Ecological Entomology (2009), 34, 107–113 DOI: 10.1111/j.1365-2311.2008.01046.x Competitor-free space mediates non-target impact of an introduced biological control agent RUSSELL H. MESSING 1 and XIN-GENG WANG 2 1 Department of Plant and Environmental Protection Science, University of Hawaii at Manoa, Kapaa, Hawaii, U.S.A. and 2 Department of Entomology, University of California, Riverside, California, U.S.A. Abstract . 1. Enemy-free space has been shown to mediate host shifts in herbivores, but this has not previously been documented in parasitoids. Also, natural enemies shown to maintain host shifts have always been from higher trophic levels, rather than competitors. 2. In Hawaii, an Australian parasitoid ( Diachasmimorpha tryoni ) of medflies that loses competition contests to a subsequently introduced Asian parasitoid (Fopius arisanus ) has shifted its realised host range to attack non-target gall flies on lantana. 3. The present study demonstrates experimentally that D. tryoni reproduction is: (i) lower on medflies in coffee when F. arisanus is present than when it is absent; (ii) higher in gall flies on lantana than on medflies in coffee, when F. arisanus is present; and (iii) higher in medflies on coffee than in gall flies on lantana, when F. arisanus is absent. This meets Berdegue et al. ’s ( Ecological Entomology , 21 , 203 – 217, 1996) three conditions to confirm the importance of enemy-free space. 4. In the field, F. arisanus is abundant on medflies, whereas D. tryoni is rare on medflies, but is the dominant parasitoid of lantana gall flies. 5. Competitor-free space is thus shown to be a key mechanism maintaining an apparent host shift by an introduced biocontrol agent onto a non-target species. Key words . Biological control , enemy-free space , intrinsic competition , medfl y , non- target impact , parasitoid . Introduction Of the numerous parasitoids introduced against tephritid fruit fly pests in the islands, several have been documented to attack Biological control of invasive species using introduced natural ene- beneficial non-target species. Lethal intrinsic competition (i.e. mies has long been considered an environmentally safe and sus- between larvae of different parasitoid species within the same tainable form of arthropod pest management. However, recent host individual) has also been shown to occur ( Wang & Messing, studies have documented that imported predators and parasitoids 2003a ). sometimes attack non-target species, and occasionally lead to eco- The present study focuses on a complex tephritid host – parasitoid logical disruption ( Boettner et al. , 2000; Louda et al. , 2003 ). To system in Hawaii ( Fig. 1 ), in which competition between two date, little attention has been paid to the mechanisms underlying introduced biological control agents for a common resource this change in the realised host range of introduced natural enemies. appears to have led to a host shift in the inferior competitor. The While studies have shown the importance of enemy-free space in larval parasitoid Diachasmimorpha tryoni (Cameron), collected promoting host shifts of herbivores, where the shift involves escape in Australia in 1913 on its host Bactrocera tryoni (Froggatt), was from higher trophic level consumers ( Mulatu et al. , 2004; Murphy, brought to Hawaii for control of the Mediterranean fruit fly [med- 2004 ), neither the factors underlying parasitoid shifts among their fly, Ceratitis capitata (Wiedemann)]. It effectively reduced the phytophagous hosts, nor the possible role of competitors in the abundance of this pest on its major host crop, coffee ( Pemberton process have previously been well documented. & Willard, 1918; Willard & Mason, 1937 ). Subsequently, the Hawaii has been a focal point in the debate about non-target egg-attacking parasitoid Fopius arisanus (Sonan) was introduced impacts of biological control agents ( Messing & Wright, 2006 ). as a biocontrol agent for the invasive Oriental fruit fly, Bactrocera dorsalis (Hendel), and was reported to displace D. tryoni as the Correspondence: Russell H. Messing, University of Hawaii at Manoa, dominant parasitoid of medfly ( Clancy, 1950; Bess et al. , 1961 ). Kauai Research Center, 7370 Kuamoo Rd, Kapaa, HI 96746. E-mail: Soon thereafter, D. tryoni was reported to attack a non-target [email protected] beneficial tephritid, the lantana gall fly (Eutreta xanthochaeta © 2008 The Authors Journal compilation © 2008 The Royal Entomological Society 107 108 Russell H. Messing and Xin-Geng Wang F. arisanus D. tryoni general concept of ‘enemy-free space,’ where competition can egg parasitoid larval parasitoid be recognised to exert strong selection pressure on an inferior SE Asia Australia competitor. It was previously determined that F. arisanus prevails in in- trinsic competition against larval parasitoids (including D. try- oni ) within multi-parasitised host larvae, through physiological suppression of parasitoid egg development ( Wang & Messing, B. dorsalis C. capitata E. xanthochaeta 2003a ). To determine whether the non-target gall flies provide Oriental fruit fly medfly lantana gall fly competitor-free space, the present study experimentally tested Asia Africa Mexico the three hypotheses of Berdegue et al. (1996) . In addition, we obtained and reared samples from the field to test the hypothesis that D. tryoni would be relatively more abundant in gall fly in- fested lantana than in medfly infested coffee. Both laboratory Lantana camera and field results indicate that competitor-free space is a key Coffee and weed other fruits C & S. America mechanism maintaining the acquisition of a new host by an in- troduced biological control agent. Fig. 1. Partial food web showing origin, host stage attacked, and rela- tionships among a suite of exotic insects, all of which interact within Hawaiian agro-ecosystems. Materials and methods Field sites Aldrich), which itself was introduced from Mexico to Hawaii for control of the noxious weed Lantana camera ( Stone et al., 1992 ). The study was conducted on the island of Kauai, Hawaii. All The target (medfly) and non-target (gall fly) hosts differ greatly collections of wasps and flies for experimental colonies and all in their ecological habitats: medflies infest fruit tissues of a wide field surveys were conducted at the 1375-ha Kauai Coffee range of host plants, while the gall fly is specific to stem tissues Plantation (elevation 122 m), and at Kokee State Park (elevation of lantana. Adult gall flies lay eggs inside the growing tips of 500 – 1500 m). Both sites are located on the western side of the newly sprouted lantana shoots, and the larvae form green sphe- island, approximately 20 km apart, separated by sugarcane roid galls on stems, each gall containing a single larva. fields and pasture. The coffee plantation contains the greatest There has been no recorded occurrence of D. tryoni attack- reservoir of naturally occurring C. capitata in Hawaii ( Vargas ing any gall-fly species in Australia, its native region. Eutreta et al. , 1995 ), while E. xanthochaeta is mostly abundant in the xanthochaeta was never established in Australia for weed Kokee State Park area ( Duan et al. , 1998 ). control ( Julien & Griffiths, 1998 ), thus parasitism of this spe- cies by D. tryoni in Hawaii represents a new host association. Diachasmimorpha tryoni was established in Hawaii in 1913, Study organisms and E. xanthochaeta has been widely established here since 1902, but D. tryoni was not recorded as parasitising the gall All laboratory tests and rearing of flies and parasitoids were fly until 1950, 1 year after the introduction of F. arisanus conducted at the University of Hawaii Kauai Agricultural ( Clancy, 1950 ). We cannot be certain that parasitism of Research Center (KARC), Kauai, under laboratory conditions E. xanthochaeta by D. tryoni did not occur prior to 1950, only (22 ± 2 °C, 60 – 90% RH). Ceratitis capitata and F. arisanus that there are no published records of parasitism in a host in- were collected from the coffee plantation during September to sect that was deliberately released and monitored by State December, 2005. Ripe coffee fruits were collected and incu- entomologists. bated on wet tissue paper in Petri dishes in the laboratory. The Berdegue et al. (1996) suggested three tests to confirm the dishes were placed inside a screened fibreglass box importance of enemy-free space in maintaining an organism’s (45 × 3 0 × 15 cm) containing 2 cm of sand on the bottom for acquisition of a new host. First, the enemy’s impact on reducing fly pupation. Puparia were collected and placed into screened the organism’s fitness should be demonstrated in the original Plexiglas cages (30 × 3 0 × 30 cm), and newly emerged adult host or habitat. Second, the existence of a refuge should be veri- C. capitata and F. arisanus were separately maintained at ap- fied by showing increased fitness of the organism in the alter- proximately 50:50 sex ratios in cages with water and honey/ nate host or habitat; and third, the positive link between enemy yeast provided ad libitum . One to two week old female flies and impact and refuge should be confirmed by documenting de- wasps from the holding cages (sexually mature, and assumed to creased fitness of the organism in the alternate host or habitat have mated) were used for all tests. when enemies are absent. Conceptually, these tests are exactly Diachasmimorpha tryoni and E. xanthochaeta were collected the same whether one is examining a herbivore feeding on a from lantana plants in the Kokee