rufifacies (Macquart) are the most abundant species during the Co., Chicago, Illinois) for pupation. Resulting adults were main- warm months of the year (Goddard, 1988; Tenorio et al., 2003; tained in 30 × 30 × 30 cm3 cages (Bioquip Products, Rancho Bucheli et al., 2009). Cochliomyia macellaria is native to the Dominguez, California) held in the growth chamber previously New World (Baumgartner, 1993) with a distribution from south- described. Granulated sugar (Imperial Sugar Co., Sugar Land, ern Canada, throughout the U.S.A., Mexico, Central America, Texas), buttermilk powder (Saco foods Inc., Middleton, Wiscon- and as far south as central Argentina. Cochliomyia macellaria is sin), and water were provided ad libitum, and 20 g of bovine liver a primary coloniser of vertebrate carrion arriving early (within was placed in the cage between 4 and 15 days post-emergence minutes in some cases) in the decomposition process (Tomber- for 4 h to induce oviposition as needed. lin & Adler, 1998). Large collective egg masses may result in Collected eggs were homogenized prior to placement in treat- > 2 1000 larvae cm in large, aggregate masses, which can quickly ments and controls. For mixed species treatments, 100 eggs consume a carcass or cadaver (Laake et al., 1936; dos Reis et al., (determined gravimetrically) of the pioneer species were intro- 1999; Slone & Gruner, 2007; Oliveira & Vasconcelos, 2010). duced to 100 g of fresh bovine liver in a 20.5 × 34.5 × 20.5 cm Chrysomya rufifacies is native to Southeast Asia. It was intro- plastic tub with 1.5 litres of sand. Eggs were transferred using duced to Central America in the mid- to late 1970s (Baum- a camel hair paintbrush. The competing species (100 eggs per gartner, 1993), arrived in the U.S.A. by 1980 (Gagne, 1981), species) was introduced 0, 1, 2, 3 or 4 days after introduction and has become well established across North America, includ- of the pioneering species (Fig. 1). To ensure that results were ing southern Canada (Rosati, 2007). Chrysomya rufifacies acts not due to resource age, a pure culture of 200 eggs of each as a secondary coloniser of vertebrate carrion (Bohart, 1951; species independently (controls) was placed on liver aged 0, 1, Norris, 1959), with adults arriving within minutes after death 2, 3 or 4 days in the growth chamber under conditions described and suspected to colonise 1–2 days later (Baumgartner,
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